Application of Sulfate-reducing Bacteria in Bioremediation from Heavy Metals and Metalloids (Review)

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Abstract

Pollution of the environment with heavy metals, metalloids and radionuclides is a global problem that seriously affects the state of the biosphere. In particular, chromium compounds have a toxic, mutagenic and carcinogenic effect. The main principle of purification of anthropogenic and natural ecosystems from chromates is the reduction of Cr(VI) to Cr(III), the salts of which are significantly less toxic and insoluble. However, currently used electrochemical and ion-exchange cleaning methods are quite expensive and require the use of special reagents. At the same time, sulfate-reducing bacteria (SRB) are of particular interest for bioremediation of this kind, since many of them are very resistant to high concentrations of heavy metals and are able to effectively reduce them in the presence of hydrogen as an electron donor. The review summarizes known data on the interaction of heavy metals, metalloids and radionuclides with SRB. The features of the metabolism of these microorganisms, leading to intracellular accumulation of heavy metals and metalloids, are considered. Complex and finely regulated enzymatic mechanisms for the reduction of toxic metals (using various cytochromes, hydrogenases, oxidoreductases, highly specific metal reductases, and thioredoxin/thioredoxin-reductase systems), as well as the possibility of using immobilized cells and biofilms of SRB in the effective bioremediation of natural waters, soils, and industrial effluents, are described.

About the authors

A. L. Bryukhanov

Lomonosov Moscow State University, Faculty of Biology

Email: tanya_khijniak@mail.ru
Russia, 119234, Moscow

T. V. Khijniak

Winogradsky Institute of Microbiology, Federal Research Center “Fundamentals of Biotechnology” RAS

