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Antonie van Leeuwenhoek

, Volume 110, Issue 12, pp 1669–1679 | Cite as

Selection for novel, acid-tolerant Desulfovibrio spp. from a closed Transbaikal mine site in a temporal pH-gradient bioreactor

  • Dmitry V. Antsiferov
  • Tatiana S. Fyodorova
  • Anastasia A. Kovalyova
  • Anastasia Lukina
  • Yulia A. Frank
  • Marat R. Avakyan
  • David Banks
  • Olli H. Tuovinen
  • Olga V. Karnachuk
Original Paper

Abstract

Almost all the known isolates of acidophilic or acid-tolerant sulphate-reducing bacteria (SRB) belong to the spore-forming genus Desulfosporosinus in the Firmicutes. The objective of this study was to isolate acidophilic/acid-tolerant members of the genus Desulfovibrio belonging to deltaproteobacterial SRB. The sample material originated from microbial mat biomass submerged in mine water and was enriched for sulphate reducers by cultivation in anaerobic medium with lactate as an electron donor. A stirred tank bioreactor with the same medium composition was inoculated with the sulphidogenic enrichment. The bioreactor was operated with a temporal pH gradient, changing daily, from an initial pH of 7.3 to a final pH of 3.7. Among the bacteria in the bioreactor culture, Desulfovibrio was the only SRB group retrieved from the bioreactor consortium as observed by 16S rRNA-targeted denaturing gradient gel electrophoresis. Moderately acidophilic/acid-tolerant isolates belonged to Desulfovibrio aerotolerans-Desulfovibrio carbinophilus-Desulfovibrio magneticus and Desulfovibrio idahonensis-Desulfovibrio mexicanus clades within the genus Desulfovibrio. A moderately acidophilic strain, Desulfovibrio sp. VK (pH optimum 5.7) and acid-tolerant Desulfovibrio sp. ED (pH optimum 6.6) dominated in the bioreactor consortium at different time points and were isolated in pure culture.

Keywords

Acid tolerant Deltaproteobacteria Desulfovibrio Mine waste Sulphate-reducing bacteria 

Notes

Acknowlegements

We are grateful to Dr. Michael Watts and his staff at the British Geological Survey for providing data on elemental and ion analysis. We thank Anna L. Gerasimchuk and Alexander Igoshin for their technical assistance with DGGE. This work was supported by the Russian Federation Agency of Science and Innovations (FCP Program, Contract No. 14.575.21.0067, Project No. FMEFI57514X0067), and the Russian Fund for Fundamental Research, Project No. 16-44-700315.

Conflict of interest

The authors declare that they have no conflict of interests.

