Abstract
Millimeter waves (MMW) or electromagnetic fields of extremely high frequencies at low intensity is a new environmental factor, the level of which is increased as technology advance. It is of interest that bacteria and other cells might communicate with each other by electromagnetic field of sub-extremely high frequency range. These MMW affected Escherichia coli and many other bacteria, mainly depressing their growth and changing properties and activity. These effects were non-thermal and depended on different factors. The significant cellular targets for MMW effects could be water, cell plasma membrane, and genome. The model for the MMW interaction with bacteria is suggested; a role of the membrane-associated proton FOF1-ATPase, key enzyme of bioenergetic relevance, is proposed. The consequences of MMW interaction with bacteria are the changes in their sensitivity to different biologically active chemicals, including antibiotics. Novel data on MMW effects on bacteria and their sensitivity to different antibiotics are presented and discussed; the combined action of MMW and antibiotics resulted with more strong effects. These effects are of significance for understanding changed metabolic pathways and distinguish role of bacteria in environment; they might be leading to antibiotic resistance in bacteria. The effects might have applications in the development of technique, therapeutic practices, and food protection technology.
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Adebayo EA, Adeeyo AO, Ayandele AA, Omomowo IO (2014) Effect of radiofrequency radiation from telecommunication base stations on microbial diversity and antibiotic resistance. J Appl Sci Environ Manag 18:669–674
Ahmed I, Istivan T, Pirogova E (2015a) Irradiation of Escherichia coli by extremely-low frequency (ELF) pulsed electromagnetic fields (PEMF): evaluation of bacterial survival. J Electromagn Waves Appl 29:26–37
Ahmed LT, Majeed AD, Shaima’a AS (2015b) The effect of mobile waves on the growth of pathogenic fungi. Int J Curr Microbiol Appl Sci 4:838–842
Alipov ED, Scheglov VS, Sarimov RM, Belyaev IY (2003) Cell-density dependent effects of low-dose ionizing radiation on E. coli cells. Radiats Biol Radioecol 43:167–171
Anton E, Rotaru A, Covatariu D, Giobica A, Timofte D, Popescu R, Anton C (2015) Links between extremely high frequency electromagnetic waves and their biological manifestations. Arch Biol Sci 67:895–897
Banik S, Bandyopadhyay S, Ganguly S (2003) Bioeffects of microwave—a brief review. Bioresour Technol 87:155–159
Belyaev I (2005) Non-thermal biological effects of microwaves. Microwave Rev 11:13–29
Belyaev IY, Scheglov VS, Alipov YD, Listsov VN (1996) Resonance effect of millimeter waves in the power range from 10−19 to 3 × 10−3 W/cm2 on Escherichia coli cells at different concentrations. Bioelectromagnetics 17:312–321
Belyaev IY, Scheglov VS, Alipov YD, Radko SP (1993) Regularities of separate and combined effects of circularly polarized millimeter waves on E. coli cells at different phases of culture growth. Bioelectrochem Bioenerg 31:49–63
Betskii OV, Devyatkov ND, Kislov VV (2000) Low intensity millimeter waves in medicine and biology. Crit Rev Biomed Eng 28:247–268
Bingi VN (2011) Principles of electromagnetic biophysics. PhysMathLit, Moscow
Buchachenko A (2016) Why magnetic and electromagnetic effects in biology are irreproducible and contradictory? Bioelectromagnetics 37:1–13
Bulgakova VG, Grushina VA, Orlova TI, Petrykina ZM, Polin AN, Noks PP, Kononenko AA, Rubin AB (1996) The effect of millimeter-band radiation of non-thermal intensity on sensitivity of Staphylococcus to various antibiotics. Biophysics 41:1315–1319
Burlakova EB, Konradov AA, Maltseva EL (2004) Effect of extremely weak chemical and physical stimuli on biological systems. Biophysics 49:522–534
