Skip to main content
SpringerLink
Log in

The Role of High Voltage Electrode Material in the Inactivation of E. coli by Direct-in-Liquid Electrical Discharge Plasma

  • Original paper
  • Published:
Plasma Chemistry and Plasma Processing Aims and scope Submit manuscript

Abstract

This work investigates the effect of high voltage (HV) electrode material of a point-plane plasma reactor on the inactivation rate of E. coli in both direct plasma and post-discharge inactivation processes. For the direct plasma processes, nickel chromium alloy, iron, tungsten and copper were used as HV electrode materials. In comparison with the other three materials, a significantly higher inactivation rate of E. coli was achieved with copper as the HV electrode. The inactivation effect was demonstrated to be mainly associated with the toxicity of copper ions, rather than from copper nanoparticles released from the electrode during the treatment. Similarly, for the post-discharge inactivation process, a higher E. coli inactivation rate was achieved in both post-plasma and plasma-treated water treatment using copper as the HV electrode, as compared to the tungsten control case. Increased inactivation rates are a result of a synergistic action between copper ions and the hydrogen peroxide generated by the plasma.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14

Similar content being viewed by others

References

  1. Marsili L, Espie S, Anderson JG, MacGregor SJ (2002) Plasma inactivation of food-related microorganisms in liquids. Radiat Phys Chem 65(4–5):507–513

    Article  CAS  Google Scholar 

  2. Gupta SB, Bluhm H (2008) The potential of pulsed underwater streamer discharges as a disinfection technique. IEEE Trans Plasma Sci 36(4):1621–1632

    Article  CAS  Google Scholar 

  3. Sakud A, Shintani H (2011) Sterilization and disinfection by plasma: sterilization mechanisms, biological, and medical applications. NOVA Science Publishers, Hauppauge

    Google Scholar 

  4. Sunka P, Babický V, Clupek M, Lukes P, Simek M, Schmidt J, Cernak M (1999) Generation of chemically active species by electrical discharges in water. Plasma Sources Sci Technol 8(2):258–265

    Article  CAS  Google Scholar 

  5. Held P (2012) An introduction to reactive oxygen species: measurement of ROS in cells (white paper), Vermont. https://www.biotek.com/resources/white-papers/an-introduction-to-reactive-oxygen-species-measurement-of-ros-in-cells/. 26 Oct 2018

  6. Dobrynin D, Fridman G, Friedman G, Fridman A (2009) Physical and biological mechanisms of direct plasma interaction with living tissue. N J Phys 11(11):115020–115045

    Article  CAS  Google Scholar 

  7. Munakata N, Hidea K, Kobayashi K, Ito A, Ito T (1986) Action spectra in ultraviolet wavelengths (150–250 nm) for inactivation and mutagenesis of Bacillus subtilis spores obtained with synchrotron radiation. Photochem Photobiol 44(3):385–390

    Article  CAS  PubMed  Google Scholar 

  8. Munakata N, Saito M, Hieda K (1991) Inactivation action spectra of Bacillus subtilis spores in extended ultraviolet wavelengths (50–300 nm) obtained with synchrotron radiation. Photochem Photobiol 54(5):761–768

    Article  CAS  PubMed  Google Scholar 

  9. Lindberg C, Horneck G (1991) Action spectra for survival and spore photoproduct formation of Bacillus subtilis irradiated with short-wavelength (200–300 nm) UV at atmospheric pressure and in vacuo. J Photochem Photobiol B 11(1):69–80

    Article  CAS  PubMed  Google Scholar 

  10. Moreau M, Feuilloley M, Veron W, Meylheuc T, Chevalier S, Brisset J-L, Orange N (2007) Gliding arc discharge in the potato pathogen Erwinia carotovora subsp. atroseptica: mechanism of lethal action and effect on membrane-associated molecules. Appl Environ Microbiol 73(18):5904–5910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Abou-Ghazala A, Katsuki S, Schoenbach KH, Dobbs FC, Moreira KR (2002) Bacterial decontamination of water by means of pulsed-corona discharges. IEEE Trans Plasma Sci 30(4):1449–1453