References

  1. Abicht HK, Mancini S, Karnachuk OV, Solioz M (2011) Genome sequence of Desulfosporosinus sp. OT, an acidophilic sulfate reducing bacterium from copper mining waste in Norilsk, Northern Siberia. J Bacteriol 193:6104–6105CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alazard D, Joseph M, Battaglia-Brunet F, Cayol J-L, Ollivier B (2010) Desulfosporosinus acidiphilus sp. nov.: a moderately acidophilic sulfate-reducing bacterium isolated from acid mining drainage sediments. Extremophiles 14:305–312CrossRefPubMedGoogle Scholar
  3. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DL (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402CrossRefPubMedPubMedCentralGoogle Scholar
  4. Banks D, Parnachev VP, Frengstad B, Holden W, Vedernikov AA, Karnachuk OV (2002) Alkaline mine drainage from metal sulphide and coal mines: examples from Svalbard and Siberia. Geol Soc London Spec Publ 198:287–296CrossRefGoogle Scholar
  5. Bijmans MFM, Dopson M, Peeters TWT, Lens PNL, Buisman CJN (2009) Sulfate reduction at pH 5 in a high-rate membrane bioreactor: reactor performance and microbial community analyses. J Microbiol Biotechnol 19:698–708PubMedGoogle Scholar
  6. Bijmans MFM, de Vries E, Yang C-H, Buisman CJN, Lens PNL, Dopson M (2010) Sulfate reduction at pH 4.0 for treatment of process and wastewaters. Biotechnol Progr 26:1029–1037Google Scholar
  7. Cardenas E, Wu W-M, Leigh MB, Carley J, Carroll S, Gentry T, Luo J, Watson D, Gu B, Ginder-Vogel M, Kitanidis PK, Jardine PM, Zhou J, Criddle CS, Marsh TL, Tiedje JM (2010) Significant association between sulfate-reducing and uranium-reducing microbial communities as revealed by a combined massively parallel sequencing-indicator species approach. Appl Environ Microbiol 76:6778–6786CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cline JD (1969) Spectrophotometric determination of hydrogen sulphide in natural waters. Limnol Oceanogr 14:454–458CrossRefGoogle Scholar
  9. Cole M, Wrubel J, Henegan P, Janzen C, Holt J, Tobin T (2011) Development of a small-scale bioreactor method to monitor the molecular diversity and environmental impacts of bacterial biofilm communities from an acid mine drainage impacted creek. J Microbiol Meth 87:96–104CrossRefGoogle Scholar
  10. Cypionka H (2000) Oxygen respiration by Desulfovibrio species. Annu Rev Microbiol 54:827–848CrossRefPubMedGoogle Scholar
  11. DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5685–5689CrossRefPubMedPubMedCentralGoogle Scholar
  12. Falagán C, Sánchez-España J, Johnson DB (2014) New insights into the biogeochemistry of extremely acidic environments revealed by a combined cultivation-based and culture-independent study of two stratified pit lakes. FEMS Microbiol Ecol 87:231–243CrossRefPubMedGoogle Scholar
  13. Frank Y, Banks D, Avakian M, Antsiferov D, Kadychakov P, Karnachuk O (2016) Firmicutes is an important component of microbial communities in water-injected and pristine oil reservoirs, Western Siberia, Russia. Geomicrobiol J 33:387–400CrossRefGoogle Scholar
  14. Frolov EN, Kublanov IV, Toshchakov SV, Samarov NI, Novikov AA, Lebedinsky AV, Bonch-Osmolovskaya EA, Chernyh NA (2017) Thermodesulfobium acidiphilum sp. nov., a thermoacidophilic, sulfate-reducing, chemoautotrophic bacterium from a thermal site. Int J System Evol Microbiol 67:1482–1485CrossRefGoogle Scholar
  15. Gyure R, Konopka A, Brooks A, Doemel W (1990) Microbial sulfate reduction in acidic (pH 3) strip-mine lakes. FEMS Microbiol Ecol 6:193–201CrossRefGoogle Scholar
  16. Han Z, Zhao Y, Yan H, Zhao H, Han M, Sun B, Sun X, Hou F, Sun H, Han L, Sun Y, Wang J, Li H, Wang Y, Du H (2015) Struvite precipitation induced by a novel sulfate-reducing bacterium Acinetobacter calcoaceticus SRB4 isolated from river sediment. Geomicrobiol J 32:868–877CrossRefGoogle Scholar
  17. Ikkert OP, Gerasimchuk AL, Bukhtiyarova PA, Tuovinen OH, Karnachuk OV (2013) Characterization of precipitates formed by H(2)S-producing, Cu-resistant Firmicute isolates of Tissierella from human gut and Desulfosporosinus from mine waste. Antonie Van Leeuwenhoek 103:1221–1234Google Scholar