Cambau E, Gutmann L (1993) Mechanisms of resistance to quinolones. Drugs 45:15–23
Caubet R, Pedarros-Caubet F, Chu M, Freye E, de Bele’m Rodrigues M, Moreau J, Ellison W (2004) A radio frequency electric current enhances antibiotic efficacy against bacterial biofilms. Antimicrob Agents Chemother 48:4662–4664
Chung C, Hung G, Lam C, Laurence M (2006) Secondary effects of streptomycin and kanamycin on macromolecular composition of Escherichia coli B23 cell. J Exp Microbiol Immunol 9:11–15
Cifra M, Fields JZ, Farhadi A (2011) Electromagnetic cellular interactions. Prog Biophys Mol Biol 105:223–246
Cohen I, Cahan R, Shani G, Cohen E, Abramovich A (2010) Effect of 99 GHz continuous millimeter wave electro-magnetic radiation on E. coli viability and metabolic activity. Int J Radiat Biol 86:390–399
Fesenko EE, Geletyuk VI, Kazachenko VN, Chemeris NK (1995) Preliminary microwave irradiation of water solutions changes their channel-modifying activity. FEBS Lett 366:49–52
Gabrielyan L, Sargsyan H, Trchounian A (2015) Effects of millimeter waves of low intensity on growth and photoproduction of hydrogen by Rhodobacter sphaeroides. In: VII Int congress “Low and Superlow Fields and radiations in Biology and Medicine”. Sci Proc, St-Petersburg (Russia), pp. 27–28
Geveke D, Brunkhorst Ch XF (2007) Radio frequency electric fields processing of orange juice. Innovative Food Sci Emerg Technol 8:549–554
Geveke DJ, Gurtler J, Zhang HQ (2009) Inactivation of Lactobacillus plantarum in apple cider, using radio frequency electric fields. J Food Prot 72:656–661
Gherardini L, Ciuti G, Tognarelli S, Cinti C (2014) Searching for the perfect wave: the effect of radiofrequency electromagnetic fields on cells. Int J Mol Sci 15:5366–5387
Golovleva V, Kopylova T, Levdikova T, Yu T (1997) Change in the electrophysical properties of water by microwave radiation. Russ Phys J 40:327–331
Guliy O, Markina L, Bunin V, Ignatov V, Ignatov O (2008) Electro-optical parameters of kanamycin-treated E. coli cell suspensions. Microbiology 77:334–338
Guofen Y, Coln E, Schoenbach K, Gellerman M, Fox P, Rec L, Beebe S, Liu S (2002) A study on biological effects of low-intensity millimeter waves. Plasm Sci 30:1489–1496
Hamnerius Y, Rasmuson Å, Rasmuson B (1985) Biological effects of high-frequency electromagnetic fields on Salmonella typhimurium and Drosophila melanogaster. Bioelectromagnetics 6:405–414
Hong S, Pedersen PL (2008) ATP synthase and the actiobns of inhibitors utilized to study its role in human health, disease, and other scientific areas. Microbiol Mol Biol Rev 72:590–641
Hwang G, Han Y, Choi SQ, Cho S, Kim H (2015) Bacterial inactivation by ultrasonic waves: role of ionic strength, humic acid, and temperature. Water Air Soil Pollut 226:1–9
Hyland GJ (2008) Physical basis of adverse and therapeutic effects of low intensity microwave radiation. Indian J Exp Biol 46:403–419
Isakhanyan V, Trchounian A (2005) Indirect and repeated electromagnetic irradiation with extremely high frequency of bacteria Escherichia coli. Biophysics 50:604–606
James C, Mahendran K, Molitor A, Bolla JM, Bessonov A, Winterhalter M, Page’s JM (2009) How β-lactam antibiotics enter bacteria: a dialogue with the porins. PLoS One 4:1–9
Kandashev V, Savin A (1997) Resonance effects of microwaves are caused by their interaction with solitons in α-helical proteins. Electro Magneto Biol 16:95–106
Kohanski M, Dwyer D, Hayete B, Lawrence C, Collins J (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130:797–810
Konovalov A, Ryzhkina I, Maltseva E, Murtazina L, Kiseleva Y, Kasparov V, Palmina N (2015) Nanoassociate formation in highly diluted water solutions of potassium phenosan with and without permalloy shielding. Electromagn Biol Med 32:141–146
