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The effects of electric, magnetic and electromagnetic fields on microorganisms in the perspective of bioremediation

  • Gabriele Beretta
  • Andrea Filippo Mastorgio
  • Lisa Pedrali
  • Sabrina Saponaro
  • Elena Sezenna
Open Access
Review Paper
  • 44 Downloads

Abstract

Some studies show how exposure to fields can enhance or reduce cell activity, with possible applicative consequences in the field of biotechnology, including biological techniques for depollution. In order to identify full-scale conditions that are suitable and potentially applicable for use in electromagnetic fields to stimulate and accelerate bioremediation processes, this paper offers an examination of the scientific literature that is available on the effects of fields on microorganisms, and a critical analysis of it. The biological effects at times contrast with each other.

Keywords

Electric field Magnetic field Electromagnetic field Bioremediation 

1 Introduction

The first studies on the influence of electromagnetism on organisms dates back to the end of the nineteenth century, to then intensify in the following decades after global electrification and the diffusion of telecommunication. The massive introduction into daily life of technologies that emit electric, magnetic and electromagnetic fields in an enormous range of frequencies and intensities led institutions and the scientific community to question itself about the effects on public health and the environment. Pertinent scientific literature is very vast and includes studies that vary greatly on the type of field, intensity, exposure duration, long-/short-term effects and considered biological targets (cell, tissue, organ and organism).

In contrast to the studies indicated above, the research that investigates the field effects on microorganisms is very limited. Model microorganisms, well characterised with genetic markers, were used in medical-health research to better understand the field action mechanisms. Some of these works showed how, in some situations, exposure to electromagnetic fields tends to enhance rather than reduce cell activity, with possible applicative consequences in the field of biotechnology, including biological techniques for depollution.

In order to identify full-scale conditions that are suitable and potentially applicable for use in electromagnetic fields to stimulate and accelerate bioremediation processes, this paper offers an examination of the scientific literature that is available on the effects of fields applied on microorganisms, and a critical analysis of it. In consideration of the objective of this document, aimed at environmental bioremediation, the effects of electromagnetic fields applied on cells, bacterial cells in particular, are focused on. The information obtained from the literature that was consulted is summarised in Tables 1, 2 and 3, respectively on nominal exposure to electrostatic fields/fields generated by direct current (DC), magnetic and electromagnetic currents/fields generated by alternate current (AC). The decision was made to treat electrostatic field applications (typically generated while maintaining a constant voltage between pairs of electrodes) together with fields generated by direct current because when the sources are applied to dielectric means (soil, wastewater, etc.) they produce similar effects. These effects are, in fact, so similar that even in most of the literature that was analysed, they are treated simultaneously, without any distinction between the two situations.
Table 1

Summary of the data of the consulted literature, in order of author, on the effects of the application of direct currents and/or electrostatic fields

Culture

Current

Field

Exposure duration

Setup and field source

Biological effect

References

Aerobic or anaerobic sludge

10–40 mA

 

12–24 h

Direct current applied to a reactor of 0.5 l through two carbon electrodes (approx. 50 cm2 each)

Inhibition of phenol degradation, both in aerobic and anaerobic conditions; reduced biomass growth (− 40%); reduced ATP levels. Effects due to pH lowering. No variation was seen at 5 mA, even in the pH value

− (indirect)/=

Ailijiang et al. (2016)

Activated sludge

 

0 V/m, 0.28 V/m, 0.57 V/m, 1.14 V/m

50 h

Aerated and mixed reactor, 2 l, with electrodes

At 28 V/m there were no effects on COD removal

−/=/+

Alshawabkeh et al. (2004)

At 57 and 114 V/m stimulation of biological activity

At 114 V/m, after 24 h, decrease in the COD removal rate

28–114 V/m was the optimal “window” for biomass stimulation

Escherichia coli, Listeria innocua, Leuconostoc mesenteroides

 

2500–3500 kV/m

20–40 pulses of 2–4 µs, at frequency of 250 pulses/s

Continuous system, with six tubular treatment chambers (∅ 0.22 cm) in serial. Electrodes mounted externally on each chamber and distant 0.23 cm from each other

Microorganisms’ inactivation increasing with the electric field intensity, duration and number of applied pulses. Even though with negative effects on all the species examined, a different susceptibility was noted, with L. innocua and L. mesenteroides being more resistant than E. coli

Aronsson et al. (2001)

Escherichia coli, Listeria innocua

 

500–1000–2000–2500–3000 kV/m

20–40 pulses of 2–4 µs, at frequency of 250 pulses/s

Continuous system, with six tubular treatment chambers (∅ 0.22 cm) in serial. Electrodes mounted externally on each chamber and distant 0.23 cm from each other

No significant effect on L. innocua at all intensities with pulses of 2 µs, reduction by one order of magnitude of the vital cells with 4 µs and fields > 2000 kV/m, with effects increasing as the field intensity increased. E. coli had negative effects in all the tested conditions, with a reduction of 5 sizes in the number of vital cells when exposed to fields ≥ 1000 kV/m and pulses of 4 μs or ≥ 1500 kV/m and 2 μs

=/−

Aronsson et al. (2005)

Denitrifying mixed culture

1 mA

 

70 h

Current applied to a digester of 0.75 l by way of graphite, steel or copper electrodes

Stimulation of denitrification with graphite and steel electrodes, inhibition with copper electrodes

− (indirect)/+

Cast and Flora (1998)

P. aeruginosa

 

500 V/m with polarity reversal every 64 s

50 h

Flow chamber with 5 flat parallel steel electrodes, two of which (at the entry and exit points of the chamber) connected to each other, and the central one connected to the voltage generator

The electric field caused a temporary reduction in the biomass of about 40% during the first 24 h of exposure; in the following 24 h biomass growth was observed, but remained about 2 orders of magnitude smaller than the control at the end of the test. The electric field also reinforced the bactericidal effect of antibiotics

Costerton et al. (1994)

Escherichia coli

16–24 mA/cm2 (320–480 mA)

 

0, 5 min a 24 mA/cm2

Reactor (6 × 4 × 5 cm3) with 5 flat parallel titanium electrodes (5 × 4 cm2) placed 1 cm from each other

99.8% inactivation at 320 mA and exposure duration 2 min

Diao et al. (2004)

   

2 min a 16 mA/cm2

 

Inactivation increased as the current increased, even with shorter exposure durations

  

Mixed culture

Variable in the range 5.7–21.3 mA

100 V/m with polarity reversal every 6–12 h

15 days

Two electrokinetic cells, (a) (24 × 12 × 7 cm) and (b) (22 × 22 × 10 cm), containing soil contaminated by 2,4 dichlorophenol. Constant voltage applied, without and with cyclic inversion of the polarity, through cylindrical graphite electrodes (∅ 0.5 cm, 6 cm), in

Inhibition of bacterial activity with unidirectional field because of pH variations

− (indirect)/+

Fan et al. (2007)

    

 (a) 2 electrodes that distance 20 cm from each other, or

With polarity inversion every 6 h, good control of the pH and pollutant removal three times higher

  
    

 (b) 7 electrodes positioned in a hexagonal manner and with one at the centre (10 cm between the perimeter electrodes and the central one)

In the hexagonal configuration, the field resulted in a uniform distribution of the residual contaminant in the soil, but with lower degradation efficiencies when compared with the configuration with parallel electrodes

  
    

 (b-1) voltage applied between the central electrode and the perimeter ones, connected in parallel with each other, with polarity inversion every 6–12 h

With rotational field, removal higher in the central portion of the system and lower at the edges, with uneven residual pollutant distribution

  
    

 (b-2) voltage applied between the central electrode and one of those at the perimeter, with a change every 6–12 h

   

Denitrifying mixed culture

0–10 mA

 

520 days

Reactor with amorphous carbon anode and steel cathode surrounded by polyurethane foam colonised by a denitrifying biofilm

Nitrate removal efficiency between 0 and 100%, proportional to the applied current

+

Feleke et al. (1998)

     

Denitrification supported exclusively by the electrochemical production of H2

  

Nitrifying mixed culture

1.25–2.5 mA/cm2 (20–50 mA)

 

40 days

Moving bed batch reactor (365 ml) with flat electrodes (6.18 × 6.35 cm2, distant 1.4 cm from each other), titanium anode (thickness 1.4 mm) and steel cathode (0.7 mm)

O2 generated electrochemically used in nitrification

+

Goel and Flora (2005a)

Hydrocarbon-degrading mixed culture

 

100 V/m with polarity reversal every 5 min

100 days

Electrokinetic cell (100 × 100 × 25 cm3) filled with 100 kg of soil contaminated by hydrocarbons (450,00 mg/kg). 25 electrodes of cylindrical graphite (∅ 1 cm, 20 cm) positioned in rows, each row having 5 connected in parallel. Constant potential difference between one row of electrodes and the next one, with periodic inversion of the polarity

Positive correlation between hydrocarbon degradation and electric field intensity

+

Cheng et al. (2014)

  

2D field of 2–50 V/m

  

Modification in the soil microbe community

  

Sphingobium sp. UG30, pentachlorophenol-degrader

3.14 A/m2 (10 mA) constant or with periodic reversal

100 V/m

36–95 days

Soil microcosm (0.5 kg; cell 13 × 5.9 × 5.4 cm3) contaminated by pentachlorophenol (100 mg/kg). Graphite electrodes (5 × 5 × 0.8 cm3)

Better results on pentachlorophenol degradation with periodic field inversion

− (indirect)/+

Harbottle et al. (2009)

    

Tests (1) and (2) with electrodes in cathode chambers, separated by the soil with an ionic exchange membrane; purified water as the electrolyte; pH control at the cathode with acid dose (test 1) or with anolyte and catholyte mix (test 2)

With mono-directional field, scarce control of the pH and humidity. Biomass inhibition

  
    

Test (3) with electrodes directly in the soil; pH control with daily inversion of the current

   

Denitrifying mixed culture in soil

5–20 mA

 

5–9 days

Electrodes of steel (∅ 0.6 cm, 15 cm) and graphite (∅ 1.4 cm, 20 cm), distant about 45 cm from each other, inserted by 6.4 cm into columns (∅ 9.7 cm, 60 cm) of sandy soil

Stimulation of denitrification proportional to the circulating current. pH needs to be controlled

+

Hayes et al. (1998)

Mixed culture in soil

 

100 V/m, with or without periodic polarity reversal

50 days

Electrokinetic cell (26 × 14 × 8 cm3) filled with about 1 kg of soil contaminated by pyrene. Two pairs of cylindrical graphite electrodes (∅ 1 cm, 14 cm)

Degradation of pyrene and biomass at the end of the test higher than in the control system without electric field. Better results with periodic polarity inversion thanks to better control of the pH

+

Huang et al. (2012)

Sulfur-oxidizing bacteria (Thiobacillus ferrooxidans and mixed culture), Acidiphilium SJH

200 mA/cm2 (20 mA)

150 V/m

28–80 h (liquid phase test)

Flat platinum bioelectrodes inserted into cylindrical cones of plastic material and positioned on an orbital mixer

Inactivation of T. ferrooxidans and Acidiphilium SJH at low cellular density in the liquid broth. At high optic densities, the effect of the current was low and did not influence the Acidiphilium SJH

=/−/+

Jackman et al. (1999)

   

240–540 h (slurry test)

 

In a water-soil slurry (with silt at 5, 10, 30% by weight), the sulphur-oxidants showed an increase in metabolic activity (greater production of sulphates). Acidiphilium SJH in a 10% and 30% slurry showed an increased consumption of glucose. No increase in the metabolic activity of the ferro-oxidans

  

Burkholderia spp., 2,4 dichloroacetic acid degrader

0.89 A/m2 (8 mA)

max 47.3 V/m

 

Electrokinetic cell (22 × 7 × 4 cm3) filled with soil contaminated by 2,4-dichlorophenoxyacetic acid. Graphite fiber electrodes and steel mesh positioned at the ends of the cell

Positive effects on pollutant biodegradation because of electromigration

+

Jackman et al. (2001)

Thiobacillus ferrooxidans

20, 30, 40, 80, 120 mA

 

84 h

Direct current applied to two graphite electrodes positioned in a reactor with biomass and growth soil

Bacterial growth stimulation; better results with currents of 30 mA

=/+

Ji et al. (2010)

     

No significant effect at 80 mA and 120 mA

  

Mixed culture from soil contaminated by diesel

0.63 mA/cm2 (10 mA)

 

25 days

Soil (4 × 4 × 20 cm3) with implanted graphite electrodes

The modifications in the pH during electrokinetic treatment reduced the total number of microorganisms and the biodiversity. The use of EDTA as an electrolyte caused toxic effects on the biomass in the cathodic region, while dehydrogenasis increased near the anode and hydrocarbon biodegradation reached 60%. These effects were related with the variation in the pH value and the effect of the electric field

− (indirect)/+

Kim et al. (2010)

Staphylococcus aureus and Yersinia enterocolitica

10–20–30 mA

 

7 days

Current applied using titanium electrodes coated with platinum (∅ 2 mm), immersed in culture gel on Petri dishes with bacteria

Inhibition of growth in both bacterial strains in all the tested conditions. Growing concentrations of NaCl in the culture gel increased the inhibiting effect of the current

− (indirect)

Król and Jarmoluk (2014)

Mixed culture from soil

3.14 A/m2 (1 mA)

 

27 days

DC applied using graphite plate electrodes (5 × 5 × 0.8 cm3) in an electrokinetic cell (5.9 × 5, 4 × 13 cm3) filled with approximately 0.5 kg of soil

Composition and diversity of the bacterial community only minimally influenced by electrokinetic treatment. Significant variations at the end of the experiments, but only near the anode, and ascribed to the variations in pH

=

Lear et al. (2004)

Sphingobium sp. UG30

3.14 A/m2 (1 mA)

 

36 days

DC applied using graphite plate electrodes (5 × 5 × 0.8 cm3) in an electrokinetic cell (5.9 × 5, 4 × 13 cm3) filled with soil contaminated by pentachlorophenol (100 mg/kg)

At the end of the test, decrease in the microbial respiration rate and in the use of soil substrata, especially at the anode where the pentachlorophenol accumulated and the pH was more acidic

Lear et al. (2007)

Activated sludge

1.98 A/m2 (a 17, 7 V/m)

0–5, 9–11, 8–17, 7–29, 4–59 V/m

32–65 h

Aerated bioelectroreactor (21 × 30 × 20 cm3), with polypropylene elements as the supporting material for the bacterial biofilm and a pair of flat steel electrodes (20 × 15 cm2) positioned 17 cm from each other. Reactor supplied continually with synthetic wastewater containing phenol (1600–2800 mg/l)

At an intensity of 5.9 V/m, no significant effects were recorded in phenol removal, while stimulation of the biological activity could be seen between 11.8 and 17.7 V/m. Better conditions (removal + 30%) observed at 17.7 V/m. Higher fields resulted in a reduction in the degradation capacity of the phenol compared with the control, with almost complete inhibition of the biomass at 59 V/m

+/=/−

Li et al. (2006)

Staphylococcus epidermidis and Staphylococcus aureus

0.01–0.1 mA

 

16 h

Electrodes in a Petri dish with culture gel and microorganisms

Antibacterial effects caused by the formation and accumulation of H2O2 and Cl2 because of anodic and cathodic reactions

− (indirect to)

Liu et al. (1997)

Phenol-degrading bacteria

5–40 mA

 

