, Volume 23, Issue 3, pp 283–304 | Cite as

Change in the microbial community of saline geothermal fluids amended with a scaling inhibitor: effects of heat extraction and nitrate dosage

  • Anke Westphal
  • Florian Eichinger
  • Lorenz Eichinger
  • Hilke WürdemannEmail author
Original Paper


Geothermal plants are often affected by corrosion caused by microbial metabolites such as H2S. In the Bad Blumau (Austria) geothermal system, an increase in microbially produced H2S was observed in the hot (107 °C) and scaling inhibitor-amended saline fluids and in fluids that had cooled down (45 °C). Genetic fingerprinting and quantification revealed the dominance, increasing abundance and diversity of sulfate reducers such as Desulfotomaculum spp. that accompanied the cooling and processing of the geothermal fluids. In addition, a δ34S isotopic signature showed the microbial origin of the H2S that has been produced either chemolithotrophically or chemoorganotrophically. A nitrate addition test in a test pipe as a countermeasure against the microbial H2S formation caused a shift from a biocenosis dominated by bacteria of the phylum Firmicutes to a community of Firmicutes and Proteobacteria. Nitrate supported the growth of nitrate-reducing sulfur-oxidizing Thiobacillus thioparus, which incompletely reduced nitrate to nitrite. The addition of nitrate led to a change in the composition of the sulfate-reducing community. As a result, representatives of nitrate- and nitrite-reducing SRB, such as Desulfovibrio and Desulfonatronum, emerged as additional community members. The interaction of sulfate-reducing bacteria and nitrate-reducing sulfur-oxidizing bacteria (NR-SOB) led to the removal of H2S, but increased the corrosion rate in the test pipe.


Geothermal plant Aquifer Hyperthermophilic sulfate reduction NR-SOB SRB Nitrate corrosion control 



The authors would like to thank the Rogner Geothermie GmbH, Bad Blumau, Austria for allowing access to the topside facility of the multifunctional used geothermal system and its technical team for the appreciated help during multiple sampling campaigns. Furthermore, we thank Sebastian Teitz for support during sampling, Jennifer Weigt for the useful help in the laboratory and Dr. Tobias Lienen for discussing the results. In addition, the authors wish to thank the German “Federal Ministry for Economic Affairs and Energy” for funding the project “ThermoInhibitor” (BMWi 0325424B).


  1. Akunna JC, Bizeau C, Moletta R (1994) Nitrate reduction by anaerobic sludge using glucose at various nitrate concentrations: ammonification, denitrification and methanogenic activities. Environ Technol 15:41–49Google Scholar
  2. Akunna JC, Bernet N, Moletta R (1998) Effect of nitrate on methanogenesis at low redox potential. Environ Technol 19:1249–1254Google Scholar
  3. Alawi M, Lerm S, Vetter A, Wolfgramm M, Seibt A, Würdemann H (2011) Diversity of sulfate-reducing bacteria in a plant using deep geothermal energy. Grundwasser 16:105–112. Google Scholar
  4. Altschul S, Gish W, Miller W (1990) Basic local alignment search tool. J Mol Biol 215:403–410Google Scholar
  5. Alt-Epping P, Waber HN, Diamond LW, Eichinger L (2013) Reactive transport modeling of the geothermal system at Bad Blumau, Austria: implications of the combined extraction of heat and CO2. Geothermics 45:18–30. Google Scholar
  6. Altschul SF, Madden TL, Schäffer A, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402Google Scholar