Author for correspondence.
Email: tanya_khijniak@mail.ru
Russia, 119071, Moscow

References

  1. Lovley D.R. // Ann. Rev. Microbiol. 1993. V. 47. P. 263–290.
  2. Michel C., Brugna M., Aubert C., Bernadac A., Bruschi M. // Appl. Microbiol. Biotechnol. 2001. V. 55. № 1. P. 95–100.
  3. Goulhen F., Gloter A., Guyot F., Bruschi M. // Appl. Microbiol. Biotechnol. 2006. V. 71. № 6. P. 892–897.
  4. Li X., Fan M., Liu L., Chang J., Zhang J. // Water Sci. Technol. 2019. V. 80. № 12. P. 2362–2372.
  5. Muyzer G., Stams A.J.M. // Nat. Rev. Microbiol. 2008. V. 6. № 6. P. 441–454.
  6. Ravenschlag K., Sahm K., Knoblauch C., Jørgensen B.B., Amann R. // Appl. Environ. Microbiol. 2000. V. 66. P. 3592–3602.
  7. Jørgensen B.B., Findlay A.J., Pellerin A. // Front Microbiol. 2019. V. 10. article 849. https://doi.org/10.3389/fmicb.2019.00849
  8. Minz D., Flax J.L., Green S.J., Muyzer G., Cohen Y., Wagner M., Rittmann B.E., Stahl D.A. // Appl. Environ. Microbiol. 1999. V. 65. № 10. P. 4666–4671.
  9. Korneeva V.A., Pimenov N.V., Krek A.V., Tourova T.P., Bryukhanov A.L. // Microbiology. 2015. V. 84. № 2. P. 297–306.
  10. Ramsing N.B., Kühl M., Jørgensen B.B. // Appl. Environ. Microbiol. 1993. V. 59. № 11. P. 3840–3849.
  11. Dopson M., Johnson D.B. // Environ Microbiol. 2012. V. 14. № 10. P. 2620–2631.
  12. Sorokin D.Y., Cherhyh N.A. // Int. J. Syst. Evol. Microbiol. 2017. V. 67. № 2. P. 396–401.
  13. Jeanthon C., L’Haridon S., Cueff V., Banta A., Reysenbach A.L., Prieur D. // Int. J. Syst. Evol. Microbiol. 2002. V. 52. № 3. P. 765–772.
  14. Brioukhanov A., Pieulle L., Dolla A. // Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology. V. 2. / Ed. A. Mendez-Vilas. Badajoz, Formatex Research Center, 2010. P. 148–159.
  15. Li X., Krumholz L.R. // J. Bacteriol. 2009. V. 191. № 15. P. 4924–4933.
  16. Bradl H.B. Heavy Metals in the Environment: Origin, Interaction and Remediation. London, Elsevier / Academic Press, 2005. 269 p.
  17. Herawati N., Suzuki S., Hayashi K., Rivai I.F., Koyoma H. // Bull. Environ. Contam. Toxicol. 2000. V. 64. № 1. P. 33–39.
  18. Tokar E.J., Boyd W.A., Freedman J.H., Waalkes M.P. Toxic Effects of Metals. / Casarett and Doull’s Toxicology: The Basic Science of Poisons 8th Ed. / Ed. C.D. Klaassen. N.Y., McGraw Hill, 2013. P. 981–1030.
  19. Nriagu J.O., Pacyna J.M. // Nature. 1988. V. 333. № 6169. P. 134–139.
  20. Nriagu J.O. // Nature. 1989. V. 338. № 6210. P. 47–49
  21. Tchounwou P.B., Yedjou C.G., Patlolla A.K., Sutton D.J. // Exp. Suppl. 2012. V. 101. P. 133–164.
  22. Kaczynski S.E., Kieber R.J. // Environ. Sci. Technol. 1993. V. 27. № 8. P. 1572–1576.
  23. Richard F.C., Bourg A.C.M. // Water Res. 1991. V. 25. № 7. P. 807–816.
  24. Wang Y., Su H., Gu Y., Song X., Zhao J. // Onco. Targets Ther. 2017. V. 10. P. 4065–4079.
  25. Sharma D.C., Chatterjee C., Sharma C.P. // Plant Sci. 1995. V. 111. № 2. P. 145–151.
  26. Venitt S., Levy L.S. // Nature. 1974. V. 250. № 5466. P. 493–495.
  27. Chandra P., Sinha S., Rai U.N. In: Phytoremediation of Soil and Water Contaminants. / Eds. E.L. Kruger, T.A. Anderson, J.R. Coats. ACS Symposium Series № 664. Washington DC, American Chemical Society, 1997. P. 274–282.