9–12 h

Graphite electrodes immersed in a closed mixed beaker (250 ml), containing biomass in mineral medium and phenol as the only source of carbon

Currents < 20 mA did not induce significant modifications in the cellular walls; at 20 mA increase in the hydrophobicity and flattening of the cell form; at 40 mA increase in the negative electrostatic charge and reduction of adhesion to the surfaces, exudates increase (cellular membrane damaged)

=/−

Luo et al. (2005a)

     

Currents of 20 mA was the limit not to induce negative effects in the tested bacterial community

  

Phenol-degrading mixed culture

12 mA (max)

100 V/m monodirectional or with periodic polarity reversal every 1.5–3 or 12 h

10 days

Electrokinetic cell (24 × 12 × 10 cm3) with cylindrical graphite electrodes (∅ 0.5 cm, 12 cm) with silty sand contaminated by phenol (200 mg/kg)

With the monodirectional field, phenol removed by about 20% in 10 days; 46% removal with periodic polarity inversion (4 times higher than the control), which made it possible to contain variations in the pH and soil humidity, with positive effects on biodegradation

+

Luo et al. (2005b)

Phenol-degrading mixed culture

 

100 V/m with periodic polarity reversal every 1.5–3 or 12 h

10 days

Electrokinetic cell (24 × 12 × 10 cm3) with 1–4 pairs of cylindrical graphite electrodes (∅ 0.5 cm, 12 cm) supplied in rotation

Periodic polarity inversion at intervals of 1.5, 3 and 12 h increased the removal of phenol, with abatement respectively of 68%, 60% and 49% in the central portion of the system. The removal of phenol was relatively uniform for inversions every 1.5 and 3 h, while for intervals of 12 h it accumulated near both electrodes

+

Luo et al. (2006)

Diesel-degrading mixed culture

 

20–40–60–200 V/m

2–7 days

Flat Ti electrodes (2 × 12 cm2) immersed in a batch reactor of 2 l containing the biomass in mineral medium and diesel/glucose

Increased respiration rate in all the test conditions. The applied field seemed to help degradation of the most recalcitrant fractions of the hydrocarbon mixture

+

Mena et al. (2014)

Mixed culture

 

50; 100; 150 V/m with periodic polarity reversal every 24 h

14 days

Electrokinetic cell with clay contaminated by hydrocarbons (10,000 mg/kg)

The degradation of pollutants with application of the electric field was equal or better than the control in all the tests carried out, with better results for fields of 150 V/m. In these conditions, however, there was local inhibition of bacterial activity near the electrodes, probably because of the variations in the pH

=/+/− (indirect to)

Mena et al. (2016a)

Novosphingobium sp. LH128

 

50–60 V/m for the first 77 h, then 20–30 V/m till the end of the test

14 days

Electrokinetic cell containing 0.7 kg of soil contaminated by PAH, inoculated with Novosphingobium. Field applied through a pair of steel electrodes fixed in the soil

When compared to the controls (abiotic with electric field and biotic without electric field), greater degradation of phenanthrene in the inoculated cell, above all near the cathode and in the central portion of the cell. Results ascribed mainly to electroosmosis

+

Niqui-Arroyo et al. (2006)

    

To avoid excessive pH variations, recirculation of buffer solution

   

Seawater bacteria

0.5–2 A

 

100–2000 ms

Electrochemical cell with flat Pt electrodes (1 × 8 cm2), distance 1 cm

Reduction in the number of vital cells with substantial damage at cellular level. The effects were amplified by the high concentration of dissolved salts

Park et al. (2003)

Mixed culture from soil polluted with diesel

 

100–200 V/m

15 days

Cylindrical electrokinetic cell (∅ 120 cm, 30 cm) containing soil contaminated by diesel (20,000 mg/kg) in the central part and sand/gravel in the anodic and cathodic compartments, where graphite electrodes are fixed. To limit the pH variations, citric acid and a buffer solution were added to the electrolyte solution

Greater removal of pollutants with higher intensity field, however with marked reduction in the respiration rate and biodiversity

+/−

Pazos et al. (2012)

Mixed culture

Up to 20 mA

666–1500 V/m

22–100 days

Cylindrical cell (∅ 6 cm, 4.5–7.5 cm) containing 100–400 g of soil contaminated by organochlorine compounds. Platinum or steel electrodes, mounted on the covers of the cell; continuous circulation of water

Removal of 80% of hexachlorobutadiene, ascribable to electrochemical reactions, variations in pH and redox potential

+

Rahner et al. (2002)

Escherichia coli, Staphylococcus aureus, Micrococcus lysodeiktieus, Sarcina lutea, Bacillus subtilis, B. cereus, B. megaterium, Clostridium welchii

800–6100 mA/cm2

490–2500 kV/m

10 pulses of 20 s each

Flat graphite electrodes and cell for holding the bacteria in soil/culture gel. Apparatus equipped with water cooling system, to keep the temperature variation within 10 °C

High intensity electric fields caused irreversible damage to the cells and killed the bacteria. The bacterial death rate increased in proportion with the intensity of the applied field and the overall duration of exposure, even though the different species had different sensitivities. Duration and number of pulses were not significant parameters. Effects related to increases in temperature and electrolysis were excluded

Sale and Hamilton (1967)

Enterobacter dissolvens

5, 10, 20, 100 mA

 

25 h

Batch reactors (100 ml) containing biomass in growth medium with glucose as a carbon source. DC applied through platinum electrodes (wires ∅ 0.3 mm) or saline bridges (KCl in agar)

In the case of electrodes with saline bridge, very limited effects (< 5%) on biomass growth or on the enzymatic activity of the bacteria, at least up to currents of 20 mA (reactions of electrolysis at the electrodes were not observed and the small differences compared to the control were ascribed to the increase in temperature of 0.5 °C in the DC system)

+/−

She et al. (2006)

     

With Pt electrodes, stimulation of the bacterial growth and dehydrogenasis activity during the exponential growth phase, ascribed to H2 and O2 produced by electrolysis at 10 mA, while in the stationary phase there was an increase in the bacterial death rate, probably related to the accumulation of intermediate radicals (OH· and O2·) of the anodic reactions

  
     

Currents of 20 and 100 mA inhibited bacterial growth

  

Sphingomonas sp. LB126

10.2 mA/cm2 (240 mA)

100 V/m

40 min

Titanium-iridium electrodes in cuvettes (8 × 8 × 3 cm3) containing biomass suspended in the culture broth

Increase (+ 40%) in the levels of ATP, without other significant effects at a cellular level (membrane integrity, chemical–physical properties of the cell surface, cultivability and fluorene biodegradation rate)

=

Shi et al. (2008)

Mixed culture

 

46 V/m

90 days

Six anodes positioned in a circle around the cathode (anode–cathode distance: 2.5 m)

Stimulation of PAH biodegradation, mainly because of increased soil temperature

+

Suni et al. (2007)

Escherichia coli, Bacillus cereus

5, 10, 20, 40 mA

 

72–192 h

Direct current with polarity inversion every 60 s, applied through a pair of graphite or copper electrodes in a cylindrical beaker containing microorganisms in the culture broth

With copper electrodes, inhibition in all the tested conditions. With graphite electrodes, no significant effects on E. coli growth at 5–10 mA; at 20–40 mA, inhibition of bacterial activity with a reduction in the ATP and enzymatic activity. At low currents, no effects on B. cereus growth and on the metabolic activity; at 40 mA, stimulation of growth, increase of ATP and stimulation of the activity of some enzymes

−/=/+

Valle et al. (2007)

Aspergillus niger

Up to 0.42 mA/cm2 (8 mA)

35 V/m

24 h

Direct current applied to electrodes coated in titanium oxide and covered with 15 g of perlite

The degradation of the hexadecane, after 8 days, was greater in comparison with the control; however, a reduction (− 52%) in the cell growth rate was observed

+

Velasco-Alvarez et al. (2011)

Heterotrophic bacteria from membrane of a MBR system

3.7–24.7 A/m2 (30–200 mA)

 

4 h

Direct current applied to two aluminium electrodes

The  % of death was not significant at 3.7 and 6.2 A/m2, was 15% at 12.3 A/m2 and 29% at 24.7 A/m2

=/−

Wei et al. (2011)

     

For values above 12.3 A/m2, the pH increased to 10, with potential negative effects on vitality

  

Mycobacterium frederiksber-gense LB501T e Sphingomonas sp. L138

 

200 V/m

60 min

Titanium-iridium electrodes (10 × 4 cm2, thickness 1.5 mm) immersed in electrode chambers (2 × 7 × 3.5 cm3) located at the ends of a chamber (35.5 × 4 × 3.5 cm3) filled with saturate soil. By-pass channel (35.5 × 2 × 3.5 cm3) hydraulically connected with the electrode chambers

No effect on the anthracene biodegradation rate

=

Wick et al. (2004)

Pseudomonas putida PpG7 (NAH7) and mixed culture

1 mA/cm2 (16 mA)

140 V/m

34 days

Constant voltage applied through titanium-iridium electrodes located in a mesocosm (40 cm × 4 cm × 4 cm), made up of two electrode chambers at the ends and a central treatment cell filled with water-saturated soil

No significant effect on the cellular membrane of P. putida. No significant effect on the physiology and composition of the bacterial community of the soil, except for the areas near the electrodes, where the effects were ascribed to variations in the pH

=

Wick et al. (2010)

Hydrocarbon-degrading mixed culture

 

130 V/m constant or with polarity reversal

25 days

Electrochemical cell with soil contaminated by cyclododecane (1000 mg/kg). Constant intensity field, also with periodic polarity inversion

The cyclohexane degradation pathway did not change. The degradation rate increased, in particular in tests with polarity inversion; at the end of the test with electric field, degradation was 79.9% and 87.0% without and with polarity inversion, respectively, in comparison with 61.5% without electric field

+

Yuan et al. (2013)

Mixed culture

 

130 V/m

42 days

Microcosms with soil

Stimulation of biodegradation and increase (+ 20%) in the biomass in comparison with the control

+

Yuan et al. (2013)

Nitrifying or denitrifying activated sludge

4.4–14 mA

1.2–2.5 V/m

36 days as 4 periods of 9 days each, the first and the third of which without electric field

Electrochemical cell (15 × 5.5 × 17 cm3) filled with glass balls and graphite grains (1:5 in volume) and 0.5 l of wastewater; current applied through flat graphite electrodes (8 × 15 cm2) colonised by nitrifying and denitrifying biomass

Nitrification and denitrification were simultaneously observed. Removal rates higher for voltages of 0.4 V. Controlling the dissolved oxygen was critical for process efficiency

+

Zhan et al. (2012)

S. aureus, E. coli

0.1–0.5 mA

< 3; 4–27 V/m

24 h

Two pairs of gold electrodes positioned perpendicularly to Petri dishes containing biomass and connected or not to a DC generator

No significant effect on E. coli, reduction of growth of S. aureus in all the tested conditions (alterations in the cellular morphology, membrane breakage and loss of cellular organisation). For fields > 10 V/m, marked reduction in the number of cells around the anode

−/=

Zituni et al. (2014)

Effect: − negative; + positive; = null

Table 2

Summary of the data in the literature, reported in alphabetical order, on the effects of magnetostatic fields (MSF)

Culture

Field

Exposure duration

Setup and field source

Biological effect

References

Pseudomonas and Enterobacter

0 (annulment of the geomagnetic field)

6 days

Helmholtz coils to cancel the geomagnetic field

Resistance to antibiotics both increased and reduced, according to the strain and the antibiotic

+/−/=

Creanga et al. (2004)

    

Half of the strains that were tested did not result as being sensitive to MSF

  

Streptomyces marinensis

3, 7, 9, 10, 11, 15 mT

144 h

Permanent magnets

In all conditions, increase in growth and synthesis of neomycin (secondary metabolite) in comparison with the control

+

Ellaiah et al. (2003)

Shewanella oneidensis

14,100 mT

1.5–12 h

Permanent magnets

No significant effect on growth during the exponential growth phase, 21 genes over- and 44 under-regulated

=

Gao et al. (2005)

E. coli, S. aureus

500–4000 mT

2 h

Superconducting magnet

No effect on growth and resistance to antibiotics

=

Grosman et al. (1992)

E. coli

2000–5000 mT

48 h

Superconducting magnet

Effects of mutagenicity

?

Ikehata et al. (1999)

E. coli

7000 mT (constant in space); 5200–6100 mT (variable in space)

24–60 h

Superconducting magnet

Modifications in the activity of enzymes not involved in the attack of organic substrata (increase in the ratio between vital cells and total cells in the exposed samples in comparison with the control) with 60 h exposure; no effect up to 20 h

?/=

Ishizaki et al. (2001)

Pseudomonas stutzeri

0.6–1.3 mT

10 h (2 h in aerobiosis, 8 h in anaerobiosis)

Helmholtz coils (∅ 18 cm, 0.15 Ω)

No significant effect during the aerobic phase

=/+

Hönes et al. (1998)

    

During the anaerobic phase, stimulation of growth at 1.3 mT (+ 25–30% in comparison with the control) and 0.6 mT (+ 7%). Cellular replication accelerated, no increase in the specific production of nitrate-reductase

  

E. coli

7000 mT (constant in space); 5200–6100 mT (variable in space)

60 h

Superconducting magnet

Modifications in the activity of enzymes not involved in the attack of organic substrata

?

Horiuchi et al. (2001, 2002)

E. coli

45, 450, 1200, 1800, 3500 mT

30–60 min

Permanent Nd–Fe–B magnets

Reduced bacterial cell vitality during the exponential growth phase in all the examined conditions; the effect grew, as the field intensity, the exposure duration and temperature increased. In relation to the variations in the applied field intensity, inhibition did not progress monotonously (local min and max)

Ji et al. (2009)

Activated sludge

5, 20, 200, 500 mT

Up to 60 h

Permanent magnet

Magnetic fields of 5 or 20 mT had a positive effect on microorganism growth. Higher values had the opposite effect

−/+

Ji et al. (2010)

Streptococcus mutans, Staphylococcus aureus, Escherichia coli

30, 60, 80, 100 mT

48 h

Permanent ferrite magnet

Decreased growth rate in anaerobic conditions

−/=

Kohno et al. (2000)

    

No effect in aerobic conditions

  

Bacillus circulans, Escherichia coli, Micrococcus luteus, Pseudomonas fluorescens, Salmonella enteritidis, Serratia marcescens, Staphylococcus aureus

160 mT (constant in space); field variable in space:

24 h

Permanent ferrite magnets

No significant effect

=

László and Kutasi (2010)

 

 (1) max 477 mT, lateral gradient of 47.7 T/m

     
 

 (2) max 12.0 mT, lateral gradient of 1.2 T/m

     
 

 (3) max 2.8 mT, lateral gradient of 0.3 T/m

     

Activated sludge

7 mT

24 h

Reactor positioned inside a magnetostatic device

Increase in substratum removal

+

Łebkowska et al. (2011)

Microbacterium maritypicum

50, 100, 200 mT

5 days

Pair of cylindrical coils powered by transformer

Increase in the degradation of benzo(a)pyrene

+

Mansouri et al. (2017)

Bacillus licheniformis

10 mT

30 h

Solenoid and DC generator

Increased bacterial growth under controlled pH conditions. Increased bacitracin synthesis both in conditions with uncontrolled (+ 36%) and controlled (+ 89%) pH

+

Mohtasham et al. (2016)

Bacillus subtilis

7000 mT (constant in space); 5200–6100 mT (variable in space)

72 h

Superconducting magnet

No effect with uniform field at 7000 mT. For field variable in space, 50% reduction in the bacterial decay rate of the cells when the stationary growth phase was reached; spore formation inhibited

=/+/?

