Magnesium magnetic isotope effects in microbiology

Abstract

Two main properties of atomic nuclei—mass and nuclear magnetic moments—are origin of many biological effects. Mass-dependent isotope effects have been studied for a long time. The effect of magnetic isotopes having a magnetic moment and spin was first shown in the early twenty-first century for the magnetic isotope magnesium 25Mg on enzymatic ATP synthesis. This stimulated the search for experimental evidence and theoretical justification of magnetic nuclei influence on biological processes. This review contains the results of scientific research on the magnesium magnetic isotope effects in microbiology. Microorganisms have been found to be sensitive to the presence of nuclear magnetic moment of magnesium isotope 25Mg compared with non-magnetic 24,26Mg isotopes.

This is a preview of subscription content, access via your institution.

Availability of data and materials

Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.

References

  1. 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 13:1205–1218

    CAS  PubMed  Article  Google Scholar 

  2. Andreini C, Bertini I, Cavallaro G, Holliday GL, Thornton JM (2009) Metal-MACiE: a database of metals involved in biological catalysis. Bioinformatics 25(16):2088–2089

    CAS  PubMed  Article  Google Scholar 

  3. Andriole VT (2005) The quinolones: past, present, and future. Clin Infect Dis 41(2):113–119

    Article  Google Scholar 

  4. Avdeeva LV, Koltover VK (2016) Nuclear spin catalysis in living nature. Moscow Univ Chem Bull 71:160–166

    Article  Google Scholar 

  5. Avdeeva LV, Evstyukhina TA, Koltover VK, Korolev VG, Kutlakhmedov YA (2019) Recovery of the yeast cells from radiation injuries by means of the magnetic isotopes: new trend in anti-radiation biomedicine. Nucl Phys Energy 20(3):271–277

    Article  Google Scholar 

  6. Berry D, Mader E, Lee TK, Woebken D, Wang Y, Zhu D, Palatinszky M, Schintlmeister A, Schmid MC, Hanson BT, Shterzer N, Mizrahi I, Rauch I, Decker T, Bocklitz T, Popp J, Gibson CM, Fowler PW, Huang WE, Wagner M (2015) Tracking heavy water (D2O) incorporation for identifying and sorting active microbial cells. Proc Natl Acad Sci USA 112(2):E194–E203

    CAS  PubMed  Article  Google Scholar 

  7. Bist P, Rao DN (2003) Identification and mutational analysis of Mg2+ binding site in EcoP15I DNA methyltransferase: involvement in target base eversion. J Biol Chem 278:41837–41848

    CAS  PubMed  Article  Google Scholar 

  8. Blakemore R (1975) Magnetotactic bacteria. Science 190:377–379

    CAS  PubMed  Article  Google Scholar 

  9. Bock AK, Glasemacher J, Schmidt R, Schönheit P (1999) Purification and characterization of two extremely thermostable enzymes, phosphate acetyltransferase and acetate kinase, from the hyperthermophilic eubacterium Thermotoga maritima. J Bacteriol 181:1861–1867

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. Bowen HJM (1960) Biological fractionation of isotopes. Int J Appl Radiat Isot 7:261–272

    CAS  PubMed  Article  Google Scholar 

  11. Buchachenko AL (2009) Magnetic isotope effect in chemistry and biochemistry. Nova Science Publishers, New York

    Google Scholar 

  12. Buchachenko AL (2014a) Magneto-biology and medicine. Nova Science Publishers, New York

    Google Scholar 

  13. Buchachenko AL (2014b) Magnetic field-dependent molecular and chemical processes in biochemistry, genetics and medicine. Russ Chem Rev 83:1–12

    Article  CAS  Google Scholar 

  14. Buchachenko AL, Kuznetsov DA, Arkhangelsky SE, Orlova MA, Markaryan AA (2005a) Magnetic isotope effect of magnesium in phosphoglycerate kinase phosphorylation. Proc Natl Acad Sci USA 102:10793–10796

    CAS  PubMed  Article  Google Scholar 

  15. Buchachenko AL, Kuznetsov DA, Arkhangelsky SE, Orlova MA, Markaryan AA (2005b) Dependence of mitochondrial ATP synthesis on the nuclear magnetic moment of magnesium ions. Cell Biochem Biophys 43:243–252