  7. Amann RI, Stromley J, Devereux R, Key R, Stahl DA (1992) Molecular and microscopic identification of sulfate-reducing bacteria in multispecies biofilms. Appl Environ Microbiol 58:614–623Google Scholar
  8. An BA, Shen Y, Voordouw G (2017) Control of sulfide production in high salinity bakken shale oil reservoirs by halophilic bacteria reducing nitrate to nitrite. Front Microbiol. Google Scholar
  9. Baena S, Fardeau ML, Labat M, Ollivier B, Garcia JL, Patel BK (1998) Desulfovibrio aminophilus sp. nov., a novel amino acid degrading and sulfate reducing bacterium from an anaerobic dairy wastewater lagoon. Syst Appl Microbiol 21:498–504. Google Scholar
  10. Balkwill D, Kieft T, Tsukuda T, Kostandarithes H, Onstott T, Macnaughton S, Bownas J, Fredrickson J (2004) Identification of iron-reducing Thermus strains as Thermus scotoductus. Extremophiles 8:37–44. Google Scholar
  11. Banihani Q, Sierra-Alvarez R, Field JA (2009) Nitrate and nitrite inhibition of methanogenesis during denitrification in granular biofilms and digested domestic sludges. Biodegradation 20:801–812. Google Scholar
  12. Barns SM, Fundyga RE, Jeffries MW, Pace NR (1994) Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc Natl Acad Sci USA 91:1609–1613. Google Scholar
  13. Barton LL, LeGall J, Odom JM, Peck HDJ (1983) Energy coupling to nitrite respiration in the sulfate-reducing bacterium Desulfovibrio gigas. J Bacteriol 153:867–871Google Scholar
  14. Bødtker G, Thorstenson T, Lillebø B-LP, Thorbjørnsen BE, Ulvøen RH, Sunde E, Torsvik T (2008) The effect of long-term nitrate treatment on SRB activity, corrosion rate and bacterial community composition in offshore water injection systems. J Ind Microbiol Biotechnol 35:1625–1636. Google Scholar
  15. Bauer S, Beyer C, Dethlefsen F, Dietrich P, Duttmann R, Ebert M, Feeser V, Görke U, Köber R, Kolditz O, Rabbel W, Schanz T, Schäfer D, Würdemann H, Dahmke A (2013) Impacts of the use of the geological subsurface for energy storage: an investigation concept. Environ Earth Sci 70:3935–3943.
  16. Cheng L, Dai L, Li X, Zhang H, Lu Y (2011) Isolation and characterization of Methanothermobacter crinale sp. nov., a novel hydrogenotrophic methanogen from the Shengli oil field. Appl Environ Microbiol 77:5212–5219. Google Scholar
  17. Cord-Ruwisch R, Kleinitz W, Widdel F (1987) Sulfate-reducing bacteria and their activities in oil production. J Pet Technol 160:97–106Google Scholar
  18. Corsi R (1986) Scaling and corrosion in geothermal equipment: problems and preventive measures. Geothermics 15:839–856Google Scholar
  19. Dalsgaard T, Bak F (1994) Nitrate reduction in a sulfate-reducing bacterium, Desulfovibrio desulfuricans, isolated from rice paddy soil: sulfide inhibition, kinetics, and regulation. Appl Environ Microbiol 60:291–298Google Scholar
  20. Daumas S, Cord-Ruwisch R, Garcia JL (1988) Desulfotomaculum geothermicum sp. nov., a thermophilic, fatty acid-degrading, sulfate-reducing bacterium isolated with H2 from geothermal ground water. Antonie Van Leeuwenhoek 54:165–178Google Scholar
  21. DIN EN 1484-H3 (1997) 08 Water analysis—guidelines for the determination of total organic carbon (TOC) and dissolved organic carbon (DOC)Google Scholar
  22. DIN 38404-6 (1984) 05 German standard methods for the examination of water, waste water and sludge; physical and physico-chemical parameters (group C); determination of the oxidation reduction (redox) potential (C 6)Google Scholar
  23. DIN EN ISO 10304-1 (2009) 07 Water quality —Determination of dissolved anions by liquid chromatography of ions - Part 1: Determination of bromide, chloride, fluoride, nitrate, nitrite, phosphate and sulfate (ISO 10304-1:2007)Google Scholar