Nakamura et al. (1997)

Activated sludge

13 mT

12 h

Two parallel magnetic plates

Increase in substratum removal

+

Niu et al. (2013)

E. coli

7000 mT (constant in space); 5200–6100 mT (variable in space)

24 h

Superconducting magnet

In the stationary phase, significant reduction (40–80%) of the bacterial decay rate in the samples exposed to a uniform field, 2.7–3.6 times higher in the samples exposed to a non-uniform field

+

Okuda et al. (1995)

E. coli

7000 mT (constant in space); 5200–6100 mT (variable in space)

12 days

Superconducting magnet

Reduced bacterial decay rate during the stationary phase; the effect was temporary and terminated at the end of exposure

+

Okuno et al. (2001)

Serratia marcescens

8 mT

24–48 h

Permanent magnets

Growth inhibition

Piatti et al. (2002)

Rhodococcus erythropolis

50 mT

4 h

Electromagnet supplied with constant current

Cell growth and phenol degradation stimulation

+

Pospíšilová et al. (2015)

    

Increased adhesion between cells

  

E. coli

200–250 mT (variable in space)

12 h

Neodymium disc magnets

No effect in vivo

=/?

Potenza et al. (2004)

    

Punctual alterations of DNA in the in vitro tests

  

Geotrichum sp.

7, 17, 33 mT

24 h

Permanent magnet

7.0 mT promoted the growth of Geotrichum sp.; no effect at 17 and 33 mT

+/=

Qu et al. (2018)

Biofilters

30, 60, 130 mT

185 days

Two magnets placed at variable distances from the reactor

Increase of trichloroethylene biodegradation at 30 and 60 mT; opposite effect at 130 mT

+/−

Quan et al. (2017)

    

Acinetobacter, Chryseobacterium and Acidovorax significantly more abundant in the exposed systems

  

E. coli

8–60 mT

90 min

Permanent magnet of Fe oxides and ceramic

Increase in antibiotic resistance

?

Stansell et al. (2001)

Activated sludge

40 mT

20 days

Permanent magnet

Improved nitrification

+

Tomska and Wolny (2008)

E. coli

7000 mT (constant in space)

30 h

Superconducting magnet

During the first 6 h approximately (start of the log growth phase), slight reduction in the growth rate. During the stationary phase, significant reduction in the bacterial decay rate (at 30 h, number of cells in the exposed samples 2–3 times greater than the control). Effect more pronounced with exposure to non-uniform than to uniform fields

?

Tsuchiya et al. (1996, 1999)

 

5200–6100 mT (variable in space)

     
 

3200–6700 mT (variable in space)

     

Rhodobacter sphaeroides (anaerobic conditions)

130–300 mT

24 h

Permanent magnets

Slight reduction of growth and increase in the extracellular production of porphyrin (secondary metabolites)

Utsunomiya et al. (2003)

Anaerobic sludge, main species: Brevibacillus sp. and Bacillus sp. (Cr(VI)-reducing bacteria)

2.4, 6, 10, 17.4 mT

24 h

Addition of Fe3O4 in suspension

Increased biomass in all the tested fields. Better effects at 6 mT

+

Xu and Sun (2008)

Anaerobic sludge, main species: Brevibacillus sp. and Bacillus sp. (Cr(VI)-reducing bacteria)

4–40 mT

10 h

Pair of permanent magnets positioned inside or outside the sludge line

No problem at all the tested field intensities

+

Xu et al. (2009)

    

The 4 mT field resulted as being the most efficient for producing methane (70.7% more than the control)

  

Activated sludge

6–46.6 mT

40 h

Solenoid

Increased substratum removal in comparison with the control reactor, for a field from 8.9 to 17.8 mT. Opposite effect with higher field values

+/−

Yavuz and Çelebi (2000)

Biofilm at the anode of a fuel cell

20, 120, 220, 360 mT

800 h

Square magnet positioned outside the microbial cell near the anode

Biofilm more active up to 220 mT; opposite effect at 360 mT

+/−

Zhao et al. (2016)

Activated sludge

8.1 mT

24 h

Magnetic actuator made up of a ring containing a ceramic frit, permanently magnetised

Increased nitrification. Biomass growth stimulation (+ 14%)

+

Zielinski et al. (2017)

Effect: − negative; + positive; = null; ? undefinable

Table 3

Summary of the data in the literature, reported in alphabetical order, on the effects of electromagnetic fields

Culture

Frequency

Intensity

Exposure duration

Setup and field source

Biological effect

References

Escherichia coli

16–50 Hz (square wave)

0–22 mT

2–3 h

E-shaped AC electromagnet

Increased growth rate

+/=

Aarholt et al. (1981)

     

At 50 Hz the effect became evident at intensities between 0.48 and 0.8 mT; at 16.66 Hz between 0.8 and 1.5 mT

  

E. coli

50 Hz

0.2–0.66 mT

2–3 h

E-shaped AC electromagnet

Alterations in the synthesis of β-galactosidase, with a “window” reply (decrease from 0.27 to 0.3 mT; increase until up to about 0.56 mT; decrease beyond 0.56 mT). The intensity of the alterations seemed to depend also on the number of cells that were present, with more marked effects for lower cell concentrations

?

Aarholt (1982)

Staphylococcus aureus

2–500 Hz

0.5, 1.0, 1.5, 2.0, 2.5 mT

90 min

Two pairs of Helmholtz coils

Reduction in cell vitality in all the irradiated samples, with a reduction of at least 20% in all the magnetic flux density values tested for frequencies above 200 Hz

Ahmed et al. (2013)

     

The maximum CFU was recorded at 1.5 mT 300 Hz

  

E. coli

2–500 Hz

0.5, 1.0, 1.5, 2.0, 2.5 mT

< 60–90 min

Two pairs of Helmholtz coils

No effect with exposure lasting less than 1 h. For exposures of 90 min, reduction in the growth rate in all the irradiated samples. The effect grew exponentially as both the magnetic flux density and the frequencies increased. The maximum reduction of CFU (77%) was recorded at 2.5 mT 500 Hz

=/−

Ahmed et al. (2015)

Lactococcus lactis subsp. lactis

< 20 Hz (square wave)

5–20 mT

4–12 h

Three pairs of prismatic-shaped magnets positioned on the recirculation circuit of a fermenter

Increase in the production of nisin (secondary bacterial metabolite) for exposures at 20 mT for 4 h, without an increase in bacterial growth

?

Alvarez et al. (2006)

E. coli

50 Hz

0.5–1–2 mT

20 min

Pair of coils

Growth inhibition only at 2 mT

=/−

Aslanimehr et al. (2013)

Staphylococcus aureus

50 Hz

0.5–1–2 mT

20 min

Pair of coils

Significant reduction (up to 65%) of the growth rate at 0.5 and 2 mT; increase in growth at 1 mT for exposure of 20 min

+/−

 

Chromobacterium violaceum

50 Hz

0.66 μT

7 h

Electric line 5000 V

Slight alteration of the cellular proteome in the exposed samples

?

Baraúna et al. (2015)

     

The field probably acted as a stress factor

  

E. coli and S. aureus

20, 40, 50 Hz

2–4 mT

1–2–4–6 h

Electromagnetic dipoles (inductance 60 mH, resistance 0.45 Ω)

Significant CFU reduction in the exposed samples, especially for prolonged exposure duration. Maximum inhibition (95.2% for S. aureus, 85% for E. coli) at 4 mT 20 Hz for 6 h. Under the same magnetic flux density, S. aureus was inhibited even at lower values in comparison with E. coli

Bayır et al. (2015)

E. coli and Linfociti umani

2–24 Hz

0.2 mT

15 min

Helmholtz coils (1200-turn, ∅ 17.6 cm, 384 Ω each, inductance 251 mH)

Different mutations of the genotype according to the frequencies. DNA–protein complex alteration, in correspondence with the frequency window (9 and 16 Hz), specific for the different species

?

Belyaev and Alipov (2001)

E. coli

9 Hz

0.03 mT

15 min

Helmholtz coils (384 Ω, inductance 251 mH)

Temporary effects of DNA–protein complex alteration observed until 2 h after exposure to the field, evident only for initial densities ≥ 4 × 108 cell/ml (negligible effects for lower cellular densities)

?

Belyaev et al. (1998)

E. coli

60 Hz

1.1 mT

15 min

Helmholtz coils

Increased DNA transduction activity

?

Cairo (1998)

E. coli

50 Hz

0.1, 0.5, 1 mT

20–120 min

Copper cylindrical solenoid (∅ 170 mm, length 450 mm, 180 turn)

In the 24 h following exposure, greater vital/death cell ratio in relation to the control. Temporary morphotype change (higher number of spherical cells during exposure and partial return of the bacillus form in the following 24 h)

+/?

Cellini et al. (2008)

     

The magnetic field was a stress condition

  

E. coli

50 Hz

0.1, 0.4, 0.8, 1.2 mT

1 h

Helmholtz coils

Increased transduction activity at 1.2 mT

?

Chow and Tung (2000)

     

Increase in the efficiency of the DNA repair processes with exposure at 0.4, 0.8 and 1.2 mT (+ 20% in comparison with the control)

  

E. coli

50 Hz

0.1, 0.2, 0.5, 1 mT

58 h

Helmholtz coils

Reduced transposition activity; cell vitality stimulated. No cell proliferation or morphological variations

?

Del Re et al. (2003)

E. coli

50 Hz (sinusoidal wave)

0.05, 0.1, 0.2, 0.5, 1 (max dB/dt = 0.66 T/s @1 mT)

58 h

Helmholtz coils

No effect at 0.05 mT

=/?

Del Re et al. (2004)

     

At higher intensities, stimulated transposition activity and reduced cell vitality, with effects that increased in a linear manner with the field intensity

  
     

No cell proliferation or morphological variations

  

E. coli

50 Hz (square wave)

0.05, 0.1, 0.2, 0.5, 1 (max dB/dt = 0.14 T/s @1 mT)

58 h

Helmholtz coils

No effect at 0.05 mT

=/?

 
     

Reduced transposition at higher intensities; stimulated cell vitality in the stationary phase

  
     

No cell proliferation or morphological variations

  

E. coli, S. aureus

1, 5, 25, 50 Hz

22, 25, 29, 34 mT

1 h

Stator and three-phase squirrel-cage induction motor with glass beaker for housing the samples

Increase in the growth and metabolic activity of E. coli and S. aureus cells, with greater effects on E. coli than S. aureus

+

Fijalkowski et al. (2013)

     

Increase in the formation of bacterial biofilm, both for E. coli and S. aureus, at 25 Hz > 29 mT and 50 Hz 34 mT

  

Cocci (S.aureus, S. xylosus, S. mutans); Bacilli (E. coli, P. aeuriginosa, S. marcescens etc.); Coccobacilli (A. baumannii)

0.5–60 Hz

25, 34 mT

1 h

Stator and three-phase squirrel-cage induction motor with glass beaker for housing the samples

Increase in the growth and metabolic activity of E. coli, S. aureus, S. marcescens, S. mutans, C. sakazakii, K. oxytoca and S. xylosus cells; inhibition of A. baumannii and P. aeruginosa

+/−

Fijałkowski et al. (2015)

Gluconacetobacter xylinus

50 Hz

34 mT

144 h

Stator and three-phase squirrel-cage induction motor with glass beaker for housing the samples

Increase in the production of bacterial cellulose in the samples exposed to the field, without degradation of the characteristics of the cellulose produced in comparison with the control

+

Fijalkowski et al. (2016)

   

 (a) 72 h B = 34 mT + 72 h B = 0 mT

    
   

 (b) 72 h B = 0 mT + 72 h B = 34 mT

    
   

 (c) 144 h B = 34 mT

    

E. coliLeclercia adecarboxylata and S. aureus

50 Hz

10 mT

< 30 min; 1 h

Cylindrical coil

Decrease in the number of colonies in all the exposed samples

Fojt et al. (2004, 2009)

     

Greater effects on E. coli, while S. aureus was the most resistant species

  
     

No morphological alteration

  

E. coli

50 Hz

1 mT (6 mV/m)

8 min; 2.5–15 h

Helmholtz coils

No effect on bacterial growth and cell morphology

=

Huwiler et al. (2012)

Staphylococcus epidermidis, S. aureus, Enterococcus faecalis, E. coli, Klebsiella pneumoniae, Pseudomonas aeruginosa

50 Hz

0.5 mT

6 h

Helmholtz coils

Reduction in the growth rate during exponential growth that persisted even after exposure, except for Klebsiella, until the stationary conditions

Inhan-Garip et al. (2011)

     

Alterations in the cellular morphology in all species

  

E. coli

< 300 Hz

10–100 mT

1–12 h

Solenoid (on the recirculation line of a fermenter)

Contrasting results from the various experiments: proliferation or bacterial growth inhibition. Effects also on the cellular yield coefficient (biomass growth for unit of substratum removed)

−/+

Justo et al. (2006)

Corynebacterium glutamicum

15 Hz

2.4, 3, 3.4, 3.8, 4.2, 9 mT

8 h

Helmholtz coils

Increased ATP levels at between 2.5 mT and 4.4 mT (with max difference at 3.4 mT). Lower or higher intensities induced a drop in ATP

?

Lei and Berg (1998)

Corynebacterium glutamicum

10–70 Hz

3.4 mT

8 h

Helmholtz coils

Increase in the levels of ATP at 15–20 Hz (max + 20% in comparison with the control)

+

 
     

At 3.4 mT > 30 Hz, reduced levels of ATP (− 40% at 70 Hz)

  
     

Stimulation of bacterial growth after 4 h

  

Corynebacterium glutamicum

50 Hz

2.4, 4.2, 4.9, 6 mT

6 h

Helmholtz coils

ATP levels increased at 2.4–5.5 mT (max + 30% at 4.9 mT)

?

 

Corynebacterium glutamicum

30–70 Hz

4.9 mT

6 h

Helmholtz coils

ATP levels increased at 4.9 mT at 45–60 Hz (max + 40% at 50 Hz)

?

 

Corynebacterium glutamicum

50 Hz

4.9 mT

8 h

Helmholtz coils

ATP levels increased (+ 30%)

?

 

Escherichia coli, Proteus vulgaris, Photobacterium phosphoreum, Photobacterium fischeri

2–50 Hz

1–10 mT

7.5–15 h

Solenoid

Reduction (3–4%) of growth in the exponential phase at 4 mT 50 Hz for 7.5 h and 2 mT 50 Hz for 15 h

Mittenzwey et al. (1996)

E. coli

60 Hz

0.05 mT

8 h

Coil

Growth stimulation (decrease of the lag phase) and increase in the consumption of glucose

+

Nasciniento et al. (2003)

Bacillus subtilis

800 Hz (2 s on/2 s off)

0.8, 1.6, 2.5 mT

30 h

Helmholtz coils at a distance of 7.5 cm (∅ 160 mm, width 16 mm, 250 coils, inductance 15 mH)

Growth stimulation

+/?