    CAS  PubMed  Article  Google Scholar 

  16. Buchachenko AL, Kuznetsov DA, Berdinsky VL (2006) New mechanisms of biological effects of electromagnetic fields. Biophysics 51(3):489–496

    Article  Google Scholar 

  17. Buchachenko AL, Kuznetsov DA, Breslavskaya NN, Shchegoleva LN, Arkhangelsky SE (2011) Calcium induced ATP synthesis: isotope effect, magnetic parameters and mechanism. Chem Phys Lett 505:130–134

    CAS  Article  Google Scholar 

  18. Buchachenko AL, Orlov AP, Kuznetsov DA, Breslavskaya NN (2013) Magnetic isotope and magnetic field effects in the DNA synthesis. Nucl Acids Res 41:8300–8307

    CAS  PubMed  Article  Google Scholar 

  19. Buchachenko AL, Bukhvostov AA, Ermakov KV, Kuznetsov DA (2020) A specific role of magnetic isotopes in biological and ecological systems. Physics and biophysics beyond. Prog Biophys Mol Biol 155:1–19

    CAS  PubMed  Article  Google Scholar 

  20. Chakrabarti G, Kim S, Gupta MLJ, Barton JS, Himes RH (1999) Stabilization of tubulin by deuterium oxide. Biochemistry 38:3067–3072

    CAS  PubMed  Article  Google Scholar 

  21. Cioni P, Strambini GB (2002) Effect of heavy water on protein flexibility. Biophys J 82:3246–3253

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  22. Creek DJ, Chokkathukalam A, Jankevics A, Burgess KEV, Breitling R, Barrett MP (2012) Stable isotope-assisted metabolomics for network-wide metabolic pathway elucidation. Anal Chem 84(20):8442–8447

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. Crespi HL (1982) The isolation of deuterated bacteriorhodopsin from fully deuterated Halobacterium halobium. Methods Enzymol 88:3–5

    CAS  Article  Google Scholar 

  24. Gardner KH, Kay LE (1998) The use of 2H, 13C, 15N multidimensional NMR to study the structure and dynamics of proteins. Annu Rev Biophys Biomol Struct 27:357–406

    CAS  PubMed  Article  Google Scholar 

  25. Guthertz N, Klopp J, Winterhalter A, Fernandez C, Gossert AD (2015) Auto-inducing media for uniform isotope labeling of proteins with 15N, 13C and 2H. J Biomol NMR 62:169–177

    CAS  PubMed  Article  Google Scholar 

  26. Katz JJ, Crespi HL (1966) Deuterated organisms: cultivation and uses. Science 151:1187–1194

    CAS  PubMed  Article  Google Scholar 

  27. Koltover VK (2019) Radiative aspects in physics of liquid matter: stable magnetic isotopes as new trend in anti-radiation defense. Proc Phys 223:301–312

    CAS  Google Scholar 

  28. Koltover VK, Shevchenko UG, Avdeeva LV, Royba EA, Berdinsky VL, Kudryashova EA (2012) Magnetic-isotope effect of magnesium in the living cell. Dokl Biochem Biophys 442:12–14

    CAS  PubMed  Article  Google Scholar 

  29. Kselikova V, Vitova M, Bisova K (2019) Deuterium and its impact on living organisms. Folia Microbiol 64:673–681

    CAS  Article  Google Scholar 

  30. Leclercq R (2002) Mechanisms of resistance to macrolides and lincosamides: nature of the resistance elements and their clinical implications. Antimicrob Resist 34:482–492

    CAS  Google Scholar 

  31. Letuta UG (2020) Combined effect of magnesium isotopes and antibiotics on morphology of E. coli. J Phys Conf Ser 1611(1):012021

    CAS  Article  Google Scholar 

  32. Letuta UG, Avdeeva EI (2017) Magnetic-dependent ATP pool in Escherichia coli. Dokl Biochem Biophys 474(1):196–199

    CAS  PubMed  Article  Google Scholar 

  33. Letuta UG, Berdinskii VL (2015) Enzymatic mechanisms of biological magnetic sensitivity: nuclear spin effects. Russ Chem Bull 64(7):1547–1554