    Article  Google Scholar 

  12. Khan MSI, Lee E-J, Kim Y-J (2016) A submerged dielectric barrier discharge plasma inactivation mechanism of biofilms produced by Escherichia coli O157: H7, Cronobacter sakazakii, and Staphylococcus aureus. Sci Rep 6:37072–37082

    Article  CAS  PubMed Central  Google Scholar 

  13. Lukes P, Clupek M, Babicky V, Sunka P (2008) Ultraviolet radiation from the pulsed corona discharge in water. Plasma Sources Sci Technol 17(2):024012–024022

    Article  CAS  Google Scholar 

  14. Lukeš P, Člupek M, Babický V, Šunka P, Skalný J, Štefečka M, Novák J, Málková Z (2006) Erosion of needle electrodes in pulsed corona discharge in water. Czech J Phys 56(2):B916–B924

    Article  Google Scholar 

  15. Holzer F, Locke BR (2008) Influence of high voltage needle electrode material on hydrogen peroxide formation and electrode erosion in a hybrid gas–liquid series electrical discharge reactor. Plasma Chem Plasma Process 28(1):1–13

    Article  CAS  Google Scholar 

  16. Kirkpatrick MJ, Locke BR (2006) Effects of platinum electrode on hydrogen, oxygen, and hydrogen peroxide formation in aqueous phase pulsed corona electrical discharge. Ind Eng Chem Res 45(6):2138–2142

    Article  CAS  Google Scholar 

  17. Vukusic T, Shi M, Herceg Z, Rogers S, Estifaee P, Thagard SM (2016) Liquid-phase electrical discharge plasmas with a silver electrode for inactivation of a pure culture of Escherichia coli in water. Innov Food Sci Emerg Technol 38:407–413

    Article  CAS  Google Scholar 

  18. Berger T, Spadaro J, Bierman R, Chapin S, Becker R (1976) Antifungal properties of electrically generated metallic ions. Antimicrob Agents Chemother 10(5):856–860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Sondi I, Salopek-Sondi B (2004) Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J Colloid Interface Sci 275(1):177–182

    Article  CAS  PubMed  Google Scholar 

  20. Rai M, Yadav A, Gade A (2009) Silver nanoparticles as a new generation of antimicrobials. Biotechnol Adv 27(1):76–83

    Article  CAS  PubMed  Google Scholar 

  21. Durán N, Durán M, de Jesus MB, Seabra AB, Fávaro WJ, Nakazato G (2016) Silver nanoparticles: a new view on mechanistic aspects on antimicrobial activity. Nanomed Nanotechnol Biol Med 12(3):789–799

    Article  CAS  Google Scholar 

  22. Karlsson HL, Cronholm P, Hedberg Y, Tornberg M, De Battice L, Svedhem S, Wallinder IO (2013) Cell membrane damage and protein interaction induced by copper containing nanoparticles—importance of the metal release process. Toxicol 313(1):59–69

    Article  CAS  Google Scholar 

  23. Ojeil M, Jermann C, Holah J, Denyer SP, Maillard J-Y (2013) Evaluation of new in vitro efficacy test for antimicrobial surface activity reflecting UK hospital conditions. J Hosp Infect 85(4):274–281

    Article  CAS  PubMed  Google Scholar 

  24. Varghese S, ElFakhri SO, Sheel DW, Sheel P, Bolton FJE, Foster HA (2013) Antimicrobial activity of novel nanostructured Cu-SiO2 coatings prepared by chemical vapour deposition against hospital related pathogens. AMB Express 3(1):53–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Atwood CS, Huang X, Moir RD, Tanzi RE, Bush AI (1999) Role of free radicals and metal ions in the pathogenesis of Alzheimer’s disease. In: Sigel A (ed) Metal ions in biological systems, 1st edn. Routledge, New York

    Google Scholar 

  26. Imlay JA, Chin SM, Linn S (1988) Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240(4852):640–642

    Article  CAS  PubMed  Google Scholar 

  27. Macomber L, Rensing C, Imlay JA (2007) Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli. J Bacteriol 189(5):1616–1626