Ramon et al. (1987)

 

1000 Hz (2 s on/2 s off)

   

Alterations in cell morphology and loss of intercellular cohesion

  

E. coli, Pseudomonas aeruginosa

50 Hz

2 mT

24 h

Helmholtz coils at a distance of 7.5 cm (∅ 130 mm, section 2 mm2, 800 coils, inductance 39 mH, resistance 2.4 Ω)

No significant effect on growth

=

Segatore et al. (2012)

E. coli

50 Hz

2.7–10 mT

12 min

Cylindrical coil, powered by current generator (50 Hz, 1.9 A effective value)

Reduced number of colonies, proportionally to magnetic flux density and exposure duration during the exponential growth phase

Strašák et al. (2002)

     

The redox activity decreased proportionally to the number of cells that were present (bactericide effect of the field but no effects on the bacterial metabolism)

  

E. coli, L. adecarboxylata, S. aureus, P. denitrificans, S. paucimobilis, R. erythropolis

50 Hz

10 mT

24 min

Cylindrical coil, powered by current generator (50 Hz, 1.9 A effective value)

Reduction in the number of cells

Strašák (2005)

Staphylococcus epidermidis, Staphylococcus aureus, Serratia marcescens and Escherichia coli

6–25 Hz variable in time (“Thomas pattern”)

2.1–5.1 μT

12 h

Resonator (cylindrical neodymium magnets rotating at 2000 rpm)

Increase in the growth rate of Staphylococcus epidermidis, Staphylococcus aureus and Escherichia coli, reduced growth of Serratia marcescens

+/−

Tessaro et al. (2015)

Monascus purpureus

50 Hz

0–2.5 mT

2–4–6–8 days

Five pairs of cylindrical coils powered by an AC generator (0–2 mA)

Exposure did not cause alterations in growth

=

Wan et al. (2017)

     

Reduction in the production of citrinin (toxic metabolite) at 1.2–1.6 mT; increased at 2 mT; no effect at 0.5–0.9 mT. The production of citrinin can increase, reduce or remain constant according to magnetic flux density, duration and exposure period; inhibition more evident with exposure during the initial growth phase

  

Salmonella typhimurium

60 Hz

14.6

4 h (5 min on, 10 min off)

Solenoid (972 copper coils) connected to an AC generator (60 Hz, 12 A)

No effect on DNA

?

Williams et al. (2006)

     

Greater resistance to stress co-factors (e.g. thermal shock)

  

Activated sludge

50 Hz (2 s on/2 s off)

17.8 mT

40 h

Solenoid (∅ 5 cm, 15 cm high)

Not significant effects with exposure to a pulsed field

=

Yavuz and Çelebi (2000)

Geobacter spp.

100 Hz

0.005

60 days

Outer coil of a single-chamber microbial fuel cell

Increase in the generated power density; increased abundance of Geobacter spp.

+

Zhou et al. (2017)

Effect: − negative; + positive, = null, ? undefinable

In consideration of the manuscript objectives, the effects indicated in the literature were divided into four different categories (“positive”, “negative”, “undefinable” or “null”) according to their possible implications on environmental bioremediation:
  1. 1.

    “positive” (+) effects: stimulation of the degradation of contaminants, increased denitrification/nitrification activity, acceleration of the substratum consumption kinetics, increase in the resistance to pollutants, increase of the biomass, increase in metabolic activity or in the activity of specific enzymes (e.g. dehydrogenases);

     
  2. 2.

    “negative” (−) effects: reduction of the degradation of pollutants and/or substratum consumption, inhibition of bacterial growth, reduction in metabolic activity or in the respiration rate, damage to the cellular membrane. At times, these effects are not tied to the direct action of the field/current on the cells, but rather to modifications in the environmental conditions (e.g. extreme pH values, electrochemical production of toxic species, radicals, etc.) (“indirect negative”);

     
  3. 3.

    undefinable (“×”): in the absence of effects (1) or (2), modifications in the activity of enzymes that are not involved in the degradative metabolism, variation in the concentration of ATP, modifications to the microbial community (structure/diversity/genotype/morphotype), effects of mutagenicity, alterations to the cell proteome, synthesis alterations of the DNA/RNA and correlated activities, variations in the transposition and production of secondary metabolites, modifications in the cell form and the characteristics of the cell wall and its electrostatic charge, increased cell hydrophobicity, increased adhesion between bacterial cells, increased or reduced resistance to antibiotics;

     
  4. 4.

    “null” (=): absence of significant effects on the aspects indicated above.

     

2 Electrostatic fields and fields generated by direct current

The first experiences in using fields that are electrostatic or generated by DC current to favour microbial growth date back to more than 50 years ago. They were based on the use of water hydrolysis to produce O2 electrochemically, as a replacement to other aeration systems, in order to grow Pseudomonas fluorescens (Sadoff et al. 1956 in Thrash and Coates 2008) or the combined production of O2 and H2 to grow the hydrogen-reducing aerobic microorganism Ralstonia eutropha H16 (Schlegel et al. 1965 in Thrash and Coates 2008).

2.1 Studies on microorganisms

Regarding the direct effects on microorganisms of the field that is electrostatic/generated by direct current, the literature indicates possible modifications in the physiology and form of the cells, the chemical–physical characteristics of the cellular membrane (Zimmermann et al. 1973) and membrane permeability and potential, with repercussions on its ability to exchange with the external environment, cell metabolism and mobility (Luo et al. 2005a; Golzio et al. 2004). The entity of these phenomena is a function of the species, but generally proportional to the intensity of the field/current applied and the duration of exposure. The results are stimulation of bacterial activity and increased cell mobility, observed in light intensity fields, as well as irreversible damage to the microorganisms, with a loss of membrane integrity, in the case of exposure to more intense electric fields (Sakakibara and Kuroda 1993; Satoshi et al. 1997; Chen et al. 2002; Diao et al. 2004; Zituni et al. 2014).

Even though different species present different levels of sensitivity, high intensity electric fields, for example of 1000 kV/m, or circulating direct currents of 1 A damage the cells irreversibly and cause the bacteria to die (Sale and Hamilton 1967; Park et al. 2003). Indeed, membranes that are exposed to an electric field become charged, in the same manner as a condenser, and this induces a potential transmembrane that, if greater than 1 V, causes cellular death. The bacterial mortality rate grows proportionally with the intensity of the field that is applied and the overall duration of exposure.

2.2 Studies in an environmental setting

Excluding extreme intensity values, a summary is given below of the environmental experiences carried out with modest intensity fields; this determines negative and/or positive effects, even contextual, on the microorganisms.

2.2.1 Beneficial effects

2.2.1.1 Electrochemical reactions

Electrochemical reactions, for example various electro-oxidations and water hydrolysis, can increase the availability of oxygen or hydrogen, respectively favouring aerobic biodegradation processes (Mena Ramírez et al. 2014) and anaerobic biodegradation processes (She et al. 2006).

Bioelectric systems based on water electrolysis were tested, in various configurations and with different operation parameters, for the removal of nitrogen from wastewater, mainly using the production of hydrogen at the cathode to promote denitrification reactions (Cast and Flora 1998; Feleke et al. 1998; Hayes et al. 1998; Mousavi et al. 2010, 2012), or oxygen at the anode to stimulate aerobic nitrification (Goel and Flora 2005a, b), or both processes simultaneously (Kuroda et al. 1996; Zhan et al. 2012). Variations in the pH and the production of H2 induced near the cathode by a current of 20 mA were used to stimulate the activity of sulphur-oxidising bacteria (Jackman et al. 1999). She et al. (2006), in a bioelectrochemical system with a current of 10 mA, stimulated dehydrogenase activity thanks to the simultaneous production of O2 and H2 at the electrodes.

In addition to water hydrolysis, other phenomena tied to electrochemical reactions were recently identified, such as the partial oxidation/reduction of pollutants, the release or removal of ions in solution, the possibility of adjusting redox potential for activating/stimulating the production of specific enzymes, as well as variations in bacterial metabolism (Aronsson et al. 2001; Li et al. 2006; Huang et al. 2012).

2.2.1.2 Electron exchange and enzyme production

Some microorganisms were able to use electroactive soluble substances (for example iron and humic substances) (Lovley et al. 1996) or solid electrodes (Bond et al. 2002; Gregory et al. 2004; Aulenta et al. 2009) as donors/acceptors of electrons for substrata oxidation/reduction. Zhang et al. (2013) affirm that in bioelectrochemical tests the electrochemical assistance provided the electrons and accelerated the electron transfer rate in the microbial reduction of 2,4-dichlorophenoxyacetic.

Zhang et al. (2014) observed an increase in the mineralisation efficiency of 2-fluoroaniline by an aerobic culture exposed to a direct current of 10–15 mA, as a result of the increased activity of the catechol dioxygenase and the selection of microorganisms with specific degradative abilities. Velasco-Alvarez et al. (2011), by applying a current of 8 mA for 24 h to a culture of Aspergillus niger, observed that the bacterial growth halved but that the hexadecane degraded more, causing the supposition of transition from an assimilative metabolism without the electric field to a non-assimilative one with the electric field.

2.2.1.3 Electrokinesis

Electrostatic fields generated by constant differences in potential (of the order of 100 V/m) applied between pairs of electrodes and fields generated by direct current are already being applied full-scale for decontamination with electrokinesis, to remove pollutants in sediments or soils (both saturated and unsaturated), especially if the particles are small (Acar et al. 1995).

The benefits of applying electric fields to soils/sediments were initially related to activated transport mechanisms (electroosmosis, electromigration, electrophoresis and dielectrophoresis) (Alshawabkeh and Bricka 2000). Electroosmosis is the movement of the liquids present in the soil pores, generally from the anode to the cathode, under the action of an electric field, which promotes the migration of pollutants towards the cathode by advection (Acar and Alshawabkeh 1993; Acar et al. 1995). Electromigration is the movement of ionic species caused directly by the electric field. Electrophoresis is the transport of solids with a charged surface, for example bacteria or clay, towards the electrode with the opposite pole, while dielectrophoresis is the movement of neutron solids with a diameter of between 1 and 1000 µm because of induced polarisation (Pohl et al. 1978). These mechanisms determine the movement of organic molecules, nutrients, fluids and bacterial cells (Luo et al. 2005b; Wick et al. 2007) with a faster recovery of pollutants, mass transfers and interactions between pollutants, bacterial cells and nutrients, which is advantageous for the bioremediation processes.

Electrostatic fields can also cause pollutants to degrade partially with an increase in their bioavailability/biodegradability (Wick et al. 2007; Yeung and Gu 2011; Gill et al. 2014; Moghadam et al. 2016). Increases in temperature because of ohmic losses can accelerate the kinetics of bioremediation (Suni et al. 2007).

Experiences of electrokinesis with electric fields having an intensity of 20–200 V/m (Wick et al. 2007; Gill et al. 2014) showed better degradation for various classes of compounds, among which petroleum hydrocarbons due to changes in the microbial community structure (Probstein and Hicks 1993; Pazos et al. 2012), polycyclic aromatic hydrocarbons due to the transport of PAH-degrading bacteria in the medium (Pazos et al. 2010), organochlorine compounds due to changes in pollutant mobility (Gomes et al. 2012), and phenols due to variation in bacteria hydrophobicity and pollutant mobility (Luo et al. 2005a, b).

2.2.2 Negative effects

On account of the variety of processes induced by the electrostatic fields or generated by DC currents, inhibitive effects on biological activity were reported, mostly related to: (1) important variations in the pH (Fan et al. 2007; Yeung and Gu 2011; Gill et al. 2014; Ailijiang et al. 2016), above all near the electrodes (Lear et al. 2004; She et al. 2006); (2) electrochemical reactions, with the production of reactive species of oxygen, chlorine or metallic ions, according to the species present in the system and the materials used for the electrodes (Liu et al. 1997; Li et al. 2011); (3) excessive heating because of ohmic loss (Palaniappan et al. 1992; Shi et al. 2008). Part of the research on these technologies focuses on investigating operation expedients for optimising the degradation processes and guaranteeing maintenance of optimal conditions for bioremediation (Jamshidi-Zanjani and Darban 2017). Approaches proposed for controlling the pH include, for example, the continual injection of electrolytes (Kim et al. 2005), anolyte and catholyte mixing (Rabbi et al. 2000), the use of buffer solutions (Niqui-Arroyo et al. 2006), the periodic inversion of the electric field polarity (Luo et al. 2005b; Guo et al. 2014; Mena et al. 2016a, b).

2.2.3 No effects

Some experiments with electrostatic fields of 100–200 V/m or applied/induced currents below 20 mA, typically bioelectrochemical and bioelectrokinetic treatments, excluded important field effects on the basis of biotransformation kinetics, evolution of the CO2, microbial charges or enzymatic activity (Jackman et al. 1999; Wick et al. 2004; Harbottle et al. 2009). Lear et al. (2004), for example, do not report any effect on the composition and structure of the microbial community of the soil following the application of direct current at 1 mA for 27 days, and attribute the variations observed near the electrodes only to the variations in pH. In Wick et al. (2004), exposure to DC currents did not cause Mycobacterium LB501T to have any effect on the degradation of some polycyclic aromatic hydrocarbons; in relation to the control experiment, the exposed microorganisms did, however, show levels of ATP that were higher by about 50%, even though without repercussions on the development of biomass and on the degradation speed of fluorine. Zanardini et al. (2002) refer to an increase of about 3 times the ATP content in a mixed culture in wastewater, after exposure for 10 days to direct currents of 40–200 mA. Luo et al. (2005a), studying the properties of the cellular membranes of phenol-degrading bacteria exposed to direct currents of different intensities, conclude that currents < 20 mA induce unimportant modifications in hydrophobicity, the electrostatic charge of the membrane and the cell form; on the contrary, currents of about 40 mA caused increases in the extracellular concentrations of cytoplasmic substances and cell flattening. Jackman et al. (1999) observed a temporary reduction in the growth rate of acidophilic bacteria subjected to a current of 20 mA for 80 h, due to bacteria membrane degradation close to the surface of the electrodes. Wei et al. (2011) indicate death rates of heterotrophic bacteria that were 10% lower than the control when exposed for 4 h to currents lower than 52 mA, and reductions of approximately 15% and 30% respectively for currents of 100 and 200 mA, due to pH variation close to the cathode surface.

