Skip to main content
Log in

Sulfate Reduction in Underground Horizons of a Flooded Coal Mine in Kuzbass

  • EXPERIMENTAL ARTICLES
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

Although dissimilatory sulfate reduction (DSR) is an important microbial process in subterranean aquifers, its geochemical consequences in this ecosystem remain insufficiently studied. The absence of data on the process rate under in situ conditions prevents quantitative estimation of the sulfur reservoir. This research is aimed at investigation of microbial sulfate reduction in subterranean aquifers associated with the Severnaya coal mine in Kuzbass. Water samples were collected from an artesian borehole broaching the underground horizons of the flooded mine. During over 10 years of sampling the water temperature fluctuated within a narrow range (10–13°C); the water was anoxic (–112 to –174 mV) and contained up to 6 mg/L sulfide. Analysis by high-throughput sequencing of the 16S rRNA genes showed that sulfur-oxidizing bacteria Sulfurovum, Sulfuricurvum, Sulfurospirillum, and Thiothrix predominated in the community. No phylotypes with known ability to carry out DSR were detected. Measurement of sulfate reduction rates with \({\text{Na}}_{{\text{2}}}^{{{\text{35}}}}{\text{S}}{{{\text{O}}}_{{\text{4}}}},\) showed the process to be relatively active, resulting in up to 178 g of reduced sulfur per year at the borehole discharge. Two organisms representing minor components of the community, a psychrophilic and acidophilic Desulfomicrobium sp. DI and a moderately thermophilic Desulfotomaculum LL1, were isolated in pure culture by varying the cultivation condition in a bioreactor. These members of the “rare biosphere” may be responsible for production of reduced sulfur species, which are used by a diverse and numerous sulfur-oxidizing community.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. Anantharaman, K., Brown, C.T., Hug, L.A., Sharon, I., Castelle, C.J., Probst, A.J., Thomas, B.C., Singh, A., Wilkins, M.J., Karaoz, U., Brodie, E.L., Williams, K.H., Hubbard, S.S., and Banfield, J.F., Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system, Nat. Commun., 2016, vol. 7, 13219.

    Article  CAS  Google Scholar 

  2. Bell E., Lamminmaki T., Alneberg J., Andersson A.F., Qian C., Xiong W., Hettich R.L., Balmer L., Frutschi M., Sommer G., Bernier-Latmani R. Biogeochemical cycling by a low-diversity microbial community in deep groundwater // Front. Microbiol. 2018. V. 9. Art. 2129. https://doi.org/10.3389/fmicb.2018.02129).

  3. Bowles, M.W., Mogollon, J.M., Kasten, S., Zabel, M., and Hinrichs, K.-U., Global rates of marine sulfate reduction and implications for sub-sea-floor metabolic activities, Science, 2014, vol. 344, pp. 889–891.

    Article  CAS  Google Scholar 

  4. Chivian, D., Brodie, E.L., Alm, E.J., Culley, D.E., Dehal, P.S., DeSantis, T.Z., Gihring, T.M., Lapidus, A., Lin, L.H., Lowry, S.R., Moser, D.P., Richardson, P.M., Southam, G., Wanger, G., Pratt L.M., et al., Environmental genomics revealed single-species ecosystem deep within Earth, Science, 2008, vol. 322, pp. 275–278.

    Article  CAS  Google Scholar 

  5. Chun, J., Oren, A., Ventosa, A., Christensen, H., Arahal, D.R., da Costa, M.S., Rooney, A.P., Yi, H., Xu, X.-W., De Meyer, S., and Trujillo, M.E., Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes, Int. J. Syst. Evol. Microbiol., 2018, vol. 68, pp. 461–466.

    Article  CAS  Google Scholar 

  6. Cline, J. D., Spectrophotometric determination of hydrogen sulfide in natural waters, Limnol. Oceanogr., 1969, vol. 14, pp. 454–458.

    Article  CAS  Google Scholar 

  7. Detmers, J., Schulte, U., Strauss, H., and Kuever, J., Sulfate reduction at a lignite seam: microbial abundance and activity, Microb. Ecol., 2001, vol. 42, pp. 238–247.