    Article  CAS  PubMed  Google Scholar 

  28. Merouani D, Abdelmalek F, Ghezzar M, Semmoud A, Addou A, Brisset J (2013) Influence of peroxynitrite in gliding arc discharge treatment of alizarin red s and postdischarge effects. Ind Eng Chem Res 52(4):1471–1480

    Article  CAS  Google Scholar 

  29. Lukes P, Brisset JL, Locke BR (2012) Biological effects of electrical discharge plasma in water and in gas–liquid environments. In: Parvulescu VI, Magureanu M, Lukes P (eds) Plasma chemistry and catalysis in gases and liquids, 1st edn. Wiley, New York

    Google Scholar 

  30. Traylor MJ, Pavlovich MJ, Karim S, Hait P, Sakiyama Y, Clark DS, Graves DB (2011) Long-term antibacterial efficacy of air plasma-activated water. J Phys D Appl Phys 44(47):472001–472004

    Article  CAS  Google Scholar 

  31. Naïtali M, Kamgang-Youbi G, Herry J-M, Bellon-Fontaine M-N, Brisset J-L (2010) Combined effects of long-living chemical species during microbial inactivation using atmospheric plasma-treated water. Appl Environ Microbiol 76(22):7662–7664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Kamgang-Youbi G, Herry J-M, Bellon-Fontaine M-N, Brisset J-L, Doubla A, Naïtali M (2007) Evidence of temporal postdischarge decontamination of bacteria by gliding electric discharges: application to Hafnia alvei. Appl Environ Microbiol 73(15):4791–4796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Jin ZT, Zhang QH (1999) Pulsed electric field inactivation of microorganisms and preservation of quality of cranberry juice. J Food Process Preserv 23(6):481–497

    Article  Google Scholar 

  34. Shen J, Tian Y, Li Y, Ma R, Zhang Q, Zhang J, Fang J (2016) Bactericidal effects against S. aureus and physicochemical properties of plasma activated water stored at different temperatures. Sci Rep 6:28505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Estifaee P, Su X, Yannam S, Rogers S, Thagard SM (2019) Mechanism of E. coli inactivation by direct-in-liquid electrical discharge plasma in low conductivity solutions. Sci Rep 9(1):2326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Yang C, Wang J, Xiao F, Su X (2014) Microwave hydrothermal disassembly for evolution from CuO dendrites to nanosheets and their applications in catalysis and photo-catalysis. Powder Technol 264:36–42

    Article  CAS  Google Scholar 

  37. Xue J, Liang W, Liu X, Shen Q, Xu B (2012) Crystallization behavior and formation mechanism of dendrite Cu2O crystals. CrystEngComm 14(23):8017–8022

    Article  CAS  Google Scholar 

  38. Li C, Cao X, Li W, Zhang B, Xiao L (2019) Co-synthesis of CuO-ZnO nanoflowers by low voltage liquid plasma discharge with brass electrode. J Alloys Compd 773:762–769

    Article  CAS  Google Scholar 

  39. Wang Y, Jiang T, Meng D, Yang J, Li Y, Ma Q, Han J (2014) Fabrication of nanostructured CuO films by electrodeposition and their photocatalytic properties. Appl Surf Sci 317:414–421

    Article  CAS  Google Scholar 

  40. Padil VVT, Černík M (2013) Green synthesis of copper oxide nanoparticles using gum karaya as a biotemplate and their antibacterial application. Int J Nanomed 8:889–899

    Google Scholar 

  41. Sudha VP, Singh KO, Prasad S, Venkatasubramanian P (2009) Killing of enteric bacteria in drinking water by a copper device for use in the home: laboratory evidence. Trans R Soc Trop Med Hyg 103(8):819–822