Figure 1 sums up the experiences described in the literature and given in Table 1, divided in terms of categories of effects found following exposure to electrostatic fields (Fig. 1a) or fields generated by direct currents (Fig. 1b), even according to the exposure duration. As a result of the numerous experiences that refer to negative effects on microorganisms, not because of the direct action of the electric field but for the variations induced in the environment (for example variations in the pH), they are highlighted in the figures with a different colour, because using suitable expedients (buffer solutions, periodic polarity inversion) this type of undesired phenomenon can be limited and controlled. When considering the intensity of the electrostatic field, all the positive effects occur at values within about 1000 V/m; however, in the same range of values, even with short exposure duration, negative effects are found. With currents up to 10 mA, the effects are above all positive or at most negligible; the few negative effects are all indirect; for higher current intensities, especially above 150 mA, no positive effects can be seen.
Fig. 1

Type of effects observed according to the intensity of the electrostatic field that was applied (a) or the intensity of the current generated by an electrostatic field (b) and the exposure duration. The numeric label of each point associates it with the reference in Table 1. “Negative” effects (red filled triangle): reduction in the degradation of pollutants and/or substratum consumption, bacterial growth inhibition, reduced metabolic activity or respiration rate, damaged cellular membrane. “Indirect negative” effects (red times symbol): not tied to a direct action of the field/current on the cells, but rather to modifications in the environmental conditions (e.g. extreme pH levels, electrochemical production of toxic species, radicals, etc.); “Positive” effects (green filled diamond): stimulation of the degradation of contaminants, increased denitrification/nitrification, acceleration in the consumption kinetic of substrata, increased resistance to pollutants, increased biomass, increased metabolic activity or in the activity of specific enzymes (e.g. dehydrogenases); “Null” effect (blue filled circle): no significant effects on the aspects mentioned above. (Color figure online)

A scheme of the various phenomena resulting from the application of an electrostatic field or a field generated by direct current is shown in Fig. 2.
Fig. 2

Scheme of the various phenomena resulting from the application of an electrostatic field or a field generated by direct current: (1) hydrolysis resulting in O2 production (a) and H2 production (b); (2) partial oxidation (a)/reduction (b) of pollutants; (3) solid electrodes as electron acceptor (a)/donor (b); (4) increase in pollutant bioavailability; (5) modification in the physiology and morphology of the cell; (6) loss of membrane integrity, with release of cytoplasmic material and cell death; (7) increase in intracellular ATP concentration; (8) increase in the transport of organic molecules, nutrients, and bacterial cells due to electroosmosis, electrophoresis and dielectrophoresis; (9) transport of dissolved ions due to electromigration; (10) increase in temperature near the electrodes; (11) divergence of the redox potential from the environmental conditions; (12) pH variation close to the electrodes

3 Magnetostatic fields

Thanks to the relative simplicity of bacteria, using these organisms as models to examine the fundamental metabolic replies to magnetic fields should make it possible to reduce experimental result interpretation errors to a minimum. In spite of this, the data reported in the literature are often conflicting, and the action mechanisms not clear. A systematic approach, an analysis of the exposure-reply relationship, and physical, biochemical and physiological explanations (Letuta and Berdinskiy 2017) are missing from the majority of the studies that have been done.

3.1 Studies on microorganisms

Potenza et al. (2004) observed an increase in the ability of Escherichia coli to form colonies when exposed to a static magnetic flux density of 300 mT, as a function of the incubation medium. In Horiuchi et al. (2001), the number of E. coli cells during the stationary growth phase was 105 times higher when under the effect of a high intensity magnetostatic field (5.2–6.1 T) than when they were exposed only to the geomagnetic field.

Pospíšilová et al. (2015) showed how Rhodococcus erythropolis favours the use of phenol under a magnetostatic field of 50 mT.

Some studies demonstrate that the magnetic field can act on DNA stability, interacting with it directly or reinforcing the activity of oxidant radicals (Li and Chow 2001).

Gao et al. (2005) observed how a magnetic flux density of 14.1 T in Shewanella oneidensis stimulated the transcription of 21 genes on the one hand, and suppressed the transcription of 44 genes without causing substantial variations in growth on the other.

According to Kohno et al. (2000), static magnetic fields can induce the formation of the hydroxyl radical and amplify the negative effect of nitrogen oxide on the proteins-channels of the cellular membrane.

The mechanism of the radical pair (highly unstable species made up of two radicals) is considered as the most reasonable mechanism of interaction between weak magnetic fields and the biochemical systems (Steiner and Ulrich 1989; Woodward 2002). Each of the two radicals has an unpaired electron; the radicals can therefore be in the singlet state or the triplet state. The mechanism of the radical pair is present in three processes that are of fundamental importance for the cells: the enzymatic synthesis of ATP, the replication of DNA, and the enzymatic phosphorylation of the proteins (Buchachenko 2009, 2014; Buchachenko et al. 2012).

The Mg2+ ion, just like other ions (Ca2+ and Zn2+), participates in hundreds of enzymatic processes, many of which involved in fundamental biological mechanisms (Andreini et al. 2008; Rittié and Perbal 2008). The magnetic fields modify the interactions between these ions and the intracellular enzymes, in particular those involved in ATP synthesis (Buchachenko et al. 2012; Buchachenko 2016; Letuta and Berdinskiy 2017).

3.2 Studies in an environmental setting

Experiments were carried out on the application of static magnetic fields for treating wastewater in activated sludge systems, in relation to a potential improvement in solid–liquid separation during the sedimentation step. At times, an increase in the removal rate of the Chemical Oxygen Demand (COD), thanks to the production of more unsaturated fatty acids to stimulate the dehydrogenase activity (Niu et al. 2014), and of other compounds (Zaidi et al. 2014) were observed. In an aerobic activated sludge reactor exposed to a magnetostatic field, the overall content of biomass increased by more than 14% in comparison with a control reactor that was not exposed to the field (Zielinski et al. 2017). In Ji et al. (2010), the acclimation of the activated sludge and the removal of COD under the effect of a magnetic field up to 20 mT were stimulated in comparison with a control system; the same result appeared in Łebkowska et al. (2011) at 7 mT. Also in Yavuz and Çelebi (2000), the biological activity of the sludge was stimulated up to 17.8 mT; opposite effects were observed with higher intensities (46.6 mT). In Tomska and Wolny (2008), periodic exposure to a magnetic flux density of 40 mT increased nitrification.

In Zhao et al. (2016), the use of a magnetic field of 220 mT stimulated the activity of the biofilm at the anode of a fuel cell for treating wastewater, thanks to the production of more extracellular polymeric substance. With a magnetostatic field of 360 mT, instead, the opposite occurred due to harmful effects to microbial growth.

Xu and Sun (2008) presented the effect that magnetostatic fields at different intensities (2.4 mT, 6 mT, 10 mT, 17.4 mT) had on the treatment of wastewater that had been contaminated by Cr(VI), and in particular on Brevibacillus sp. and Bacillus sp. with Cr-reducing abilities. In all the cases, the quantity of microorganisms in the liquid medium was higher than the control (32–65%), with maximum abatement of Cr(VI) occurring when exposure was at 6 mT. On the sludge line, Xu et al. (2009) found an increase in the production of methane with exposures at 4 mT.

In Xu and Sun (2008), soil exposed to a magnetostatic field of 0.15–0.35 T had a higher respiration rate in comparison with the control. A magnetic flux density field of 7.0 mT instigated both the desorption of Cr(VI) and the growth of Geotrichum sp. in a soil column test (Qu et al. 2018).

In Mansouri et al. (2017), Microbacterium maritypicum, isolated from a contaminated lagoon, doubled the biodegradation rate of benzo(a)pyrene when exposed to a magnetic flux density of 200 mT.

Using biofilters to degrade trichloroethylene, exposed to magnetostatic fields of 30–60 mT, Quan et al. (2017) recorded more removal (+ 2.4%) than the control. The result was mainly ascribed to the differences in the bacterial community that developed, with relative abundances of Acinetobacter, Chryseobacterium and Acidovorax that were significantly higher in the exposed systems.

Figure 3 summaries the experiences described in the literature given in Table 2 in relation to exposure to magnetostatic fields, divided into categories of effects found, even according to exposure duration. The effects are classified into “positive”, “negative”, “null” and “undefinable”, as already reported previously. From an analysis of the data, the opportunity of containing the intensity of a magnetostatic field within 10 mT appears to be evident. Even though positive effects were obtained also for exposure to fields of 10 mT and higher, experiences with negative effects were found to be more frequent. In addition, by analysing Fig. 3, it can be seen how negative effects on the microorganisms can result even with low exposure duration; progressive adaptation by the microorganisms cannot, however, be excluded for extended exposure duration.
Fig. 3

Type of effects observed according to the intensity of the magnetostatic field and the exposure duration. The numeric label reported close to each point associates it with the reference in Table 2. “Negative” effects (red filled triangle): reduction in the degradation of pollutants and/or substratum consumption, bacterial growth inhibition, reduced metabolic activity or respiration rate, damaged cellular membrane. “Positive” effects (green filled diamond): stimulation of the degradation of contaminants, increased denitrification/nitrification, speed up in the consumption kinetic of substrata, increased resistance to pollutants, increased biomass, increased metabolic activity or in the activity of specific enzymes (e.g. dehydrogenases); “Null” effect (blue filled circle): no significant effects on the aspects mentioned above; “Undefinable” effects (purple filled square): in the absence of positive or negative effects, modifications in the activity of enzymes that are not involved in the degradative metabolism, variation of the ATP concentration, modifications of the microbial community (structure/diversity/genotype/morphotype), effects of mutagenicity, cellular proteome alterations, DNA/RNA synthesis alterations/modifications and related activities, variations in secondary metabolite transposition and production, modifications to the cell form and the characteristics of the cellular wall and its electrostatic charge, increased cell hydrophobicity, increased adhesion between the bacterial cells, increased or reduced resistance to antibiotics. (Color figure online)

4 Electromagnetic fields

4.1 Studies on microorganisms

The first studies on the effects of pulsed electric fields on microorganisms were carried out by Sale and Hamilton in 1967–1968 (Sale and Hamilton 1967, 1968), who investigated the effects on the vitality of the exposed cells and the lethal effects. The reduction in vitality (up to 99.99%) following exposure to high intensity electric pulses was ascribed to the increase of the external cellular membrane permeability. The lethal effect resulted as being related mainly to field intensity and exposure duration, but was also influenced by the production of toxic substances through electrolysis (Hülsheger and Niemann 1980; Hülsheger et al. 1981, 1983).

In 1986 it was seen how the electric charges of cells exposed to an alternate electric field separate, with the formation of an oscillating dipole (Hofmann and Evans 1986).

More recent research (Schoenbach et al. 1997, 2000) clarified that the exposure of cells to an electric field causes the accumulation of electric charges on the cell membrane and, as a result, a variation in the potential gradient between the two sides of the membrane. In the case of low intensity electric fields, this causes the tension-dependent channels of the cell membrane to open. As a result, a flow of ions (Na+, K+) crosses the channels and modifies the concentrations close to the membrane, causing cellular stress. Stress on short electric signals with a low intensity electric field lasts for a few milliseconds and does not cause irreversible damage. With more intense electric fields, a major potential gradient invests the cell membrane, modifying its permeability until the cell is no longer able to fix its damage, which results in cell death (irreversible breakage). The entity of the voltage that causes the tension-dependent channels to open or cell membrane lysis depends on the cell type and size, and the duration of the pulse. For pulses that vary from tens of microseconds to milliseconds, an electric field intensity of around 10 kV/cm is critical for E. coli lysis (Hülsheger et al. 1981).

The presence of an alternate magnetic field influences singlet ⇄ triplet interconversion in the mechanism of the radical-pair already mentioned in the section on magnetostatic fields (Maeda et al. 2008; Rodgers 2009) and, as a consequence, the physiological state of the cell and the enzymatic reaction rates can change (Binhi 2001).

Rakoczy et al. (2016) and Fijałkowski et al. (2015) demonstrated that 1 h of exposure to a sinusoidal magnetic field with an effective intensity of 30 mT and frequency 50 Hz increases the growth and cellular metabolic activity of E. coli and Staphylococcus aureus significantly in comparison with the controls. Furthermore, the authors observed greater stimulation of growth and metabolic activity in cultures of S. aureus in comparison with E. coli. In Fijałkowski et al. (2015), different results were obtained in cultures of Acinetobacter baumannii and Pseudomonas aeruginosa, where the sinusoidal magnetic field (34 mT, 50 Hz) caused the metabolic activity of the cells to decrease. As proposed by Strašák (2005) and Fijałkowski et al. (2015), the effect observed after exposure to the magnetic field could depend on the form of the exposed bacteria. However, following a comparison of the results of the study carried out on A. baumannii and P. aeruginosa with those on other rod-shaped bacterial species (E. coli, Serratia marcescens, Cronobacter sakazakii, Klebsiella oxytoca), the effect on the microorganisms could depend on the specific species, independently from the cellular form.

The results of an additional study carried out on E. coli exposed for 1 h to a sinusoidal magnetic field of intensity 10 mT and frequency 50 Hz, to verify how the field affected cell vitality, were not significantly different from the non-exposed controls (Fojt et al. 2009).

A study carried out on Salmonella exposed to a sinusoidal magnetic field (14.6 mT, 60 Hz) demonstrated no direct damage to the DNA; the results, however, supplied evidence that exposure to the field induces the expression of heat-shock proteins (Williams et al. 2006), which act as biological indicators of cellular stress and help repair or degrade the proteins that were damaged by thermal shock.

Alternate magnetic fields at moderate intensity (200–660 μT, 50 Hz) alter the transcription speed of the lac operon in E. coli (Aarholt 1982). A non-linear dose–effect relationship seems to exist for this type of effect. As an example, while a field intensity of 300 μT suppresses transcription, a field intensity of 550 μT causes a substantial increase.

It was seen that sinusoidal magnetic fields (1.1–1.2 mT, 50–60 Hz) increase the translation activity of the mRNA in E. coli (Goodman et al. 1994; Cairo 1998).

In two consecutive studies, Del Re et al. (2003, 2004) observed the effects on transposition activity in cultures of E. coli exposed to two electromagnetic fields with different characteristics. The results of the first study highlighted that E. coli cells exposed to a sinusoidal magnetic field (50 Hz, 0.1–1 mT) were significantly less active than those of the controls. Conversely, in the subsequent study, the exposure of E. coli cells to a pulsed magnetic field, having the same intensity and frequency, led to significantly greater transposition activity than that of the non-exposed controls being observed. In both studies, transposition was negatively/positively linked to the field intensity with a linear dose–effect relationship. In addition, in both the first and the second study, this phenomenon did not influence bacterial cell proliferation and a significant difference between the amount of colonies exposed or not to the field did not arose. These results suggest that the biological effects depend critically on the physical characteristics of the magnetic signal, in particular the wave shape.

Cellini et al. (2008) exposed cultures of E. coli to magnetic fields of frequency 50 Hz and variable intensity (0.1, 0.5, 1.0 mT). During this study, the effects of electromagnetic radiation on different biological parameters were investigated: Colony-forming Units (CFU), cellular vitality state, morphological and transcription profile. According to the results of the experiments, the studied parameters of the irradiated samples did not present significant differences in comparison with the controls, except for increased cellular vitality and change in the morphology of E. coli, with the presence of “coccoid” cells even aggregated in clusters.

Another study on the effects of pulsed electromagnetic radiation at extremely low frequency on the growth of the bacteria S. aureus showed a decrease in the growth rate. The results evidenced how, in all the tests carried out on cell cultures exposed to fields of intensity within the 0.5–2.5 mT range and frequencies between 2 and 500 Hz, there was a reduction in the number of CFUs in comparison with the non-irradiated controls. In particular, the lowest CFU value was reached after exposure for 90 min at 1.5 mT and 300 Hz (Ahmed et al. 2013).

4.2 Studies in an environmental setting

The recent review of Piyadasa et al. (2017) sums up the experiences carried out when controlling precipitation and fouling in inverse-osmosis membrane systems, in particular for desalination. The use of pulsed electromagnetic fields helped speed up clogging of suspended particles and their precipitation.

In the wastewater treatment field, Yavuz and Çelebi (2000) present the effects of an alternate (8.9–46.6 mT, 50 Hz) or pulsed (17.8 mT 2 s on/2 s off) electromagnetic field. In the first case, an increase of 44% in the substratum removal rate was observed, while in the second there were no significative effects.

In Zhou et al. (2017), a pulsed electromagnetic field (square wave with frequency 100 Hz and intensity 5 μT) applied to a bioelectrochemical system caused changes in the microbial community at the anode: a relatively greater abundance of Geobacter spp. was found (4–8%) than in the control.