    CAS  Article  Google Scholar 

  34. Letuta UG, Berdinskiy VL (2017) Magnetosensitivity of bacteria E. coli: magnetic isotope and magnetic field effects. Bioelectromagnetics 38(8):581–591

    CAS  PubMed  Article  Google Scholar 

  35. Letuta UG, Berdinskiy VL (2019) Biological effects of static magnetic fields and zinc isotopes on E. coli bacteria. Bioelectromagnetics 40(1):62–73

    CAS  PubMed  Article  Google Scholar 

  36. Letuta UG, Tikhonova TA (2019) Magnetic fields and magnetic isotope 25Mg effects on biofilms formation by bacteria E. coli. Dokl Biochem Biophys 484(1):85–87

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  37. Letuta UG, Tikhonova TA (2020) The magnetic isotopes effect of magnesium 25Mg on the physiological properties of bacteria E. coli. J Phys Conf Ser 1443(1):012016

    CAS  Article  Google Scholar 

  38. Letuta UG, Avdeeva EI, Berdinsky VL (2014) Magnetic field effects in bacteria E. coli in the presence of Mg isotopes. Russ Chem Bull 63(5):1102–1106

    CAS  Article  Google Scholar 

  39. Letuta UG, Vekker AS, Kornilova TA, Gryaznov AA, Cheplakov IA (2016) Magnetic isotope effect of magnesium 25Mg on E. coli resistance to antibiotics. Dokl Biochem Biophys 469(1):281–283

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  40. Letuta UG, Berdinskiy VL, Udagawa C, Tanimoto Y (2017) Enzymatic mechanisms of biological magnetic sensitivity. Bioelectromagnetics 38(7):511–521

    CAS  PubMed  Article  Google Scholar 

  41. Letuta UG, Binder AS, Tikhonova TA (2020) Effect of magnesium isotopes on antibiotic sensitivity of E. coli. Microbiology 89(3):273–277

    CAS  Article  Google Scholar 

  42. Li Y, Green KD, Johnson BR, Garneau-Tsodikova S (2015) Inhibition of aminoglycoside acetyltransferase resistance enzymes by metal salts. Antimicrob Agents Chemother 59:4148–4156

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  43. Mackay GM, Zheng L, van den Broek NJ, Gottlieb E (2015) Analysis of cell metabolism using LC–MS and isotope tracers. Methods Enzymol 561:171–196

    CAS  PubMed  Article  Google Scholar 

  44. McCready RGL, Laishley EJ, Krouse HR (1976) The use of stable sulfur isotope labelling to elucidate sulfur metabolism by Clostridium pasteurianum. Arch Microbiol 109:315–317

    CAS  PubMed  Article  Google Scholar 

  45. McIntosh LP, Dahlquist FW (1989) Biosynthetic incorporation of 15N and 13C. Q Rev Biophys 23:1–38

    Article  Google Scholar 

  46. Muchmore DC, McIntosh LP, Russel CB et al (1989) Expression and nitrogen-15 labeling of proteins for proton and nitrogen-15 nuclear magnetic resonance. Methods Enzymol 177:44–73

    CAS  PubMed  Article  Google Scholar 

  47. Mueller D, Heinzle E (2013) Stable isotope-assisted metabolomics to detect metabolic flux changes in mammalian cell cultures. Curr Opin Biotechnol 24(1):54–59

    CAS  PubMed  Article  Google Scholar 

  48. Nies DH, Silver S (2007) Molecular microbiology of heavy metals. Springer Science & Business Media, Berlin

    Google Scholar 

  49. Osburn MR, Dawson KS, Fogel ML, Alex L (2016) Sessions fractionation of hydrogen isotopes by sulfate- and nitrate-reducing bacteria. Front Microbiol 7:1166