Kucera O, Cervinkova K, Nerudova M, Cifra M (2015) Spectral perspective on the electromagnetic activity of cells. Curr Top Med Chem 15:513–522
Lee S, Hinz A, Bauerle E, Angermeyer A, Juhaszova K (2009) Targeting a bacterial stress response to enhance antibiotic action. Proc Natl Acad Sci U S A 106:14570–14575
Matewele P (2010) The effect of electromagnetic field on antimicrobial activity of lime oil. J Microbiol Methods 83:275–276
McLeod BR, Fortun S, Costerton JW, Stewart PS (1999) Enhanced bacterial biofilm control using electromagnetic fields in combination with antibiotics. Methods Enzymol 310:656–670
McMurry L, Hendricks M, Levy S (1986) Effects of toluene permeabilization and cell deenergization on tetracycline resistance in Escherichia coli. J Bacteriol 29:681–686
Mishra T, Kushwah P, Dholiya K, Kothari V (2013) Effect of low power microwave radiation on microorganisms and other life forms. Adv Microwave Wireless Technol 1:4–11
Nakae R, Nakae T (1982) Diffusion of aminoglycoside antibiotics across the outer membrane of Escherichia coli. Antimicrob Agents Chemother 22:554–559
Neshev N, Kirilova E (1994) Possible non-thermal influence of millimeter waves on proton transfer in biomembranes. Electro Magnet Biol 13:191–194
Nikolaev Y (2000) Distant interactions in bacteria. Microbiology 69:497–503
Novoselova EG, Glushkova OV, Sinotova OA, Fesenko EE (2005) Stress response of the cell to exposure to ultraweak electromagnetic radiation. Dokl Russ Acad Sci 401:117–119
Ohanyan V, Sargsyan H, Tadevosyan H, Trchounian A (2008) The action of low-intensity extremely high frequency electromagnetic radiation on growth parameters for bacteria. Biophysics 53:406–408
Ohanyan V, Torgomyan H, Soghomonyan D, Hovnanyan K, Trchounian A (2015) Novel data on bacterial effects of low intensity electromagnetic field in extremely high frequencies: Effects of irradiated antibiotics on Enterococcus hirae and Escherichia coli growth and morphology, ion flux alyernations fur to combined treatment of Lactobacillus acidophilus with irradiation and antibiotics. In: In VII Int Congress “Low and Superlow Fields and radiations in Biology and Medicine”. Sci Proc, St-Petersburg (Russia), p. 213
Ohanyan VA (2012) Combined effects of extremely high frequency electromagnetic field and antibiotics on Enterococcus hirae growth and survival. Rep Nat Acad Sci Armenia 112:87–94
Pakhomov AG, Murphy MB (2000) Comprehensive review of the research on biological effects of pulsed radiofrequency radiation in Russia and the former Soviet Union. In: Lin JC (ed) Advances in electromagnetic fields in living system, 3. Kluwer Acad Plenum Publ, New York, pp. 265–290
Pakhomov AG, Akyel Y, Pakhomova ON, Stuck BE, Murphy MR (1998) Current state and implications of research on biological effects of millimeter waves: a review of the literature. Bioelectromagnetics 19:393–413
Pickering SA, Bayston R, Scammell BE (2003) Electromagnetic augmentation of anbiotic efficacy in infection of orthopaedic implants. J Bone Joint Surg (Br) 85:588–593
Potselueva MM, Pustovidko AV, Evtodienko I, Khramov RN, Chaĭlakhian LM (1998) Formation of reactive oxygen species in aqueous solutions after exposure to extremely-high frequency electromagnetic fields. Rep Acad Sci 359:415–418
Presman AS (1970) Electromagnetic field and life. Plenum Press, NY & London
Ratushnyak AA, Andreeva MG, Morozova OV, Morozov GA, Trushin MV (2008) Effect of extremely high frequency electromagnetic fields on the microbiological community in rhizosphere of plants. Int Agrophys 22:71–74
Redlarski G, Lewczuk B, Zak A, Koncicki A, Krawszuk M, Piechocki J, Jakubiuk K, Tojza P, Jaworski J, Ambroziak D, Skarbek L, Gradolewski D (2015) The influence of electromagnetic pollution on living organisms: Historical trends and forecasting changes. Biomed Res Int 2015, ID 234098, 18 p.