  18. Jameson E, Rowe OF, Hallberg KB, Johnson DB (2010) Sulfidogenesis and selective precipitation of metals at low pH mediated by Acidithiobacillus spp. and acidophilic sulfate-reducing bacteria. Hydrometallurgy 104:488–493CrossRefGoogle Scholar
  19. Kadnikov VV, Ivasenko DA, Beletskii AV, Mardanov AV, Danilova EV, Pimenov NV, Karnachuk OV, Ravin NV (2016) A novel uncultured bacterium of the family Gallionellaceae: description and genome reconstruction based on metagenomic analysis of microbial community in acid mine drainage. Mikrobiologiya 85:449–461Google Scholar
  20. Kaksonen AH, Plumb JJ, Franzmann PD, Puhakka JA (2004) Simple organic electron donors support diverse sulfate-reducing communities in fluidized-bed reactors treating acidic metal- and sulfate-containing wastewater. FEMS Microbiol Ecol 47:279–289CrossRefPubMedGoogle Scholar
  21. Kaksonen AH, Dopson M, Karnachuk OV, Tuovinen OH, Puhakka JA (2008) Biological iron oxidation and sulfate reduction in the treatment of acid mine drainage at low temperatures. In: Margesin R, Schinner F, Marx J-C, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 429–454CrossRefGoogle Scholar
  22. Karnachuk OV, Pimenov NV, Yusupov SK, Frank YA, Puhakka JA, Ivanov MV (2006) Distribution, diversity, and activity of sulfate-reducing bacteria in the water column in Gek-Gel lake, Azerbaijan. Mikrobiologiya 75:101–109Google Scholar
  23. Karnachuk OV, Sasaki K, Gerasimchuk AL, Sukhanova O, Ivasenko DA, Kaksonen AH, Puhakka JA, Tuovinen OH (2008) Precipitation of Cu-sulfides by copper-tolerant Desulfovibrio isolates. Geomicrobiol J 25:219–227CrossRefGoogle Scholar
  24. Karnachuk OV, Gerasimchuk AL, Banks D, Frengstad B, Stykon GA, Tikhonova ZL, Kaksonen A, Puhakka J, Yanenko AS, Pimenov NV (2009) Bacteria of the sulfur cycle in the sediments of gold mine tailings, Kuznetsk Basin, Russia. Mikrobiologiya 78:483–491Google Scholar
  25. Karnachuk OV, Kurganskaya IA, Avakyan MR, Frank YA, Ikkert OP, Filenko RA, Danilova EV, Pimenov NV (2015a) An acidophilic Desulfosporosinus isolated from the oxidized mining wastes in the Transbaikal area. Mikrobiologiya 84:595–605Google Scholar
  26. Karnachuk OV, Mardanov AV, Avakyan MR, Kadnikov VV, Vlasova M, Beletsky AV, Gerasimchuk AL, Ravin NV (2015b) Draft genome sequence of the first acid-tolerant sulfate-reducing deltaproteobacterium Desulfovibrio sp. TomC having potential for mine water treatment. FEMS Microbiol Lett 362(4):fnv007CrossRefGoogle Scholar
  27. Karnachuk OV, Kadnikov VV, Panova IA, Mardanov AV, Beletsky AV, Danilova EV, Avakyan MR, Ravin NV (2017) Genome sequence of the copper resistant and acid-tolerant Desulfosporosinus sp. BG isolated from the tailings of a molybdenum-tungsten mine in the Transbaikal area. Genomics Data 11:106–108CrossRefPubMedGoogle Scholar
  28. Koschorreck M (2008) Microbial sulphate reduction at a low pH. FEMS Microbiol Ecol 64:329–342CrossRefPubMedGoogle Scholar
  29. Koschorreck M, Geller W, Neu T, Kleinsteuber S, Kunze T, Trosiener A, Wendt-Potthoff K (2010) Structure and function of the microbial community in an in situ reactor to treat an acidic mine pit lake. FEMS Microbiol Ecol 73:385–395PubMedGoogle Scholar
  30. Küsel K, Roth U, Trinkwalter T, Peiffer S (2001) Effect of pH on the anaerobic microbial cycling of sulfur in mining-impacted freshwater lake sediment. Environ Experim Bot 46:213–223CrossRefGoogle Scholar
  31. Lane DJ (1991) 16S/23S rRNA Sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
  32. Lefticariu L, Walters ER, Pugh CW, Bender KS (2015) Sulfate reducing bioreactor dependence on organic substrates for remediation of coal-generated acid mine drainage: field experiments. Appl Geochem 63:70–82CrossRefGoogle Scholar
  33. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar Buchner A, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüßmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer K-H (2004) ARB: a software environment for sequence data. Nucl Acids Res 32:1363–1371CrossRefPubMedPubMedCentralGoogle Scholar
  34. Mardanov AV, Panova IA, Beletsky AV, Avakyan MR, Kadnikov VV, Antsiferov DV, Banks D, Frank YA, Pimenov NV, Ravin NV, Karnachuk OV (2016) Genomic insight into a new acidophilic, copper-resistant Desulfosporosinus isolate from the oxidised tailings area of an abandoned gold mine. FEMS Microbiol Ecol 92(8):fiw111CrossRefPubMedGoogle Scholar