    Article  CAS  PubMed  Google Scholar 

  42. Borkow G, Gabbay J (2005) Copper as a biocidal tool. Curr Med Chem 12(18):2163–2175

    Article  CAS  PubMed  Google Scholar 

  43. Pârvulescu VI, Magureanu M, Lukes P (2012) Plasma chemistry and catalysis in gases and liquids. Wiley, New York

    Book  Google Scholar 

  44. Chieppa M, Giannelli G (2018) Immune cells and microbiota response to iron starvation, the quercetin paradigm. Front Med 5:109–112

    Article  Google Scholar 

  45. Lemire JA, Harrison JJ, Turner RJ (2013) Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat Rev Microbiol 11(6):371–384

    Article  CAS  PubMed  Google Scholar 

  46. Kremer ML (2003) The Fenton reaction. Dependence of the rate on pH. J Phys Chem A 107(11):1734–1741

    Article  CAS  Google Scholar 

  47. Wang H, Sweikart MA, Turner JA (2003) Stainless steel as bipolar plate material for polymer electrolyte membrane fuel cells. J Power Sources 115(2):243–251

    Article  CAS  Google Scholar 

  48. Mengoni A, Barzanti R, Gonnelli C, Gabbrielli R, Bazzicalupo M (2001) Characterization of nickel-resistant bacteria isolated from serpentine soil. Environ Microbiol 3(11):691–698

    Article  CAS  PubMed  Google Scholar 

  49. Yang L, Yang X, Liu J, Li Y, Lou Q, Liu Q (2003) Synthesis, characterization and susceptibility of bacteria against Sulfamethoxydiazine complexes of copper (II), zinc (II), nickel (II), cadmium (II), chromium (III) and iron (III). J Coord Chem 56(13):1131–1139

    Article  CAS  Google Scholar 

  50. Lukes P, Clupek M, Babicky V, Sisrova I, Janda V (2011) The catalytic role of tungsten electrode material in the plasmachemical activity of a pulsed corona discharge in water. Plasma Sources Sci Technol 20(3):034011–034021

    Article  CAS  Google Scholar 

  51. Koribanics NM, Tuorto SJ, Lopez-Chiaffarelli N, McGuinness LR, Häggblom MM, Williams KH, Long PE, Kerkhof LJ (2015) Spatial distribution of an uranium-respiring betaproteobacterium at the Rifle, CO field research site. PLoS ONE 10(4):e0123378–e0123391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lv Q, Zhang B, Xing X, Zhao Y, Cai R, Wang W, Gu Q (2018) Biosynthesis of copper nanoparticles using Shewanella loihica PV-4 with antibacterial activity: Novel approach and mechanisms investigation. J Hazard Mater 347:141–149

    Article  CAS  PubMed  Google Scholar 

  53. Gutiérrez MF, Malaquias P, Hass V, Matos TP, Lourenço L, Reis A, Loguercio AD, Farago PV (2017) The role of copper nanoparticles in an etch-and-rinse adhesive on antimicrobial activity, mechanical properties and the durability of resin-dentine interfaces. J Dent 61:12–20

    Article  CAS  PubMed  Google Scholar 

  54. Zhu J, Uliana A, Wang J, Yuan S, Li J, Tian M, Simoens K, Volodin A, Lin J, Bernaerts K (2016) Elevated salt transport of antimicrobial loose nanofiltration membranes enabled by copper nanoparticles via fast bioinspired deposition. J Mater Chem A 4(34):13211–13222

    Article  CAS  Google Scholar 

  55. Kothari R (2018) Copper nanoparticles synthesized from cinnamomum zeylanicum and its antibacterial activity. Am J Nanosci Nanotechnol 6(1):1–7

    Google Scholar 

  56. Pramanik A, Laha D, Bhattacharya D, Pramanik P, Karmakar P (2012) A novel study of antibacterial activity of copper iodide nanoparticle mediated by DNA and membrane damage. Colloids Surf B Biointerfaces 96:50–55

    Article  CAS  PubMed  Google Scholar 

  57. Gunawan C, Teoh WY, Marquis CP, Amal R (2011) Cytotoxic origin of copper (II) oxide nanoparticles: comparative studies with micron-sized particles, leachate, and metal salts. ACS Nano 5(9):7214–7225