Reguera G (2011) When microbial conversations get physical. Trends Microbiol 19:105–116
Rodrigez-Chueca J, Mediano A, Ormad MP, Mosteo R, Ovelleiro JL (2014) Disinfection of wastewater effluents with the Fenton-like process induced by electromagnetic fields. Water Res 60:250–258
Rogacheva SM, Denisova SA, Shulgin SV, Somov AL, Kuznetsov PE (2008) Biological effects of electromagnetic radiation of extremely high frequencies combined with physiologically active compounds. Radiats Biol Radioecol 48:474–480
Rojavin MA, Ziskin MC (1998) Medical application of millimetre waves. Q J Med 91:57–66
Ruediger HW (2009) Genotoxic effects of radiofrequency electromagnetic fields. Pathophysiology 16:89–102
Ryzhkina IS, Kiseleva YV, Murtazina LI, Konovalov AI (2012) Effect of ultralow concentrations and electromagnetic fields. Dokl Phys Chem 446:153–157
Schaechter M, the View from Here Group (2001) Escherichia coli and Salmonella 2000: the view from here. Microbiol Mol Biol Rev 65:119–130
Scheglov VS, Alipov ED, Belyaev IY (2002) Cell-to-cell communication in response of E. coli cells at different phases pf growth to low-intensity microwaves. Biochim Biophys Acta 1572:101–106
Shamis Y, Taube A, Shramkov Y, Mitik-Dineva N, Vu B, Ivanova E (2008) Development of a microwave treatment technique for bacterial decontamination of raw meat. Int J Food Eng 4:1–13
Shamis Y, Croft R, Taube A, Crawford RJ, Ivanova EP (2012) Review of the specific effects of microwave radition on bacterial cells. Appl Microbiol Biotechnol 96:319–325
Silva ED (2001) High frequency and microwave engineering. Butterworth-Heinemann, Oxford
Sinitsyn N, Petrosyan V, Yolkin V, Devyatkov N, Yu G, Betskii O (2000) Special function of the “millimeter wavelength waves-aqueous medium” system in nature. Crit Rev Biomed Eng 28:269–305
Soghomonyan D, Trchounian A (2013) Comparable effects of low-intensity electromagnetic irradiation at the frequency of 51.8 GHz and 53 GHz and antibiotic ceftazidime on Lactobacillus acidophilus growth and survival. Cell Biochem Biophys 67:829–835
Soghomonyan D, Kalantaryan V, Trchounian A (2014) Changes in the FOF1-ATPase activity of irradiated Lactobacillus acidophilus in the presence of ceftazidime at low pH. Biolog J Armenia 66(3):39–43
Tadevosyan H, Trchounian A (2009) Effects of coherent extremely high frequency and low intensity electromagnetic radiation on the activity of membrane systems of Escherichia coli bacteria. Biofizika 54:1055–1059
Tadevosyan H, Kalantaryan V, Trchounian A (2007) The effects of electromagnetic radiation of extremely high frequency and low intensity on the growth rate of Escherichia coli and the role of medium pH. Biophysics 52:893–898
Tadevosyan H, Kalantaryan V, Trchounian A (2008) Extremely high frequency electromagnetic radiation enforces bacterial effects of inhibitors and antibiotics. Cell Biochem Biophys 51:97–103
Torgomyan H, Trchounian A (2011) Low-intensity electromagnetic irradiation of 70.6 and 73 GHz frequencies enhances the effects of disulfide bonds reducer on Escherichia coli growth and affects the bacterial surface oxidation–reduction state. Biochem Biophys Res Commun 414:265–269
Torgomyan H, Trchounian A (2012) Escherichia coli membrane-associated energy-dependent processes and sensitivity toward antibiotics changes as responses to low-intensity electromagnetic irradiation of 70.6 and 73 GHz frequencies. Cell Biochem Biophys 62:451–461
Torgomyan H, Trchounian A (2013) Bactericidal effects of low-intensity extremely high frequency electromagnetic field: an overview with phenomenon, mechanisms, targets and consequences. Crit Rev Microbiol 39:102–111
Torgomyan H, Trchounian A (2015) The enhanced effects of antibiotics irradiated of extremely high frequency electromagnetic field on Escherichia coli growth properties. Cell Biochem Biophys 71:419–424