  35. Meier J, Piva A, Fortin D (2012) Enrichment of sulfate-reducing bacteria and resulting mineral formation in media mimicking pore water metal ion concentrations and pH conditions of acidic pit lakes. FEMS Microbiol Ecol 79:69–84CrossRefPubMedGoogle Scholar
  36. Mori K, Kim H, Kakegawa T, Hanada S (2003) A novel lineage of sulfate-reducing microorganisms: thermodesulfobiaceae fam. nov., Thermodesulfobium narugense, gen. nov., sp. nov., a new thermophilic isolate from a hot spring. Extremophiles 7:283–290CrossRefPubMedGoogle Scholar
  37. Muyzer G, Hottenträger S, Teske A, Wawer C (1996) Denaturing gradient gel electrophoresis of PCR-amplified 16S rDNA—a new molecular approach to analyse the genetic diversity of mixed microbial communities. In: Akkermans ADL, Van Elsas JD, De Bruijn JD (eds) Molecular microbial ecology manual. Kluwer, Dordrecht, pp 1–23Google Scholar
  38. Pruden A, Messner N, Pereyra L, Hiibel SR, Reardon KF (2007) The effect of inoculum on the performance of sulfate-reducing columns treating heavy metal contaminated water. Water Res 41:904–914CrossRefPubMedGoogle Scholar
  39. Ramel F, Brasseur G, Pieulle L, Valette O, Hirschler-Réa A, Fardeau ML, Dolla A (2015) Growth of the obligate anaerobe Desulfovibrio vulgaris Hildenborough under continuous low oxygen concentration sparging: impact of the membrane-bound oxygen reductases. PLoS ONE 10:e0123455CrossRefPubMedPubMedCentralGoogle Scholar
  40. Rampinelli LR, Azevedo RD, Teixeira MC, Guerra-Sá R, Leão VA (2008) A sulfate-reducing bacterium with unusual growing capacity in moderately acidic conditions. Biodegradation 19:613–619CrossRefPubMedGoogle Scholar
  41. Sánchez-Andrea I, Sanz JL, Bijmans MFM, Stams AJM (2014) Sulfate reduction at low pH to remediate acid mine drainage. J Hazard Mater 269:98–109CrossRefPubMedGoogle Scholar
  42. Sánchez-Andrea I, Stams AJM, Hedrich S, Ňancucheo I, Johnson DB (2015) Desulfosporosinus acididurans sp. nov.: an acidophilic sulfate-reducing bacterium isolated from acidic sediments. Extremophiles 19:39–47CrossRefPubMedGoogle Scholar
  43. Senko JM, Zhang G, McDonough JT, Bruns MA, Burgos WD (2009) Metal reduction at low pH by a Desulfosporosinus species: implications for the biological treatment of acidic mine drainage. Geomicrobiol J 26:71–82CrossRefGoogle Scholar
  44. Stackebrandt E, Schumann P, Schüler E, Hippe H (2003) Reclassification of Desulfotomaculum auripigmentum as Desulfosporosinus auripigmenti corrig., comb. nov. Int J System Evolut Microbiol 53:1439–1443CrossRefGoogle Scholar
  45. Tuttle JH, Dugan PR, MacMillan CB, Randles CI (1969a) Microbial dissimilatory sulfur cycle in acid mine water. J Bacteriol 97:594–602PubMedPubMedCentralGoogle Scholar
  46. Tuttle JH, Dugan PR, Randles CI (1969b) Microbial sulfate reduction and its potential utility as an acid mine water pollution abatement procedure. Appl Microbiol 17:297–302PubMedPubMedCentralGoogle Scholar
  47. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703CrossRefPubMedPubMedCentralGoogle Scholar
  48. Widdel FF, Bak R (1992) Gram negative mesophilic sulfate reducing bacteria. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds) The prokaryotes: a handbook on the biology of bacteria: ecophysiology, isolation, identification, applications, 2nd edn. Springer, Berlin, pp 3352–3378Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Dmitry V. Antsiferov
    • 1
  • Tatiana S. Fyodorova
    • 1
  • Anastasia A. Kovalyova
    • 1
  • Anastasia Lukina
    • 1
  • Yulia A. Frank
    • 1
  • Marat R. Avakyan
    • 1
  • David Banks
    • 2
    • 3
  • Olli H. Tuovinen
    • 1
    • 4
  • Olga V. Karnachuk
    • 1
  1. 1.Laboratory of Biochemistry and Molecular BiologyTomsk State UniversityTomskRussia
  2. 2.School of Engineering, Systems Power and EnergyGlasgow UniversityGlasgowScotland, UK
  3. 3.Holymoor Consultancy LtdChesterfieldUK
  4. 4.Department of MicrobiologyOhio State UniversityColumbusUSA

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