Figure 4 shows a summary of the effects on microorganisms (according to the positive, null, negative and undefinable classification) following exposure to sinusoidal electromagnetic fields with frequencies 50–60 Hz, according to the intensity of the magnetic field (given that in most of the manuscripts the induced electric field intensity is not reported) and exposure duration. The choice was made to report the experimental data referred to 50–60 Hz, being typical frequencies of the electric distribution networks, which are most surveyed in the literature.
Fig. 4

Type of effects observed for exposure to electromagnetic fields of frequency 50-60 Hz, according to the intensity of the magnetic field and the exposure duration. The numeric label reported close to each point associates it with the reference in Table 3. Negative” effects (red filled triangle): reduction in the degradation of pollutants and/or substratum consumption, bacterial growth inhibition, reduced metabolic activity or respiration rate, damaged cellular membrane. “Positive” effects (green filled diamond): stimulation of the degradation of specific contaminants, increased denitrification/nitrification, acceleration in the kinetic consumption of substrata, increased resistance to pollutants, increased biomass, increased metabolic activity in general or in the activity of specific enzymes (e.g. dehydrogenases); “Null” effect (blue filled circle): no significant effects on the aspects mentioned above; “Undefinable” effects (purple filled square): in the absence of positive or negative effects, modifications in the activity of enzymes that are not involved in the degradative metabolism, variation of the ATP concentration, modifications of the microbial community (structure/diversity/genotype/morphotype), effects of mutagenicity, cellular proteome alterations, DNA/RNA synthesis alterations/modifications and related activities, variations in secondary metabolite transposition and production, modifications to the cell form and the characteristics of the cellular wall and its electrostatic charge, increased cell hydrophobicity, increased adhesion between the bacterial cells, increased or reduced resistance to antibiotics. (Color figure online)

Most of the experiments took place with magnetic intensity below 20 mT. Even though not numerous, in the case of fields lower than 1 mT the experiments resulted in effects that were mostly positive; on the contrary, with fields that varied between 1 and 10 mT, more studies indicated effects that were negligible, undefinable and negative than those in which positive effects were observed. It should be noted, however, that some authors refer to a field intensity even of a few tens of mT, at which positive effects were observed. The “window” of field intensity at which negligible, undefinable and negative effects were observed varies in relation to the bacterial species. As the mechanisms responsible for bacterial stimulation/inhibition are not currently understood, it seems not possible to forecast the microorganism behaviour to electromagnetic fields of different intensities.

In comparison with electrostatic and magnetostatic fields, the experiments with electromagnetic fields were limited to an exposure duration of a few days at most, and it is not clear if there were microorganism adaptation.

5 Conclusions

The scientific literature that was considered refers to biological effects that at times contrast with each other. For some common microorganisms, suitably insulated and exposed to fields, increases in the cell activity were noted, with effects on the biomass growth rate and the metabolic kinetics. In the few experiences carried out in the environmental field, there is also some evidence of positive effects of exposure to fields, even in the biological wastewater treatment or bioremediation.

The most surveyed fields in relation to bioremediation are certainly the electrostatic fields or generated by continuous currents, already being used today in electrokinesis processes to remove pollutants in sediments and fine grain soils. In some of these processes carried out at full-scale and in situ, biostimulation was also ascribed to the applied electric field. These results are reported in very recent studies and, certainly, further research and experiments must be done to find further evidence using different soils and contaminants, in addition to understanding the mechanisms.

Regarding magnetostatic fields, the most important applications in the environmental field involve wastewater treatment in activated sludge systems. In addition to a potential improvement in solid–liquid separation during the sedimentation step, increases in the degradation kinetics of the organic substance or increased biomass were related to exposure to magnetic fields.

The limited experiences concerning electromagnetic fields in the environmental ambit involve wastewater treatment and in particular the control of fouling.

Even though in the review it was not possible to identify operative conditions that could certainly stimulate biological activity, additional research could be done:
  • on the effects of fields that are electrostatic or generated by direct currents until around 100 V/m (or induced currents of about 10 mA), for the bioremediation of contaminated soils or sediments. Some positive laboratory experiences have been reported for treating solid matrixes in bioelectrochemical or electro-bioremediation systems (as a development of the electrokinesis systems). In consideration of these initial results, but also considering the scarce understanding of the phenomena in play and the decisive role of the choice of operative conditions for compensating the negative effects induced by the electric field (extreme variations in pH, etc.), further research on this matter is certainly necessary for developing and scaling up the technologies;

  • an assessment of the effects of magnetostatic fields of 1–10 mT on bioremediation in soil; from the literature, this aspect does not seem to have been explored yet. Special attention should be placed on assessing how the applied field interacts with the mineral components of the soil, which could present ferromagnetic properties;

  • on electromagnetic fields; even though some research refers to positive effects on bacterial activity, the results as a whole seem to be very contrasting and do not make it possible to identify, from the start, the operative conditions on which to sketch out possible experiments.

Notes

Compliance with ethical standards

Conflict of interest

The authors declared that they have no conflict of interest.