Torgomyan H, Kalantaryan V, Trchounian A (2011a) Low intensity electromagnetic irradiation with 70.6 and 73 GHz frequencies affects Escherichia coli growth and changes water properties. Cell Biochem Biophys 60:275–281
Torgomyan H, Tadevosyan H, Trchounian A (2011b) Extremely high frequency electromagnetic irradiation in combination with antibiotics enhances antibacterial effects on Escherichia coli. Curr Microbiol 62:962–967
Torgomyan H, Ohanyan V, Blbulyan S, Kalantaryan V, Trchounian A (2012) Electromagnetic irradiation of Enterococcus hirae at low-intensity 51.8 and 53.0 GHz frequencies: changes in bacterial cell membrane properties and enhanced antibiotics effects. FEMS Microbiol Lett 329:131–137
Torgomyan H, Hovnanyan K, Trchounian A (2013a) Escherichia coli growth changes by the mediated effects after low-intensity electromagnetic irradiation of extremely high frequencies. Cell Biochem Biophys 65:445–454
Torgomyan H, Ohanyan V, Blbulyan S, Trchounian A (2013b) Changes in ion transport through membranes, ATPase activity and antibiotics effects in Enterococcus hirae after low intensity electromagnetic irradiation of 51.8 and 53.0 GHz frequencies. Biophysics 58:524–529
Trchounian A (2004) Escherichia coli proton-translocating F0F1-ATP synthase and its association with solute secondary transpopters and/or enzymes of anaerobic oxidation-reduction under fermentation. Biochem Biophys Res Commun 315:1051–1057
Trchounian A, Sawers RG (2014) Novel insights into the bioenergetics of mixed-acid fermentation: can hydrogen and proton cycles combine to help maintain a proton motive force? IUBMB Life 66:1–7
Trchounian A, Ogandzhanyan E, Sarkisyan E, Gonyan S, Oganesyan A, Oganesyan S (2001) Membranotropic effects of electromagnetic radiation of extremely high frequency in Escherichia coli. Biophysics 46:69–76
Trushin MV (2003) Culture-to-culture physical interactions causes the alteration in red and infrared light stimulation of Escherichia coli growth rate. J Microbiol Immunol Infect 36:149–152
Ukuku D, Geveke D, Cooke P, Zhang H (2008) Membrane damage and viability loss of K-12 in apple juice treated with radio frequency electric field. J Food Prot 71:684–690
Usichenko TI, Edinger H, Gizhko VV, Lehmann C, Wendt M, Feyerherd F (2006) Low-intensity electromagnetic millimeter waves for pain therapy. Evid Compl Alter Med 3:201–207
Xu A, Lin X, Ren H, Zhang Y, Wang S, Peng X (2006) Analysis of outer membrane proteome of Escherichia coli related to resistance to ampicillin and tetracycline. Proteome 6:462–473
Yadollahpour A, Jalilifar M, Rashidi S (2014) Antimicrobial effects of electromagnetic fields: A review of current techniques and mechanisms of action. J Pure Appl Microbiol 8:4031–4043.
Zand N, Foroudi F, Mailova E, Voskanyan A (2010) Sterilization of flexible pouch by high frequency electromagnetic induction, using cooked chick and chick meal. Afr J Microbiol Res 4:2011–2021
Zohre R, Yadollahpour A, Mostafa J, Samaneh R (2015) Nondrug antimicrobial techniques: electromagnetic fields and photodynamic therapy. Biomed Pharmacol J 8:147–155
Acknowledgments
The authors thank Dr. V. Kalantaryan (Department of Telecommunication and High Frequency Radiophysics, Yerevan State University, Armenia) for discussion and advice. The study was done within the framework of Basic Support of State Committee of Science, Ministry of Education and Science of Armenia (#10-3/9).
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Soghomonyan, D., Trchounian, K. & Trchounian, A. Millimeter waves or extremely high frequency electromagnetic fields in the environment: what are their effects on bacteria?. Appl Microbiol Biotechnol 100, 4761–4771 (2016). https://doi.org/10.1007/s00253-016-7538-0
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DOI: https://doi.org/10.1007/s00253-016-7538-0