    PubMed  PubMed Central  Article  Google Scholar 

  50. Ramirez MS, Tolmasky ME (2017) Amikacin: uses, resistance, and prospects for inhibition. Molecules 22:2267–2290

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  51. Ramirez MS, Nikolaidis N, Tolmasky ME (2013) Rise and dissemination of aminoglycoside resistance: the AAC(6′)-Ib paradigm. Front Microbiol 4:121

    PubMed  PubMed Central  Article  Google Scholar 

  52. Rittie L, Perbal B (2008) Enzymes used in molecular biology: a useful guide. J Cell Commun Signal 2:25–45

    PubMed  PubMed Central  Article  Google Scholar 

  53. Romani AMP (2011) Cellular magnesium homeostasis. Arch Biochem Biophys 512(1):1–23

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  54. Shevchenko UG, Berdinskii VL (2011) Enzymic processes as a mechanism of biological magnetoreception. Russ J Phys Chem B 5(3):519–524

    CAS  Article  Google Scholar 

  55. Shevchenko UG, Avdeeva EI, Berdinskii VL (2012) Biological effects of the 25Mg magnetic isotope in E. coli cells. Russ J Phys Chem B 6(4):531–537

    CAS  Article  Google Scholar 

  56. Sideris EG, Mukherjee R, Vomvoyanni V (1975) Effect of deuterium water on the mitotic cycle, the deoxyribonucleic acid stability, and the frequency of radiation induced chromosome aberrations in barley. Radiat Res 61:457–467

    CAS  PubMed  Article  Google Scholar 

  57. Surkov AV, Michael EB, Kuever J (2000) Stable sulfur isotope fractionation during the reduction of thiosulfate by Dethiosulfovibrio russensis. Arch Microbiol 174:448–451

    CAS  PubMed  Article  Google Scholar 

  58. Vanatulu K, Paalme T, Vilu R, Burkhardt N, Jünemann R, May R, Rühl M, Wadzack J, Nierhaus KH (1993) Large-scale preparation of fully deuterated cell components: ribosomes from Escherichia coli with high biological activity. Eur J Biochem 216:315–321

    Article  Google Scholar 

  59. Vasilescu V, Katona E (1986) Deuteration as a tool in investigating the role of water in the structure and function of excitable membranes. Methods Enzymol 127:662–678

    CAS  PubMed  Article  Google Scholar 

  60. Wackett LP, Dodge AG, Ellis LBM (2004) Microbial genomics and the periodic table. Appl Environ Microbiol 70(2):647–655

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  61. Walker GM (1994) The roles of magnesium in biotechnology. Crit Rev Biotechnol 14:311–354

    CAS  PubMed  Article  Google Scholar 

  62. Yang XY, Chen WP, Rendahl AK, Hegeman AD, Gray WM, Cohen JD (2010) Measuring the turnover rates of Arabidopsis proteins using deuterium oxide: an auxin signaling case study. Plant J 63(4):680–695

    CAS  PubMed  Article  Google Scholar 

  63. Zachledera V, Vitovaa M, Hlavovaa M, Moudrikovab S, Mojzesb HH, Becherc JR, Bisova K (2018) Stable isotope compounds—production, detection, and application. Biotechnol Adv 36:784–797

    Article  CAS  Google Scholar 

  64. Zhang X, Gillespie AL, Sessions AL (2009) Large D/H variations in bacterial lipids reflect central metabolic pathways. Proc Natl Acad Sci USA 106:12580–12586

    PubMed  Article  Google Scholar 

Download references

Funding

This work was financially supported by the Council for grants of the President of the Russian Federation, the application of SP-225.2019.4, and by the Ministry of Science and Higher Education of the Russian Federation, Project No. FSGU-2020-0003.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ulyana G. Letuta.

Ethics declarations

Conflict of interest

None of the authors have any conflict of interests to declare.

Consent for publication

Yes.

Consent to participate

Yes.

Additional information

Publisher's Note

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

Communicated by Erko Stackebrandt.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Letuta, U.G. Magnesium magnetic isotope effects in microbiology. Arch Microbiol (2021). https://doi.org/10.1007/s00203-021-02219-4

Download citation

Keywords

  • Magnetic isotope effect
  • Magnesium
  • Bacteria
  • ATP
  • Biofilm formation
  • Antibiotic resistance