References

  1. Aarholt E (1982) Magnetic fields affect the lac operon system. J Phys Med Biol 27(4):603–610CrossRefGoogle Scholar
  2. Aarholt E, Flinn EA, Smith CW (1981) Effects of low-frequency magnetic fields on bacterial growth rate. Phys Med Biol 26(4):613–621CrossRefGoogle Scholar
  3. Acar YB, Alshawabkeh AN (1993) Principles of electrokinetic remediation. Environ Sci Technol 27(13):2638–2647CrossRefGoogle Scholar
  4. Acar YB, Gale RJ, Alshawabkeh AN, Marks RE, Puppala S, Bricka M, Parker R (1995) Electrokinetic remediation: basics and technology status. J Hazard Mater 40(2):117–137CrossRefGoogle Scholar
  5. Ahmed I, Istivan T, Cosic I, Pirogova E (2013) Evaluation of the effects of Extremely Low Frequency (ELF) Pulsed Electromagnetic Fields (PEMF) on survival of the bacterium Staphylococcus aureus. EPJ Nonlinear Biomed Phys 1:1–17CrossRefGoogle Scholar
  6. Ahmed I, Istivan T, Pirogova E (2015) Irradiation of Escherichia coli by extremely-low frequency (ELF) pulsed electromagnetic fields (PEMF): evaluation of bacterial survival. J Electromagnet Wave 29(1):26–37CrossRefGoogle Scholar
  7. Ailijiang N, Chang J, Wu Q, Li P, Liang P, Zhang X, Huang X (2016) Phenol degradation by suspended biomass in aerobic/anaerobic electrochemical reactor. Water Air Soil Pollut 227(7):227–233CrossRefGoogle Scholar
  8. Alshawabkeh AN, Bricka RM (2000) Basics and applications of electrokinetic remediation. In: Chapter 4 in Remediation engineering of contaminated soils. Marcel Dekker, Inc., New York, NY, pp 95–111Google Scholar
  9. Alshawabkeh AN, Shen Y, Maillacheruvu KY (2004) Effect of DC electric fields on COD in aerobic mixed sludge processes. Environ Eng Sci 21(3):321–329CrossRefGoogle Scholar
  10. Alvarez DC, Pérez VH, Justo OR, Alegre RM (2006) Effect of the extremely low frequency magnetic field on nisin production by Lactococcus lactis subsp. lactis using cheese whey permeate. Process Biochem 41(9):1967–1973CrossRefGoogle Scholar
  11. Andreini C, Bertini I, Cavallaro G, Holliday GL, Thornton JM (2008) Metal ions in biological catalysis: from enzyme databases to general principles. J Biol Inorg Chem 13(8):1205–1218CrossRefGoogle Scholar
  12. Aronsson K, Lindgren M, Johansson BR, Rönner U (2001) Inactivation of microorganisms using pulsed electric fields: the influence of process parameters on Escherichia coli, Listeria innocua, Leuconostoc mesenteroides and Saccharomyces cerevisiae. Innov Food Sci Emerg Technol 2(1):41–54CrossRefGoogle Scholar
  13. Aronsson K, Rönner U, Borch E (2005) Inactivation of Escherichia coli, Listeria innocua and Saccharomyces cerevisiae in relation to membrane permeabilization and subsequent leakage of intracellular compounds due to pulsed electric field processing. Int J Food Microbiol 99(1):19–32CrossRefGoogle Scholar
  14. Aslanimehr M, Pahlevan A-A, Fotoohi-Qazvini F, Jahani-Hashemi H (2013) Effects of extremely low frequency electromagnetic fields on growth and viability of bacteria. Int J Res Med Health Sci 1(2):8–15Google Scholar
  15. Aulenta F, Canosa A, Reale P, Rossetti S, Panero S, Majone M (2009) Microbial reductive dechlorination of trichloroethene to ethene with electrodes serving as electron donors without the external addition of redox mediators. Biotechnol Bioeng 103(1):85–91CrossRefGoogle Scholar
  16. Baraúna RA, Santos AV, Graças DA, Santos DM, Ghilardi Júnior R, Piment AMC, Carepo MSP, Schneider MPC, Silva A (2015) Exposure to an extremely low-frequency electromagnetic field only slightly modifies the proteome of Chromobacterium violaceum ATCC 12472. Genet Mol Biol 38(2):227–230CrossRefGoogle Scholar
  17. Bayır E, Bilgi E, Şendemir-Ürkmez A, Hameş-Kocabaş EE (2015) The effects of different intensities, frequencies and exposure times of extremely low-frequency electromagnetic fields on the growth of Staphylococcus aureus and Escherichia coli O157:H7. Electromagn Biol Med 34(1):14–18CrossRefGoogle Scholar
  18. Belyaev IY, Alipov ED (2001) Frequency-dependent effects of ELF magnetic field on chromatin conformation in Escherichia coli cells and human lymphocytes. Biochim Biophys Acta 1526(3):269–276CrossRefGoogle Scholar
  19. Belyaev IY, Alipov YD, Matronchik AY (1998) Cell density dependent response of E. coli cells to weak ELF magnetic fields. Bioelectromagnetics 19(5):300–309CrossRefGoogle Scholar
  20. Binhi VN (2001) Theoretical concepts in magnetobiology. Electro Magnetobiol 20(1):43–58CrossRefGoogle Scholar
  21. Bond DR, Holmes DE, Tender LM, Lovley DR (2002) Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295(5554):483–485CrossRefGoogle Scholar
  22. Buchachenko A (2009) Magnetic isotope effect in chemistry and biochemistry. Nova Science Publisher, NY, ISBN: 978-1-60741-363-9Google Scholar
  23. Buchachenko LA (2014) Magnetic control of enzymatic phosphorylation. Phys Chem Biophys 4(2):1000142Google Scholar
  24. Buchachenko A (2016) Why magnetic and electromagnetic effects in biology are irreproducible and contradictory? Bioelectromagnetics 37(1):1–13CrossRefGoogle Scholar
  25. Buchachenko AL, Kuznetsov DA, Breslavskaya NN (2012) Chemistry of enzymatic ATP synthesis: an insight through the isotope window. Chem Rev 112(4):2042–2058CrossRefGoogle Scholar
  26. Cairo P (1998) Magnetic field exposure enhances mRNA expression of sigma32 in E. coli growth of cultures. J Cell Biochem 68(1):1–7CrossRefGoogle Scholar
  27. Cast KL, Flora JRV (1998) An evaluation of two cathode materials and the impact of copper on bioelectrochemical denitrification. Water Res 32(1):63–70CrossRefGoogle Scholar
  28. Cellini L, Grande R, Di Campli E, Di Bartolomeo S, Di Giulio M, Robuffo I, Trubiani O, Mariggiò MA (2008) Bacterial response to the exposure of 50 Hz electromagnetic fields. Bioelectromagnetics 29(4):302–311CrossRefGoogle Scholar
  29. Chen X, Chen G, Yue PL (2002) Investigation on the electrolysis voltage of electrocoagulation. Chem Eng Sci 57(13):2449–2455CrossRefGoogle Scholar
  30. Cheng Y, Fan W, Guo L (2014) Coking wastewater treatment using a magnetic porous ceramsite carrier. Sep Purif Technol 130:167–172CrossRefGoogle Scholar
  31. Chow K, Tung WL (2000) Magnetic field exposure stimulates transposition through the induction of DnaK/J synthesis. FEBS Lett 478:133–136CrossRefGoogle Scholar
  32. Costerton JW, Ellis B, Lam K, Johnson F, Khoury AE (1994) Mechanism of electrical enhancement of efficacy of antibiotics in killing biofilm bacteria. Antimicrob Agents Chemother 38(12):2803–2809CrossRefGoogle Scholar
  33. Creanga DE, Poiata A, Morariu VV, Tupu P (2004) Zero-magnetic field effect in pathogen bacteria. J Magn Magn Mater 272–276:2442–2444CrossRefGoogle Scholar
  34. Del Re B, Garoia F, Mesirca P, Agostini C, Bersani F, Giorgi G (2003) Extremely low frequency magnetic fields affect transposition activity in Escherichia coli. Radiat Environ Biophys 42(2):113–118CrossRefGoogle Scholar
  35. Del Re B, Bersani F, Agostini C, Mesirca P, Giorgi G (2004) Various effects on transposition activity and survival of Escherichia coli cells due to different ELF-MF signals. Radiat Environ Biophys 43(4):265–270CrossRefGoogle Scholar
  36. Diao HF, Li XY, Gu JD, Shi HC, Xie ZM (2004) Electron microscopic investigation of the bactericidal action of electrochemical disinfection in comparison with chlorination, ozonation and Fenton reaction. Process Biochem 39(11):1421–1426CrossRefGoogle Scholar
  37. Ellaiah P, Adinarayana K, Sunitha M (2003) Effect of magnetic field on the biosynthesis of neomycin by Streptomyces marinensis. Pharmazie 58(1):58–59Google Scholar
  38. Fan X, Wang H, Luo Q, Ma J, Zhang X (2007) The use of 2D non-uniform electric field to enhance in situ bioremediation of 2,4-dichlorophenol-contaminated soil. J Hazard Mater 148(1–2):29–37CrossRefGoogle Scholar
  39. Feleke Z, Araki K, Sakakibara Y, Watanabe T, Kuroda M (1998) Selective reduction of nitrate to nitrogen gas in a biofilm-electrode reactor. Water Res 32(9):2728–2734CrossRefGoogle Scholar
  40. Fijalkowski K, Nawrotek P, Struk M, Kordas M, Rakoczy R (2013) The effects of rotating magnetic field on growth rate, cell metabolic activity and biofilm formation by Staphylococcus aureus and Escherichia coli. J Magn 18(3):289–296CrossRefGoogle Scholar
  41. Fijalkowski K, Żywicka A, Drozd R, Junka AF, Peitler D, Kordas M, Konopacki M, Szymczyk P, El Fray M, Rakoczy R (2016) Increased yield and selected properties of bacterial cellulose exposed to different modes of a rotating magnetic field. Eng Life Sci 16(5):483–493CrossRefGoogle Scholar
  42. Fijałkowski K, Nawrotek P, Struk M, Kordas M, Rakoczy R (2015) Effects of rotating magnetic field exposure on the functional parameters of different species of bacteria. Electromagn Biol Med 34(1):1536–8378CrossRefGoogle Scholar
  43. Fojt L, Strašák L, Vetterl V (2004) Comparison of the low frequency magnetic field effects on bacteria E. coli, L. adecarboxylata and S. aureus. Bioelectrochemistry 63(1–2):337–341CrossRefGoogle Scholar
  44. Fojt L, Klapetek P, Strašák L, Vetterl V (2009) 50 Hz magnetic field effect on the morphology of bacteria. Micron 40(8):918–922CrossRefGoogle Scholar
  45. Gao W, Liu Y, Zhou J, Pan H (2005) Effects of a strong static magnetic field on bacterium Shewanella oneidensis: an assessment by using whole genome microarray. Bioelectromagnetics 26(7):558–563CrossRefGoogle Scholar
  46. Gill RT, Harbottle MJ, Smith JWN, Thornton SF (2014) Electrokinetic-enhanced bioremediation of organic contaminants: a review of processes and environmental applications. Chemosphere 107:31–42CrossRefGoogle Scholar
  47. Goel R, Flora J (2005a) Stimulating biological nitrification via electrolytic oxygenation. J Environ Eng 131(11):1607–1613CrossRefGoogle Scholar
  48. Goel RK, Flora JRV (2005b) Sequential nitrification and denitrification in a divided cell attached growth bioelectrochemical reactor. Environ Eng Sci 22(4):440–449CrossRefGoogle Scholar
  49. Golzio M, Rols MP, Teissié J (2004) In vitro and in vivo electric field-mediated permeabilization, gene transfer, and expression. Methods 33(2):126–135CrossRefGoogle Scholar
  50. Gomes HI, Dias-Ferreira C, Ribeiro AB (2012) Electrokinetic remediation of organochlorines in soil: enhancement techniques and integration with other remediation technologies. Chemosphere 87(10):1077–1090CrossRefGoogle Scholar
  51. Goodman EM, Greenebaum B, Marron MT (1994) Magnetic fields after translation in Escherichia coli. Bioelectromagnetics 15(1):77–83CrossRefGoogle Scholar
  52. Gregory KB, Bond DR, Lovley DR (2004) Graphite electrodes as electron donors for anaerobic respiration. Environ Microbiol 6(6):596–604CrossRefGoogle Scholar
  53. Grosman Z, Kolár M, Tesaríková E (1992) Effects of static magnetic field on some pathogenic microorganisms. Acta Univ Palacki Olomuc Fac Med 134:7–9Google Scholar
  54. Guo S, Fan R, Li T, Hartog N, Li F, Yang X (2014) Synergistic effects of bioremediation and electrokinetics in the remediation of petroleum-contaminated soil. Chemosphere 109:226–233CrossRefGoogle Scholar
  55. Harbottle MJ, Lear G, Sills GC, Thompson IP (2009) Enhanced biodegradation of pentachlorophenol in unsaturated soil using reversed field electrokinetics. J Environ Manag 90(5):1893–1900CrossRefGoogle Scholar
  56. Hayes AM, Flora JRV, Khan J (1998) Electrolytic stimulation of denitrification in sand columns. Water Res 32(9):2830–2834CrossRefGoogle Scholar
  57. Hofmann GA, Evans GA (1986) Electronic genetic—physical and biological aspects of cellular electro manipulation. IEEE Eng Med Biol Mag 5(4):6–25CrossRefGoogle Scholar
  58. Hönes I, Pospischil A, Berg H (1998) Electrostimulation of proliferation of the denitrifying bacterium Pseudomonas stutzeri. Bioelectrochem Bioenerg 44(2):275–277CrossRefGoogle Scholar
  59. Horiuchi S, Ishizaki Y, Okuno K, Ano T, Shoda M (2001) Drastic high magnetic field effect on suppression of Escherichia coli death. Bioelectrochemistry 53:149–153CrossRefGoogle Scholar
  60. Horiuchi S, Ishizaki Y, Okuno K, Ano T, Shoda M (2002) Change in broth culture is associated with significant suppression of Escherichia coli death under high magnetic field. Bioelectrochemistry 57(2):139–144CrossRefGoogle Scholar
  61. Huang D, Xu Q, Cheng J, Lu X, Zhang H (2012) Electrokinetic remediation and its combined technologies for removal of organic pollutants from contaminated soils. Int J Electrochem Sci 7:4528–4544Google Scholar
  62. Hülsheger H, Niemann E-G (1980) Lethal effects of high-voltage pulses on E. coli K12. Radiat Environ Biophys 18(4):281–288CrossRefGoogle Scholar
  63. Hülsheger H, Potel J, Niemann E-G (1981) Killing of bacteria with electric pulses of high field strength. Radiat Environ Biophys 20(1):53–65CrossRefGoogle Scholar
  64. Hülsheger H, Potel J, Niemann EG (1983) Electric field effects on bacteria and yeast cells. Radiat Environ Biophys 22(2):149–162CrossRefGoogle Scholar
  65. Huwiler SG, Beyer C, Fröhlich J, Hennecke H, Egli T, Schürmann D, Rehrauer H, Fischer HM (2012) Genome-wide transcription analysis of Escherichia coli in response to extremely low-frequency magnetic fields. Bioelectromagnetics 33(6):488–496CrossRefGoogle Scholar
  66. Ikehata M, Koana T, Suzuki Y, Shimizu H, Nakagawa M (1999) Mutagenicity and co-mutagenicity of static magnetic fields detected by bacterial mutation assay. Mutat Res 427(2):147–156CrossRefGoogle Scholar
  67. Inhan-Garip A, Aksu B, Akan Z, Akakin D, Ozaydin AN, San T (2011) Effect of extremely low frequency electromagnetic fields on growth rate and morphology of bacteria. Int J Radiat Biol 87(12):1155–1161CrossRefGoogle Scholar
  68. Ishizaki Y, Horiuchi SI, Okuno K, Ano T, Shoda M (2001) Twelve hours exposure to inhomogeneous high magnetic field after logarithmic growth phase is sufficient for drastic suppression of Escherichia coli death. Bioelectrochemistry 54:101–105CrossRefGoogle Scholar
  69. Jackman SA, Maini G, Sharman AK, Knowles CJ (1999) The effects of direct electric current on the viability and metabolism of acidophilic bacteria. Enzyme Microb Technol 24(5–6):316–324CrossRefGoogle Scholar
  70. Jackman SA, Maini G, Sharman AK, Sunderland G, Knowles CJ (2001) Electrokinetic movement and biodegradation of 2,4-dichlorophenoxyacetic acid in silt soil. Biotechnol Bioeng 74(1):40–48CrossRefGoogle Scholar
  71. Jamshidi-Zanjani A, Darban AK (2017) A review on enhancement techniques of electrokinetic soil remediation. Pollution 3(1):157–166Google Scholar
  72. Ji W, Huang H, Deng A, Pan C (2009) Effects of static magnetic fields on Escherichia coli. Micron 40(8):894–898CrossRefGoogle Scholar
  73. Ji Y, Wang Y, Sun J, Yan T, Li J, Zhao T, Yin X, Sun C (2010) Enhancement of biological treatment of wastewater by magnetic field. Bioresour Technol 101(22):8535–8540CrossRefGoogle Scholar
  74. Justo OR, Pérez VH, Alvarez DC, Alegre RM (2006) Growth of Escherichia coli under extremely low-frequency electromagnetic fields. Appl Biochem Biotechnol 134(2):155–164CrossRefGoogle Scholar
  75. Kim JR, Min B, Logan BE (2005) Evaluation of procedures to acclimate a microbial fuel cell for electricity production. Appl Microbiol Biotechnol 68(1):23–30CrossRefGoogle Scholar
  76. Kim SH, Han HY, Lee YJ, Kim CW, Yang JW (2010) Effect of electrokinetic remediation on indigenous microbial activity and community within diesel contaminated soil. Sci Total Environ 408(16):3162–3168CrossRefGoogle Scholar
  77. Kohno M, Yamazaki M, Kimura I, Wada M (2000) Effect of static magnetic fields on bacteria: Streptococcus mutans, Staphylococcus aureus, and Escherichia coli. Pathophysiology 7(2):143–148CrossRefGoogle Scholar
  78. Król Z, Jarmoluk A (2014) The effects of using a direct electric current on the chemical properties of gelatine gels and bacterial growth. J Food Eng 170:1–7CrossRefGoogle Scholar
  79. Kuroda M, Watanabe T, Umedu Y (1996) Simultaneous oxidation and reduction treatments of polluted water by a bio-electro reactor. Water Sci Technol 34(9):101–108CrossRefGoogle Scholar
  80. László J, Kutasi J (2010) Static magnetic field exposure fails to affect the viability of different bacteria strains. Bioelectromagnetics 31(3):220–225Google Scholar
  81. Lear G, Harbottle MJ, Van Der Gast CJ, Jackman SA, Knowles CJ, Sills G, Thompson IP (2004) The effect of electrokinetics on soil microbial communities. Soil Biol Biochem 36(11):1751–1760CrossRefGoogle Scholar
  82. Lear G, Harbottle MJ, Sills G, Knowles CJ, Semple KT, Thompson IP (2007) Impact of electrokinetic remediation on microbial communities within PCP contaminated soil. Environ Pollut 146(1):139–146CrossRefGoogle Scholar
  83. Łebkowska M, Rutkowska-Narozniak A, Pajor E, Pochanke Z (2011) Effect of a static magnetic field on formaldehyde biodegradation in wastewater by activated sludge. Bioresour Technol 102:8777–8782CrossRefGoogle Scholar
  84. Lei C, Berg H (1998) Electromagnetic window effects on proliferation rate of Corynebacterium glutamicum. Bioelectrochem Bioenerg 45(2):261–265CrossRefGoogle Scholar
  85. Letuta UG, Berdinskiy VL (2017) Magnetosensitivity of bacteria E. coli: magnetic isotope and magnetic field effects. Bioelectromagnetics 38:581–591CrossRefGoogle Scholar
  86. Li S, Chow K (2001) Magnetic field exposure induces DNA degradation. Biochem Biophys Res Commun 280(5):1385–1388CrossRefGoogle Scholar
  87. Li XG, Wang T, Sun JS, Huang X, Kong XS (2006) Biodegradation of high concentration phenol containing heavy metal ions by functional biofilm in bioelectro-reactor. J Environ Sci China 18(4):639–643Google Scholar
  88. Li H, Zhu X, Ni J (2011) Comparison of electrochemical method with ozonation, chlorination and monochloramination in drinking water disinfection. Electrochim Acta 56(27):9789–9796CrossRefGoogle Scholar