    Article  CAS  Google Scholar 

  8. Edgar, R.C., Search and clustering orders of magnitude faster than BLAST, Bioinformatics, 2010, vol. 26, pp. 2460–2461.

    Article  CAS  Google Scholar 

  9. Frank, Y., Banks, D., Avakian, M., Antsiferov, D., Kadychagov, P., and Karnachuk, O., Firmicutes is an important component of microbial communities in water-injected and pristine oil reservoirs, Western Siberia, Russia, Geomicrobiol. J., 2016, vol. 33, pp. 387–400.

    Article  Google Scholar 

  10. Glombitza, C., Mangelsdorf, K., and Horsfield, B., A novel procedure to detect low molecular weight compounds released by alkaline ester cleavage from low maturity coals to assess its feedstock potential for deep microbial life, Organic Geochemistry, 2009, vol. 40, pp, 175–183.

  11. Kaksonen, A.H., Dopson, M., Karnachuk, O., Tuovinen, O.H., and Puhakka, J.A., Biological iron oxidation and sulfate reduction in the treatment of acid mine drainage at low temperatures, in Psychrophiles: From Biodiversity to Biotechnology, Margesin, R., Schinner, F., Marx, J.C., and Gerday, C., Eds., Berlin, Heidelberg: Springer-Verlag, 2008, pp. 429–454.

    Google Scholar 

  12. Kadnikov, V.V., Mardanov, A.V., Beletsky, A.V., Ravin, N.V., Antsiferov, D.V., Kovalyova, A.A., and Karnachuk, O.V., Sulfur-oxidizing bacteria dominate in the water from a flooded coal mine shaft in Kuzbass, Microbiology (Moscow), 2019, vol. 88, pp. 120–123.

    Article  CAS  Google Scholar 

  13. Karnachuk, O.V., Kurganskaya, I.A., Avakyan, M.R., Frank, Y.A., Ikkert, O.P., Filenko, R.A., Danilova, E.V., and Pimenov, N.V., An acidophilic Desulfosporosinus isolated from the oxidized mining wastes in the Transbaikal area, Microbiology (Moscow), 2015, vol. 84, pp. 677–686.

    Article  CAS  Google Scholar 

  14. Karnachuk, O.V., Frank, Yu.A., Pimenov, N.V., Yusupov, S.K., Ivanov, M.V., and Puhakka, Ya.A., Distribution, diversity, and activity of sulfate-reducing bacteria in the water column in Gek-Gel Lake, Azerbaijan, Microbiology (Moscow), 2006, vol. 75, pp. 82–89.

    Article  CAS  Google Scholar 

  15. Karnachuk, O.V., Frank, Y.A., Lukina, A.P., Kadnikov, V.V., Beletsky, A.V., Mardanov, A.V., and Ravin, N.V., Domestication of previously uncultivated Candidatus Desulforudis audaxviator from a deep aquifer in Siberia sheds light on its physiology and evolution, ISME J., 2019, vol. 13, pp. 1947–1959.

    Article  CAS  Google Scholar 

  16. Magnabosco, C., Tekere, M., Lau, M.C.Y., Linage, B., Kuloyo, O., Erasmus, M., Cason, E., van Heerden, E., Borgonie, G., Kieft, T.L., Olivier, J., and Onstott, T.C., Comparisons of the composition and biogeographic distribution of the bacterial communities occupying South African thermal springs with those inhabiting deep subsurface fracture water, Front. Microbiol., 2014, vol. 5, art. 679. https://doi.org/10.3389/fmicb.2014.00679

    Article  Google Scholar 

  17. Magoč, T. and Salzberg, S.L., FLASH: fast length adjustment of short reads to improve genome assemblies, Bioinformatics, 2011, vol. 27(21), pp. 2957–2963.

    Article  Google Scholar 

  18. Mardanov, A.V., Panova, I.A., Beletsky, A.V., Avakyan, M.R., Kadnikov, V.V., Antsiferov, D.V., Banks, D., Frank, Y.A., Pimenov, N.V., Ravin, N.V., and Karnachuk, O.V., Genomic insights into a new acidophilic, copper-resistant Desulfosporosinus isolate from the oxidized tailings area of an abandoned gold mine, FEMS Microbiol. Ecol., 2016, vol. 92, p. fiw111.