  28. Kotaś J., Stasicka Z. // Environ. Pollut. 2000. V. 107. № 3. P. 263–283.
  29. Stein K., Schwedt G. // Fresenius’ J. Anal. Chem. 1994. V. 350. P. 38–43.
  30. Bernhoft R.A. // ScientificWorldJournal. 2013. ID 394652. https://doi.org/10.1155/2013/394652
  31. Wedepohl K.H. // Geochim. Cosmochim. Acta. 1995. V. 59. № 7. P. 1217–1232.
  32. Nordberg G.F., Nogawa K., Nordberg M., Friberg L. Cadmium / Handbook on the Toxicology of Metals. / Eds. G.F. Nordberg, B.F. Fowler, M. Nordberg, L. Friberg. Amsterdam, Elsevier, 2007. P. 445–486.
  33. Jiang W., Fan W. // Ann. N.Y. Acad. Sci. 2008. V. 1140. P. 446–454.
  34. Stoeppler M. Arsenic / Elements and Their Compounds in the Environment: Occurrence, Analysis, and Biological Relevance. 2nd Ed. / Eds. E. Merian, M. Anke, M. Inhat, M. Stoeppler. Weinheim, Wiley-VCH, 2004. P. 1321–1364.
  35. Rüde T.R. Beiträge zur Geochemie des Arsens. / Karlsruher Geochemische Hefte: Schriftenreihe des Instituts für Petrographie und Geochemie. 1996. V. 10. P. 206–210.
  36. Smedley P.L., Kinniburgh D.G. // Appl. Geochem. 2002. V. 17. № 5. P. 517–568
  37. Sadler R., Olszowy H., Shaw G., Biltoft R., Connell D. // Water Air Soil Pollut. 1994. V. 78. № 1. P. 189–198.
  38. Chappell W., Beck B., Brown K., Chaney R., Cothern C., Irgolic K., North D., Thornton I., Tsongas T. // Environ. Health Perspect. 1997. V. 105. № 10. P. 1060–1067.
  39. Bissen M., Frimmel F.H. // Acta Hydrochim. Hydrobiol. 2003. V. 3l. № 1. P. 9–l8.
  40. Tchounwou P.B., Patlolla A.K., Centeno J.A. // Toxicol. Pathol. 2003. V. 31. № 6. P. 575–588.
  41. Hughes M.F. // Toxicol. Lett. 2002. V. 133. № 1. P. 1–16.
  42. McNeal J.M., Balistrieri L.S. Geochemistry and Occurrence of Selenium: an Overview. In: Selenium in Agriculture and the Environment. V. 23. / Ed. L.W. Jacobs. Soil Science Society of America, 1989. P. 1–13.
  43. Lakin H.W. // Geol. Soc. Am. Bull. 1973. V. 83. № 1. P. 181–190.
  44. Emsley J. Uranium / Nature’s Building Blocks: An A to Z Guide to the Elements. / Ed. J. Emsley. Oxford, Oxford University Press, 2001. P. 476–482.
  45. Arfsten D.P., Still K.R., Ritchie G.D. // Toxicol. Ind. Health. 2001. V. 17. № 5–10. P. 180–191.
  46. Macaskie L.E. // Crit. Rev. Biotechnol. 1991. V. 11. № 1. P. 41–112.
  47. Cataldo D.A., Garland T.R., Wildung R.E., Fellows R.J. // Health Phys. 1989. V. 57. № 2. P. 281–288.
  48. Гвоздяк П.И., Могилевич Н.Ф., Рыльский А.Ф., Грищенко Н.И. // Микробиология. 1986. Т. 55. № 6. С. 962–965.
  49. Yamamoto K., Kato J., Yano T., Ohtake H. // Biotechnol. Bioeng. 1993. V. 41. № 1. P. 129–133.
  50. Hardoyo J.K., Ohtake H. // J. Gen. Appl. Microbiol. 1991. V. 37. P. 519–522.
  51. Lovley D.R., Phillips E.J.P. // Appl. Environ. Microbiol. 1992. V. 58. № 3. P. 850–856.
  52. Coleman M.L., Hedrick D.B., Lovley D.R., White D.C., Pye K. // Nature. 1993. V. 361. P. 436–438.
  53. Lovley D.R., Phillips E.J.P. // Appl. Environ. Microbiol. 1994. V. 60. № 2. P. 726–728.
  54. Assfalg M., Bertini I., Bruschi M., Michel C., Turano P. // Proc. Natl. Acad. Sci. USA. 2002. V. 99. № 15. P. 9750–9754.
  55. Chardin B., Giudici-Orticoni M.T., De Luca G., Guigliarelli B., Bruschi M. // Appl. Microbiol. Biotechnol. 2003. V. 63. № 3. P. 315–321.