  24. DIN EN ISO 10523 (2012) 04 Water quality—Determination of pH (ISO 10523:2008)Google Scholar
  25. Dunsmore B, Whitfield T, Lawson P, Collins M (2004) Corrosion by sulfate-reducing bacteria that utilize nitrate. Corrosion 60:1–15Google Scholar
  26. Eckford RE, Fedorak PM (2002) Chemical and microbiological changes in laboratory incubations of nitrate amendment “sour” produced waters from three western Canadian oil fields. J Ind Microbiol Biotechnol 29:243–254. Google Scholar
  27. Eichinger L, Eichinger F, Schneider J (2011) Angewandte Konzepte zur Sicherstellung der nachhaltigen Nutzung der Geothermieanlage Bad Blumau. Schlussbericht zum Förderprogramm „Einfalls!Reich“Projektnummer: 1000027135Google Scholar
  28. Esnault G, Caumette P, Garcia JL (1988) Characterization of Desulfovibrio giganteus sp. nov., a sulfate-reducing bacterium isolated from a brackish coastal lagoon. Syst Appl Microbiol 10:147–151Google Scholar
  29. Fida TT, Chen C, Okpala G, Voordouw G (2016) Implications of limited thermophilicity of nitrite reduction for control of sulfide production in oil reservoirs. Appl Environ Microbiol 82:4190–4199. Google Scholar
  30. Flynn TM, Sanford RA, Ryu H, Bethke CM, Levine AD, Ashbolt NJ, Santo Domingo JW (2013) Functional microbial diversity explains groundwater chemistry in a pristine aquifer. BMC Microbiol 13:146. Google Scholar
  31. Foss S, Harder J (1998) Thauera linaloolentis sp. nov. and Thauera terpenica sp. nov., isolated on oxygen-containing monoterpenes (linalool, menthol, and eucalyptol) and nitrate. Syst Appl Microbiol 21:365–373. Google Scholar
  32. Friedrich AB, Antranikian G (1996) Keratin degradation by Fervidobacterium pennavorans, a novel thermophilic anaerobic species of the order Thermotogales. Appl Environ Microbiol 62:2875–2882Google Scholar
  33. Gafan GP, Lucas VS, Roberts GJ, Wilson M, Spratt DA, Petrie A (2005) Statistical analyses of complex denaturing gradient gel electrophoresis profiles. J Clin Microbiol 43:3971–3978. Google Scholar
  34. Gantner S, Andersson AF, Alonso-Sáez L, Bertilsson S (2011) Novel primers for 16S rRNA-based archaeal community analyses in environmental samples. J Microbiol Methods 84:12–18. Google Scholar
  35. Gaylarde CC, Beech IB (1988) Molecular basis of bacterial adhesion to metal. In: Sequeira C, Tiller A (eds) Microb. Corros. Elsevier Applied Science, London, pp 20–28Google Scholar
  36. Geets J, Borremans B, Diels L, Springael D, Vangronsveld J, van der Lelie D, Vanbroekhoven K (2006) DsrB gene-based DGGE for community and diversity surveys of sulfate-reducing bacteria. J Microbiol Methods 66:194–205. Google Scholar
  37. Goldbrunner JE (1999) Hydrogeology of deep groundwaters in Austria. Mitteilungen Österreichische Geol Gesellschaft 92:281–294Google Scholar
  38. Goldbrunner J (2005) State, possible future developments in and barriers to the exploration and exploitation of geothermal energy in Austria. In: Proc. World Geotherm. Congr. 2005, Antalya, Turkey, 24–29 April 2005. pp 24–29Google Scholar
  39. Gounder K, Brzuszkiewicz E, Liesegang H, Wollherr A, Daniel R, Gottschalk G, Reva O, Kumwenda B, Srivastava M, Bricio C, Berenguer J, van Heerden E, Litthauer D (2011) Sequence of the hyperplastic genome of the naturally competent Thermus scotoductus SA-01. BMC Genom 12:577. Google Scholar