    Article  CAS  PubMed  Google Scholar 

  58. Sotiriou GA, Pratsinis SE (2010) Antibacterial activity of nanosilver ions and particles. Environ Sci Technol 44(14):5649–5654

    Article  CAS  PubMed  Google Scholar 

  59. Xiu Z, Zhang Q, Puppala HL, Colvin VL, Alvarez PJ (2012) Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett 12(8):4271–4275

    Article  CAS  PubMed  Google Scholar 

  60. Vincent M, Duval RE, Hartemann P, Engels-Deutsch M (2018) Contact killing and antimicrobial properties of copper. J Appl Microbiol 124(5):1032–1046

    Article  CAS  PubMed  Google Scholar 

  61. Santo CE, Lam EW, Elowsky CG, Quaranta D, Domaille DW, Chang CJ, Grass G (2011) Bacterial killing by dry metallic copper surfaces. Appl Environ Microbiol 77(3):794–802

    Article  CAS  Google Scholar 

  62. Santo CE, Quaranta D, Grass G (2012) Antimicrobial metallic copper surfaces kill Staphylococcus haemolyticus via membrane damage. MicrobiologyOpen 1(1):46–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Mathews S, Hans M, Mücklich F, Solioz M (2013) Contact killing of bacteria on copper is suppressed if bacteria-metal contact is prevented and is induced on iron by copper ions. Appl Environ Microbiol 79(8):2605–2611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Grass G, Rensing C, Solioz M (2011) Metallic copper as an antimicrobial surface. Appl Environ Microbiol 77(5):1541–1547

    Article  CAS  PubMed  Google Scholar 

  65. Gray RD (1969) Kinetics of oxidation of copper (I) by molecular oxygen in perchloric acid-acetonitrile solutions. J ACS 91(1):56–62

    CAS  Google Scholar 

  66. Millero FJ, Sharma V, Karn B (1991) The rate of reduction of copper (II) with hydrogen peroxide in seawater. Mar Chem 36(1–4):71–83

    Article  CAS  Google Scholar 

  67. Pham AN, Xing G, Miller CJ, Waite TD (2013) Fenton-like copper redox chemistry revisited: Hydrogen peroxide and superoxide mediation of copper-catalyzed oxidant production. J Catal 301:54–64

    Article  CAS  Google Scholar 

  68. Kang N, Lee DS, Yoon J (2002) Kinetic modeling of Fenton oxidation of phenol and monochlorophenols. Chemosphere 47(9):915–924

    Article  CAS  PubMed  Google Scholar 

  69. Strlic M, Kolar J, Selih V-S, Kocar D, Pihlar B (2003) A comparative study of several transition metals in Fenton-like reaction systems at circum-neutral pH. Acta Chim Slov 50(4):619–632

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Prof. Richard Partch (Department of Chemistry, Clarkson University) for allowing them to use the SEM-preparation equipment.

Author information

Authors and Affiliations

  1. Department of Chemical and Biomolecular Engineering, Clarkson University, 8 Clarkson Avenue, Potsdam, NY, 13699, USA

    Xudong Su & Selma Mededovic Thagard

  2. Institute for a Sustainable Environment, Clarkson University, 8 Clarkson Avenue, Potsdam, NY, 13699, USA

    Meng Feng

  3. Department of Civil and Environmental Engineering, Clarkson University, 8 Clarkson Avenue, Potsdam, NY, 13699, USA

    Shane Rogers & Thomas M. Holsen

Authors
  1. Xudong Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Meng Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shane Rogers
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas M. Holsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Selma Mededovic Thagard
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Selma Mededovic Thagard.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 556 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Su, X., Feng, M., Rogers, S. et al. The Role of High Voltage Electrode Material in the Inactivation of E. coli by Direct-in-Liquid Electrical Discharge Plasma. Plasma Chem Plasma Process 39, 577–596 (2019). https://doi.org/10.1007/s11090-019-09980-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11090-019-09980-x

Keywords

Search

Navigation