  56. Macy J.M., Santini J.M., Pauling B.V., O’Neill A.H., Sly L.I. // Arch. Microbiol. 2000. V. 173. № 1. P. 49–57.
  57. Mabbett A.N., Lloyd J.R., Macaskie L.E. // Biotechnol. Bioeng. 2002. V. 79. № 4. P. 389–397.
  58. Chardin B., Dolla A., Chaspoul F., Fardeau M.L., Gallice P., Bruschi M. // Appl. Microbiol. Biotechnol. 2002. V. 60. № 3. P. 352–360.
  59. Cypionka H. // Annu. Rev. Microbiol. 2000. V. 54. P. 827–848.
  60. Franco L.C., Steinbeisser S., Zane G.M., Wall J.D., Fields M.W. // Appl. Microbiol. Biotechnol. 2018. V. 102. № 6. P. 2839–2850.
  61. Gu W., Zheng D., Li D., Wei C., Wang X., Yang Q., Tian C., Cui M. // Chemosphere. 2021. V. 279. Article 130437. https://doi.org/10.1016/j.chemosphere.2021.130437
  62. Ohtake H., Cervantes C., Silver S. // J. Bacteriol. 1987. V. 169. № 8. P. 3853–3856.
  63. Smith W.L., Gadd G.M. // J. Appl. Microbiol. 2000. V. 88. № 6. P. 983–991.
  64. Battaglia-Brunet F., Foucher S., Denamur A., Ignatiadis I., Michel C., Morin D. // J. Ind. Microbiol. Biotechnol. 2002. V. 28. № 3. P. 154–159.
  65. Kim I.H., Choi J.-H., Joo J.O., Kim Y.-K., Choi J.-W., Oh B.-K. // J Microbiol. Biotechnol. 2015. V. 25. № 9. P. 1542–1546.
  66. Lin W-H., Chen C.-C., Ou J.-H., Sheu Y.-T., Hou D., Kao C.-M. // Chemosphere. 2022. V. 295. Article 133877.
  67. Cheung K.H., Gu J.D. // Chemosphere. 2003. V. 52. № 9. P. 1523–1529.
  68. Singh R., Kumar A., Kirrolia A., Kumar R., Yadav N., Bishnoi N.R., Lohchab R.K. // Bioresour. Technol. 2011. V. 102. № 2. P. 677–682.
  69. Qian J., Wei L., Liu R., Jiang F., Hao X., Chen G.-H. // Sci. Rep. 2016. V. 6. Article 23694. doi.org/https://doi.org/10.1038/srep23694
  70. Li X., Fan M., Ling Liu L., Jinghua Chang J., Jiawen Zhang J. // Water Sci. Technol. 2019. V. 80. № 12. P. 2362–2372.
  71. Humphries A.C., Mikheenko I.P., Macaskie L.E. // Biotechnol. Bioeng. 2006. V. 94. № 1. P. 81–90.
  72. Naz N., Young H.K., Ahmed N., Gadd G.M. // Appl. Environ. Microbiol. 2005. V. 71. № 8. P. 4610–4618.
  73. Jiang Y., Zhang J., Wen Q., Zheng J., Zhang Y., Wei Q., Qin Y., Zhang X. // Biodegradation. 2022. V. 33. № 3. P. 239–253.
  74. Gonçalves M.M., de Oliveira Mello L.A., da Costa A.C. // Appl. Biochem. Biotechnol. 2008. V. 147 № 1–3. P. 97–105.
  75. Newman D.K., Beveridge T.J., Morel F.M.M. // Appl. Environ. Microbiol. 1997. V. 63. № 5. P. 2022–2028.
  76. Newman D.K., Kennedy E.K., Coates J.D., Ahmann D., Ellis D.J., Lovley D.R., Morel F.M. // Arch. Microbiol. 1997. V. 168. № 5. P. 380–388.
  77. Upadhyaya G., Clancy T.M., Brown J., Hayes K.F., Raskin L. // Environ. Sci. Technol. 2012. V. 46. № 21. P. 11702–11709.
  78. Le Pape P., Battaglia–Brunet F., Parmentier M., Joulian C., Gassaud C., Fernandez-Rojo L., Guigner J.-M., Ikogou M., Stetten L., Olivi L., Casiot C., Morin G. // J. Hazard. Mater. 2017. V. 321. P. 764–772.
  79. Sun J., Hong Y., Guo J., Yang J., Huang D., Lin Z., Jiang F. // Water Res. 2019. V. 151. P. 362–370.
  80. Gao J., Zheng T., Deng Y., Jiang H. // Sci. Total Environ. 2021. V. 768. Article 144709.
  81. Taylor B., Oremland R. // Curr. Microbiol. 1979. V. 3. P. 101–103.