    Article  Google Scholar 

  19. Momper, L., Jungbluth, S., Lee, M., and Amend, J.P., Energy and carbon metabolisms in a deep terrestrial subsurface fluid microbial community, ISME J., 2017, vol. 11, pp. 2319–2333.

    Article  CAS  Google Scholar 

  20. Moser, D.P., Gihring, T.M., Brockman, F.J., Fredrick-son, J.K., Balkwill, D.L., Dollhopf, M.E., Lollar, B.S. Pratt, L.M., Boice, E., Southam, G., Wanger, G., Baker, B.J., Pfiffner, S.M., Lin, L.-H., and Onstott, T.C., Desulfotomaculum and Methanobacterium spp. dominate a 4- to 5-kilometer-deep fault, Appl. Environ. Microbiol., 2005, vol. 71, pp. 8773–8783.

    Article  CAS  Google Scholar 

  21. Orcutt, B.N., LaRowe, D.E., Biddle, J.F., Colwell, F.S., Glazer, B.T., Reese, B.K., Kirkpatrich, J.B., Lapham, L.L., Mills, H.J., Sylvan, J.B., Wankel, S.D., and Wheat, C.G., Microbial activity in the marine deep biosphere: progress and prospects, Front. Microbiol., 2013, vol. 4, 189. https://doi.org/10.3389/fmicb.2013.00189

  22. O’Sullivan, L.A., Roussel, E.G., Weightman, A.J., Webster, G., Hubert, C.R.J., Bell, E, Head, I., Sass, H., and Parkes, R. J., Survival of Desulfotomaculum spores from estuarine sediments after serial autoclaving and high-temperature exposure, ISME J., 2015, vol. 9, pp. 922–933.

    Article  Google Scholar 

  23. Pruesse, E., Peplies, J., and Glöckner, F.O., SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes, Bioinformatics, 2012, vol. 28, pp. 1823–1829.

    Article  CAS  Google Scholar 

  24. Yang, G., Guo, J., Zhuang, L., Yuan, Y., and Zhou, S., Desulfotomaculum ferrireducens sp. nov., a moderately thermophilic sulfate-reducing and dissimilatory Fe(III)-reducing bacterium isolated from compost, Int. J. Syst. Evol. Microbiol., 2016, vol. 66, pp. 3022−3028.

    Article  CAS  Google Scholar 

  25. Wang, Y., Liu, Q., Yan, L., Gao, Y., Wang, Y., and Wang, W., A novel lignin degradation bacterial consortium for efficient pulping, Bioresour. Technol., 2013, vol. 139, pp. 113–119.

    Article  CAS  Google Scholar 

  26. Widdel, F.F. and Bak, R., Gram negative mesophilic sulfate reducing bacteria, in The Prokaryotes: A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications, Balows, A., Trüper, H.G., Dworkin, M., Harder, W., and Schleifer, K.-H., Eds., Berlin: Springer, 1992, pp. 3352–3378.

    Google Scholar 

Download references

ACKNOWLEDGMENTS

The authors are grateful to D. Banks for the help provided in collecting water samples and evaluation of physicochemical parameters in 2006 and to V. Maibakh for the logistic support.

Funding

This work was supported by the Russian Foundation for Basic Research project no. 19-04-00981 (O.V.K.); isolation and investigation of Desulfomicrobium sp. DI was supported by the Russian Foundation for Basic Research project no. 18-34-00472 (A.A.K.); radiolabeling experiments were supported by the Ministry of Science and Higher Education of the Russian Federation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. V. Karnachuk.

Ethics declarations

Conflict of interests. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by D. Timchenko

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Panova, I.A., Rusanov, I.I., Kadnikov, V.V. et al. Sulfate Reduction in Underground Horizons of a Flooded Coal Mine in Kuzbass. Microbiology 89, 542–550 (2020). https://doi.org/10.1134/S0026261720050185

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261720050185

Keywords:

Navigation