  40. Greene EA, Hubert C, Nemati M, Jenneman GE, Voordouw G (2003) Nitrite reductase activity of sulphate-reducing bacteria prevents their inhibition by nitrate-reducing, sulphide-oxidizing bacteria. Environ Microbiol 5:607–617Google Scholar
  41. Henry EA, Devereux R, Maki JS, Gilmour CC, Woese CR, Mandelco L, Schauder R, Remsen CC, Mitchell R (1994) Characterization of a new thermophilic sulfate-reducing bacterium Thermodesulfovibrio yellowstonii, gen. nov. and sp. nov.: its phylogenetic relationship to Thermodesulfobacterium commune and their origins deep within the bacterial domain. Arch Microbiol 161:62–69Google Scholar
  42. Hetzer A, Morgan HW, McDonald IR, Daughney CJ (2007) Microbial life in Champagne Pool, a geothermal spring in Waiotapu, New Zealand. Extremophiles 11:605–614. Google Scholar
  43. Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST (1994) Bergey’s manual of determinative bacteriology. Williams and Wilkins, BaltimoreGoogle Scholar
  44. Huber R, Langworthy TA, Knig H, Thomm M, Woese CR, Sleytr UB, Stetter KO (1986) Thermotoga maritima sp. nov. represents a new genus of unique extremely thermophilic eubacteria growing up to 90°C. Arch Microbiol 144:324–333Google Scholar
  45. Hubert C, Voordouw G (2007) Oil field souring control by nitrate-reducing Sulfurospirillum spp. that outcompete sulfate-reducing bacteria for organic electron donors. Appl Environ Microbiol 73:2644–2652. Google Scholar
  46. Hubert C, Nemati M, Jenneman G, Voordouw G (2003) Containment of biogenic sulfide production in continuous up-flow packed-bed bioreactors with nitrate or nitrite. Biotechnol Prog 19:338–345. Google Scholar
  47. Hubert C, Nemati M, Jenneman G, Voordouw G (2005) Corrosion risk associated with microbial souring control using nitrate or nitrite. Appl Microbiol Biotechnol 68:272–282. Google Scholar
  48. Iino T, Mori K, Uchino Y, Nakagawa T, Harayama S, Suzuki K-I (2010) Ignavibacterium album gen. nov., sp. nov., a moderately thermophilic anaerobic bacterium isolated from microbial mats at a terrestrial hot spring and proposal of Ignavibacteria classis nov., for a novel lineage at the periphery of green sulfur bacteria. Int J Syst Evol Microbiol 60:1376–1382. Google Scholar
  49. Jenneman GE, Mcinerney MJ, Knapp RM (1986) Effect of nitrate on biogenic sulfide production. Appl Environ Microbiol 51:1205–1211Google Scholar
  50. Jørgensen BB, Isaksen MF, Jannasch HW (1992) Bacterial sulfate reduction above 100 °C in deep-sea hydrothermal vent sediments. Science 258:1756–1757. Google Scholar
  51. Kaksonen AH, Spring S, Schumann P, Kroppenstedt RM, Puhakka JA (2007) Desulfovirgula thermocuniculi gen. nov., sp. nov., a thermophilic sulfate-reducer isolated from a geothermal underground mine in Japan. Int J Syst Evol Microbiol 57:98–102. Google Scholar
  52. Katayama T, Yoshioka H, Mochimaru H, Meng XY, Muramoto Y, Usami J, Ikeda H, Kamagata Y, Sakata S (2014) Methanohalophilus levihalophilus sp. nov., a slightly halophilic, methylotrophic methanogen isolated from natural gas-bearing deep aquifers, and emended description of the genus Methanohalophilus. Int J Syst Evol Microbiol 64:2089–2093. Google Scholar
  53. Kielemoes J, De Boever P, Verstraete W (2000) Influence of denitrification on the corrosion of iron and stainless steel powder. Environ Sci Technol 34:663. Google Scholar
  54. Klüber HD, Conrad R (1998) Inhibitory effects of nitrate, nitrite, NO and N2O on methanogenesis by Methanosarcina barkeri and Methanobacterium bryantii. FEMS Microbiol Ecol 25:331–339Google Scholar
  55. Knittel K, Boetius A (2009) Anaerobic methane oxidation: progress with unknown process. Annu Rev Microbiol 63:311–334Google Scholar