  82. Newport P.J., Nedwell D.B. // J. Appl. Bacteriol. 1988. V. 65. № 5. P. 419–423.
  83. Valente F.M., Almeida C.C., Pacheco I., Carita J., Saraiva L.M., Pereira I.A. // J. Bacteriol. 2006. V. 188. № 9. P. 3228–3235.
  84. Hockin S.L., Gadd G.M. // Appl. Environ. Microbiol. 2003. V. 69. № 12. P. 7063–7072.
  85. Hockin S.L., Gadd G.M. // Environ. Microbiol. 2006. V. 8. № 5. P. 816–826.
  86. Michalke K., Wickenheiser E.B., Mehring M., Hirner A.V., Hensel R. // Appl. Environ. Microbiol. 2000. V. 66. № 7. P. 2791–2796.
  87. Lenz M., Van Hullebusch E.D., Hommes G., Corvini P.F., Lens P.N. // Water Res. 2008. V. 42. № 8-9. P. 2184–2194.
  88. Lovley D.R., Widman P.K., Woodward J.C., Phillips E.J.P. // Appl. Environ. Microbiol. 1993. V. 59. № 11. P. 3572–3576.
  89. Lloyd J.R., Nolting H.F., Solé V.A., Bosecker K. // Geomicrobiol. J. 1998. V. 15. № 1. P. 45–58.
  90. Lloyd J.R., Ridley J., Khizniak T., Lyalikova N.N., Macaskie L.E. // Appl. Environ. Microbiol. 1999. V. 65. № 6. P. 2691–2696.
  91. Lloyd J.R., Thomas G.H., Finlay J.A., Cole J.A., Macaskie L.E. // Biotechnol. Bioeng. 1999. V. 66. № 2. P. 122–130.
  92. De Luca G., de Philip P., Dermoun Z., Rousset M., Verméglio A. // Appl. Environ. Microbiol. 2001. V. 67. № 10. P. 4583–4587.
  93. Mohagheghi A., Updegraff D.M, Goldhaber M.B. // Geomicrobiol. J. 1985. V. 4. № 2. P. 153–173.
  94. Lovley D.R., Phillips E.J.P, Gorby Y.A., Landa E.R. // Nature. 1991. V. 350. P. 413–416.
  95. Tucker M.D., Barton L.L., Thomson B.M. // J. Ind. Microbiol. Biotechnol. 1998. V. 20. № 1. P. 13–19.
  96. Zhou C., Vannela R., Hyun S.P., Hayes K.F., E Rittmann B.E. // Environ. Sci. Technol. 2014. V. 48. № 12. P. 6928–6937.
  97. Elias D.A., Suflita J.M., McInerney M.J., Krumholz L.R. // Appl. Environ. Microbiol. 2004. V. 70. № 1. P. 413–420.
  98. Lovley D.R., Phillips E.J.P. // Environ. Sci. Technol. 1992. V. 26. № 11. P. 2228–2234.
  99. Tucker M.D., Barton L.L., Thomson B.M. // Appl. Microbiol. Biotechnol. 1996. V. 46. P. 74–77.
  100. Pietzsch K., Hard B.C., Babel W.A. // J. Basic Microbiol. 1999. V. 39. P. 365–372.
  101. Tebo B.M., Obraztsova A.Y. // FEMS Microbiol. Lett. 1998. V. 162. № 1. P. 193–198.
  102. Park H.S., Lin S., Voordouw G. // Antonie Van Leeuwenhoek. 2008. V. 93. № 1–2. P. 79–85.
  103. Junier P., Junier T., Podell S., Sims D.R., Detter J.C., Lykidis A., Han C.S., Wigginton N.S., Gaasterland T., Bernier-Latmani R. // Environ. Microbiol. 2010. V. 12. № 10. P. 2738–2754.
  104. Townsend L.T., Kuippers G., Lloyd J.R., Natrajan L.S., Boothman C., Mosselmans J.F.W., Shaw S., Morris K. // ACS Earth Space Chem. 2021. V. 5. № 11. P. 3075–3086.
  105. Payne R.B., Gentry D.M., Rapp-Giles B.J., Casalot L., Wall J.D. // Appl. Environ. Microbiol. 2002. V. 68. № 6. P. 3129–3132.
  106. Holmgren A. // Ann. Rev. Biochem. 1985. V. 54. P. 237–271.
  107. Pieulle L., Stocker P., Vinay M., Nouailler M., Vita N., Brasseur G., Garcin E., Sebban-Kreuzer C., Dolla A. // J. Biol. Chem. 2011. V. 286. № 10. P. 7812–7821.
  108. Garcin E.B., Bornet O., Elantak L., Vita N., Pieulle L., Guerlesquin F., Sebban–Kreuzer C. // J. Biol. Chem. 2012. V. 287. № 3. P. 1688–1697.

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