  89. Liu WK, Brown MRW, Elliott TSJ (1997) Mechanisms of the bactericidal activity of low amperage electric current (DC). J Antimicrob Chemother 39(6):687–695CrossRefGoogle Scholar
  90. Lovley DR, Coates JD, Blunt-Harris EL, Phillips EJP, Woodward JC (1996) Humic substances as electron acceptors for microbial respiration. Nature 382(6590):445–448CrossRefGoogle Scholar
  91. Luo Q, Wang H, Zhang X, Qian Y (2005a) Effect of direct electric current on the cell surface properties of phenol-degrading bacteria. Appl Environ Microbiol 71(1):423–427CrossRefGoogle Scholar
  92. Luo Q, Zhang X, Wang H, Qian Y (2005b) The use of non-uniform electrokinetics to enhance in situ bioremediation of phenol-contaminated soil. J Hazard Mater 121(1–3):187–194CrossRefGoogle Scholar
  93. Luo Q, Wang H, Zhang X, Fan X, Qian Y (2006) In situ bioelectrokinetic remediation of phenol-contaminated soil by use of an electrode matrix and a rotational operation mode. Chemosphere 64(3):415–422CrossRefGoogle Scholar
  94. Maeda K, Henbest KB, Cintolesi F, Kuprov I, Rodgers CT, Liddell PA, Gust D, Timmel CR, Hore PJ (2008) Chemical compass model of avian magnetoreception. Nature 453(7193):387–390CrossRefGoogle Scholar
  95. Mansouri A, Abbes C, Landoulsi A (2017) Combined intervention of static magnetic field and growth rate of Microbacterium maritypicum CB7 for Benzo(a)Pyrene biodegradation. Microb Pathog 113:40–44CrossRefGoogle Scholar
  96. Mena Ramírez E, Villaseñor Camacho J, Rodrigo MA, Cañizares P (2014) Feasibility of electrokinetic oxygen supply for soil bioremediation purposes. Chemosphere 117(1):382–387CrossRefGoogle Scholar
  97. Mena E, Villaseñor J, Cañizares P, Rodrigo MA (2014) Effect of a direct electric current on the activity of a hydrocarbon-degrading microorganism culture used as the flushing liquid in soil remediation processes. Sep Purif Technol 124:217–223CrossRefGoogle Scholar
  98. Mena E, Villaseñor J, Cañizares P, Rodrigo MA (2016a) Effect of electric field on the performance of soil electro-bioremediation with a periodic polarity reversal strategy. Chemosphere 146:300–307CrossRefGoogle Scholar
  99. Mena E, Villaseñor J, Cañizares P, Rodrigo MA (2016b) Influence of electric field on the remediation of polluted soil using a biobarrier assisted electro-bioremediation process. Electrochim Acta 190:294–304CrossRefGoogle Scholar
  100. Mittenzwey R, Süßmuth R, Mei W (1996) Effects of extremely low-frequency electromagnetic fields on bacteria—the question of a co-stressing factor. Bioelectrochem Bioenerg 40(1):21–27CrossRefGoogle Scholar
  101. Moghadam MJ, Moayedi H, Sadeghi MM, Hajiannia A (2016) A review of combinations of electrokinetic applications. Environ Geochem Health 38(6):1217–1227CrossRefGoogle Scholar
  102. Mohtasham P, Keshavarz-Moore E, Kale I, Keshavarz T (2016) Application of magnetic field for improvement of microbial productivity. Chem Eng Trans 49:43–48Google Scholar
  103. Mousavi SAR, Ibrahim S, Aroua MK, Ghafari S (2010) Bio-electrochemical denitrification—a review. Int J Chem Environ Eng 2(2):140–146Google Scholar
  104. Mousavi S, Ibrahim S, Aroua MK, Ghafari S (2012) Development of nitrate elimination by autohydrogenotrophic bacteria in bio-electrochemical reactors—a review. Biochem Eng J 67:251–264CrossRefGoogle Scholar
  105. Nakamura K, Okuno K, Ano T, Shoda M (1997) Effect of high magnetic field on the growth of measured in a newly developed superconducting magnet biosystem. Bioelectrochem Bioenerg 43:23–128CrossRefGoogle Scholar
  106. Nasciniento LFC, Botura G, Mota RP (2003) Glucose consume and growth of E. coli under electromagnetic field. Rev Inst Med Trop Sao Paulo 45(2):65–67CrossRefGoogle Scholar
  107. Niqui-Arroyo JL, Bueno-Montes M, Posada-Baquero R, Ortega-Calvo JJ (2006) Electrokinetic enhancement of phenanthrene biodegradation in creosote-polluted clay soil. Environ Pollut 142(2):326–332CrossRefGoogle Scholar
  108. Niu C, Geng J, Ren H, Ding L, Xu K, Liang W (2013) The strengthening effect of a static magnetic field on activated sludge activity at low temperature. Bioresour Technol 150:156–162CrossRefGoogle Scholar
  109. Niu C, Liang W, Ren H, Geng J, Ding L, Xu K (2014) Enhancement of activated sludge activity by 10–50 mT static magnetic field intensity at low temperature. Bioresour Technol 159:18–54CrossRefGoogle Scholar
  110. Okuda M, Saito K, Kamikado T, Ito S, Matsumoto K, Okuno K, Tsuchiya K, Ano T, Shoda M (1995) New 7 T superconducting magnet system for bacterial cultivation. Cryogenics 35(1):41–47CrossRefGoogle Scholar
  111. Okuno K, Fujinami R, Ano T, Shoda M (2001) Disappearance of growth advantage in stationary phase GASP phenomenon under a high magnetic field. Bioelectrochemistry 53:165–169CrossRefGoogle Scholar
  112. Palaniappan S, Sastry SK, Richter ER (1992) Effects of electroconductive heat treatment and electrical pretreatment on thermal death kinetics of selected microorganisms. Biotechnol Bioeng 39(2):225–232CrossRefGoogle Scholar
  113. Park JC, Lee MS, Lee DH, Park BJ, Han DW, Uzawa M, Takatori K (2003) Inactivation of bacteria in seawater by low-amperage electric current. Appl Environ Microbiol 69(4):2405–2408CrossRefGoogle Scholar
  114. Pazos M, Rosales E, Alcántara T, Gómez J, Sanromán MA (2010) Decontamination of soils containing PAHs by electroremediation: a review. J Hazard Mater 177(1–3):1–11CrossRefGoogle Scholar
  115. Pazos M, Plaza A, Martín M, Lobo MC (2012) The impact of electrokinetic treatment on a loamy-sand soil properties. Chem Eng Sci 183:231–237CrossRefGoogle Scholar
  116. Piatti E, Albertini MC, Baffone W, Fraternale D, Citterio B, Piacentini MP, Dacha M, Vetrano F, Accorsi A (2002) Antibacterial effect of a magnetic field on Serratia marcescens and related virulence to Hordeum vulgare and Rubus fruticosus callus cells. Comp Biochem Physiol B 132:359–365CrossRefGoogle Scholar
  117. Piyadasa C, Yeager TR, Gray SR, Stewart MB, Ridgway HF, Pelekani C, Orbell JD (2017) The effect of electromagnetic fields, from two commercially available water treatment devices, on bacterial culturability. Water Sci Technol 73(6):1371–1377CrossRefGoogle Scholar
  118. Pohl HA, Pollock K, Crane JS (1978) Dielectrophoretic force: a comparison of theory and experiment. J Biol Phys 6(3–4):133–160CrossRefGoogle Scholar
  119. Pospíšilová D, Schreiberová O, Jirku V, Lederer T (2015) Effects of magnetic field on phenol biodegradation and cell physiochemical properties of Rhodococcus erythropolis. Bioremediat J 19(3):201–206CrossRefGoogle Scholar
  120. Potenza L, Ubaldi L, De Sanctis R, De Bellis R, Cucchiarini L, Dacha M (2004) Effects of a static magnetic field on cell growth and gene expression in Escherichia coli. Mutat Res 561(1–2):53–62CrossRefGoogle Scholar
  121. Probstein RF, Hicks RE (1993) Removal of contaminants from soils by electric fields. Science 260(5107):498–503CrossRefGoogle Scholar
  122. Qu M, Chen J, Huang Q, Chen J, Xu Y, Luo J, Wang K, Gao W, Zheng Y (2018) Bioremediation of hexavalent chromium contaminated soil by a bioleaching system with weak magnetic fields. Int Biodeterior Biodeg 128:41–47CrossRefGoogle Scholar
  123. Quan Y, Wu H, Yin Z, Fang Y, Yin C (2017) Effect of static magnetic field on trichloroethylene removal in a biotrickling filter. Bioresour Technol 239:7–16CrossRefGoogle Scholar
  124. Rabbi M, Clark B, Gale R, Ozsu-Acar E, Pardue J, Jackson A (2000) In situ TCE bioremediation study using electrokinetic cometabolite injection. Waste Manag 20(4):279–286CrossRefGoogle Scholar
  125. Rahner D, Ludwig G, Röhrs J (2002) Electrochemically induced reactions in soils—a new approach to the in situ remediation of contaminated soils? Part 1: the microconductor principle. Electrochim Acta 47(9):1395–1403CrossRefGoogle Scholar
  126. Rakoczy R, Konopacki M, Fijałkowski K (2016) The influence of a ferrofluid in the presence of an external rotating magnetic field on the growth rate and cell metabolic activity of a wine yeast strain. Biochem Eng J 109:43–50CrossRefGoogle Scholar
  127. Ramon C, Martin JT, Powell MR (1987) Low-level, magnetic-field-induced growth modification of Bacillus subtilis. Bioelectromagnetics 8(3):275–282CrossRefGoogle Scholar
  128. Rittié L, Perbal B (2008) Enzymes used in molecular biology: a useful guide. J Cell Commun Signal 2(1–2):25–45CrossRefGoogle Scholar
  129. Rodgers CT (2009) Magnetic field effects in chemical systems. Pure Appl Chem 81(1):19–43CrossRefGoogle Scholar
  130. Sakakibara Y, Kuroda M (1993) Electric prompting and control of denitrification. Biotechnol Bioeng 42(4):535–537CrossRefGoogle Scholar
  131. Sale A, Hamilton W (1967) Effects of high electric fields on microorganisms. I. Killing of bacteria and yeasts. Biochim Biophys Acta Gen Subj 148(3):781–788CrossRefGoogle Scholar
  132. Sale AJH, Hamilton WA (1968) Effects of high electric fields on micro-organisms: III. Lysis of erythrocytes and protoplasts. Biochim Biophys Acta Biomembr 163(1):37–43CrossRefGoogle Scholar
  133. Satoshi N, Norio M, Hiroshi S (1997) Electrochemical cultivation of Thiobacillus ferrooxidans by potential control. Bioelectrochem Bioenerg 43:61–67CrossRefGoogle Scholar
  134. Schoenbach KH, Peterkin FE, Alden RW, Beebe SJ (1997) The effect of pulsed electric fields on biological cells: experiments and applications. IEEE Trans Plasma Sci 25(2):284–292CrossRefGoogle Scholar
  135. Schoenbach KH, Joshi RP, Stark RH, Dobbs FC, Beebe SJ (2000) Bacterial decontamination of liquids with pulsed electric fields. IEEE Trans Dielectr Electr Insul 7(5):637–645CrossRefGoogle Scholar
  136. Segatore B, Setacci D, Bennato F, Cardigno R, Amicosante G, Iorio R (2012) Evaluations of the effects of extremely low-frequency electromagnetic fields on growth and antibiotic susceptibility of Escherichia coli and Pseudomonas aeruginosa. Int J Microbiol.  https://doi.org/10.1155/2012/587293 CrossRefGoogle Scholar
  137. She P, Song B, Xing XH, Van Loosdrecht M, Liu Z (2006) Electrolytic stimulation of bacteria Enterobacter dissolvens by a direct current. Biochem Eng J 28(1):23–29CrossRefGoogle Scholar
  138. Shi L, Müller S, Harms H, Wick LY (2008) Factors influencing the electrokinetic dispersion of PAH-degrading bacteria in a laboratory model aquifer. Appl Microbiol Biotechnol 80(3):507–515CrossRefGoogle Scholar
  139. Stansell MJ, Winters WD, Doe RH, Dart BK (2001) Increased antibiotic resistance of E. coli exposed to static magnetic fields. Bioelectromagnetics 22(2):129–137CrossRefGoogle Scholar
  140. Steiner UE, Ulrich T (1989) Magnetic field effects in chemical kinetics and related phenomena. Chem Rev 89(1):51–147CrossRefGoogle Scholar
  141. Strašák L (2005) Effects of 50 Hz MF on the viability of different bacterial strains. Electromagn Biol Med 24(3):293–300CrossRefGoogle Scholar
  142. Strašák L, Vetterl V, Šmarda J (2002) Effects of low-frequency magnetic fields on bacteria Escherichia coli. Bioelectrochemistry 55(1–2):161–164CrossRefGoogle Scholar
  143. Suni S, Malinen E, Kosonen J, Silvennoinen H, Romantschuk M (2007) Electrokinetically enhanced bioremediation of creosote-contaminated soil: laboratory and field studies. J Environ Sci Health A 42(3):277–287CrossRefGoogle Scholar
  144. Tessaro LWE, Murugan NJ, Persinger MA (2015) Bacterial growth rates are influenced by cellular characteristics of individual species when immersed in electromagnetic fields. Microbiol Res 172:26–33CrossRefGoogle Scholar
  145. Thrash JC, Coates JD (2008) Review: direct and indirect electrical stimulation of microbial metabolism. Environ Sci Technol 42(11):3921–3931CrossRefGoogle Scholar
  146. Tomska A, Wolny L (2008) Enhancement of biological wastewater treatment by magnetic field exposure. Desalination 222:368–373CrossRefGoogle Scholar
  147. Tsuchiya K, Nakamura K, Okuno K, Ano T, Shoda M (1996) Effect of homogeneous and inhomogeneous high magnetic fields on the growth of Escherichia coli. J Ferment Bioeng 81(4):343–346CrossRefGoogle Scholar
  148. Tsuchiya K, Okuno K, Ano T, Tanaka K, Takahashi H, Shoda M (1999) High magnetic field enhances stationary phase-specific transcription activity of Escherichia coli. Bioelectrochem Bioenerg 48(2):383–387CrossRefGoogle Scholar
  149. Utsunomiya T, Yamane Y-I, Watanabe M, Sasaki K (2003) Stimulation of porphyrin production by application of an external magnetic field to a photosynthetic bacterium, Rhodobacter sphaeroides. J Biosci Bioeng 95(4):401–404CrossRefGoogle Scholar
  150. Valle A, Zanardini E, Abbruscato P, Argenzio P, Lustrato G, Ranalli G, Sorlini C (2007) Effects of low electric current (LEC) treatment on pure bacterial cultures. J Appl Microbiol 103(5):1376–1385CrossRefGoogle Scholar
  151. Velasco-Alvarez N, González I, Damian-Matsumura P, Gutiérrez-Rojas M (2011) Enhanced hexadecane degradation and low biomass production by Aspergillus niger exposed to an electric current in a model system. Bioresour Technol 102(2):509–1515CrossRefGoogle Scholar
  152. Wan Y, Zhang J, Han H, Li L, Liu Y, Gao M (2017) Citrinin-producing capacity of Monascus purpureus in response to low-frequency magnetic fields. Process Biochem 53:25–29CrossRefGoogle Scholar
  153. Wei V, Elektorowicz M, Oleszkiewicz JA (2011) Influence of electric current on bacterial viability in wastewater treatment. Water Res 45(16):5058–5062CrossRefGoogle Scholar
  154. Wick LY, Mattle PA, Wattiau P, Harms H (2004) Electrokinetic transport of PAH-degrading bacteria in model aquifers and soil. Environ Sci Technol 38(17):4596–4602CrossRefGoogle Scholar
  155. Wick LY, Shi L, Harms H (2007) Electro-bioremediation of hydrophobic organic soil-contaminants: a review of fundamental interactions. Electrochim Acta 52:3441–3448CrossRefGoogle Scholar
  156. Wick LY, Buchholz F, Fetzer I, Kleinsteuber S, Härtig C, Shi L, Miltner A, Harms H, Pucci GN (2010) Responses of soil microbial communities to weak electric fields. Sci Total Environ 408(20):4886–4893CrossRefGoogle Scholar
  157. Williams PA, Ingebretsen RJ, Dawson RJ (2006) 14.6 mT ELF magnetic field exposure yields no DNA breaks in model system Salmonella, but provides evidence of heat stress protection. Bioelectromagnetics 27(6):445–450CrossRefGoogle Scholar
  158. Woodward JR (2002) Radical pairs in solution. Prog React Kinet Mech 27(3):165–207CrossRefGoogle Scholar
  159. Xu YB, Sun SY (2008) Effect of stable weak magnetic field on Cr(VI) bio-removal in anaerobic SBR system. Biodegradation 19(3):455–462CrossRefGoogle Scholar
  160. Xu YB, Duan XJ, Yan JN, Du YY, Sun SY (2009) Influence of magnetic field on activity of given anaerobic sludge. Biodegradation 20(6):875–883CrossRefGoogle Scholar
  161. Yavuz H, Çelebi SS (2000) Effects of magnetic field on activity of activated sludge in wastewater treatment. Enzyme Microb Technol 26(1):22–27CrossRefGoogle Scholar
  162. Yeung AT, Gu Y-Y (2011) A review on techniques to enhance electrochemical remediation of contaminated soils. J Hazard Mater 195:11–29CrossRefGoogle Scholar
  163. Yuan Y, Guo S-H, Li F-M, Li T-T (2013) Effect of an electric field on n-hexadecane microbial degradation in contaminated soil. Int Biodeter Biodegr 77:78–84CrossRefGoogle Scholar
  164. Zaidi NS, Sohaili J, Muda K, Sillanpää M (2014) Magnetic field application and its potential in water and wastewater treatment systems. Sep Purif Rev 43(3):206–240CrossRefGoogle Scholar
  165. Zanardini E, Valle A, Gigliotti C, Papagno G, Ranalli G, Sorlini C (2002) Laboratory-scale trials of electrolytic treatment on industrial wastewaters: microbiological aspects. J Environ Sci Health A Tox Hazard Subst Environ Eng 37(8):1093–4529CrossRefGoogle Scholar
  166. Zhan G, Zhang L, Li D, Su W, Tao Y, Qian J (2012) Autotrophic nitrogen removal from ammonium at low applied voltage in a single-compartment microbial electrolysis cell. Bioresour Technol 116:271–277CrossRefGoogle Scholar
  167. Zhang JL, Cao ZP, Zhang HW, Zhao LM, Sun XD, Mei F (2013) Degradation characteristics of 2,4-dichlorophenoxyacetic acid in electro-biological system. J Hazard Mater 262:137–142CrossRefGoogle Scholar
  168. Zhang X, Feng H, Shan D, Shentu J, Wang M, Yin J, Shen D, Huang B, Ding Y (2014) The effect of electricity on 2-fluoroaniline removal in a bioelectrochemically assisted microbial system (BEAMS). Electrochim Acta 135:439–446CrossRefGoogle Scholar
  169. Zhao YN, Li XF, Ren YP, Wang XH (2016) Effect of static magnetic field on the performances of and anode biofilms in microbial fuel cells. RSC Adv 6(85):82301–82308CrossRefGoogle Scholar
  170. Zhou H, Liu B, Wang Q, Sun J, Xie G, Ren N, Ren ZJ, Xing D (2017) Pulse electromagnetic fields enhance extracellular electron transfer in magnetic bioelectrochemical systems. Biotechnol Biofuels 10(1):238CrossRefGoogle Scholar
  171. Zielinski M, Cydzik-Kwiatkowska A, Zielinska M, Dębowski M, Rusanowska P, Kopańska J (2017) Nitrification in activated sludge exposed to static magnetic field. Water Air Soil Pollut 228(4):126CrossRefGoogle Scholar
  172. Zimmermann U, Schulz J, Pilwat G (1973) Transcellular ion flow in Escherichia coli B and electrical sizing of bacterias. Biophys J 13(10):1005–1013CrossRefGoogle Scholar
  173. Zituni D, Schütt-Gerowitt H, Kopp M, Krönke M, Addicks K, Hoffmann C, Hellmich M, Faber F, Niedermeier W (2014) The growth of Staphylococcus aureus and Escherichia coli in low-direct current electric fields. Int J Oral Sci 6(1):7–14CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Civil and Environmental EngineeringPolitecnico di MilanoMilanItaly

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