  56. Lambie SC, Kelly WJ, Leahy SC, Li D, Reilly K, McAllister TA, Valle ER, Attwood GT, Altermann E (2015) The complete genome sequence of the rumen methanogen Methanosarcina barkeri CM1. Stand Genom Sci 10:57. Google Scholar
  57. Lambo AJ, Noke K, Larter SR, Voordouw G (2008) Competitive, microbially-mediated reduction of nitrate with sulfide and aromatic oil components in a low-temperature, western Canadian oil reservoir. Environ Sci Technol 42:8941–8946. Google Scholar
  58. Lane D (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic Acid Tech. Bact. Syst. Wiley, New York, pp 115–175Google Scholar
  59. Lerm S, Westphal A, Miethling-Graff R, Alawi M, Seibt A, Wolfgramm M, Würdemann H (2013) Thermal effects on microbial composition and microbiologically induced corrosion and mineral precipitation affecting operation of a geothermal plant in a deep saline aquifer. Extremophiles 17:311–327. Google Scholar
  60. Liu Z, Frigaard N-U, Vogl K, Iino T, Ohkuma M, Overmann J, Bryant DA (2012) Complete genome of Ignavibacterium album, a metabolically versatile, flagellated, facultative anaerobe from the phylum Chlorobi. Front Microbiol 3:185. Google Scholar
  61. Liu B, Frostegård A, Shapleigh JP (2013) Draft genome sequences of five strains in the genus Thauera. Genome Announc 1:1–2. Google Scholar
  62. Marchesi JR, Weightman AJ, Cragg BA, Parkes RJ, Fry JC (2001) Methanogen and bacterial diversity and distribution in deep gas hydrate sediments from the Cascadia Margin as revealed by 16S rRNA molecular analysis. FEMS Microbiol Ecol 34:221–228Google Scholar
  63. Marshall K, Stout R, Mitchell R (1971) Mechanism of the initial events in the sorption of marine bacteria to surfaces. J Gen Microbiol 68:337–348Google Scholar
  64. Mateo-Sagasta Dávila J, Khassab G, Klapwijk A, van Lier JB (2009) Combination of methanogenesis and denitrification in a UASB reactor for water reclamation applied to small agglomerations. Desalin Water Treat 4:177–182. Google Scholar
  65. Mori K, Hanada S, Maruyama A, Marumo K (2002) Thermanaeromonas toyohensis gen. nov., sp. nov., a novel thermophilic anaerobe isolated from a subterranean vein in the Toyoha Mines. Int J Syst Evol Microbiol 52:1675–1680. Google Scholar
  66. 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 7:283–290. Google Scholar
  67. Morozova D, Alawi M, Shaheed M, Kock D (2011) The influence of microbial activity on rock fluid interaction: baseline characterization of deep biosphere for Enhanced Gas Recovery in the Altmark natural gas reservoir. Energy Proc 4:4633–4640. Google Scholar
  68. Moura I, Bursakov S, Costa C, Moura JJ (1997) Nitrate and nitrite utilization in sulfate-reducing bacteria. Anaerobe 3:279–290. Google Scholar
  69. Moura JJG, Gonzalez P, Moura I, Fauque G (2007) Dissimilatory nitrate and nitrite ammonification by sulphate-reducing eubacteria. In: Barton L, Hamilton W (eds) Sulphate-reducing Bact Environ Eng Syst. Cambridge University Press, Cambridge, pp 241–264Google Scholar
  70. Muyzer G, Stams AJM (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6:441–454. Google Scholar
  71. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700Google Scholar
  72. Myhr S, Lillebø BLP, Sunde E, Beeder J, Torsvik T (2002) Inhibition of microbial H2S production in an oil reservoir model column by nitrate injection. Appl Microbiol Biotechnol 58:400–408. Google Scholar
  73. Nadkarni MA, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148:257–266Google Scholar
  74. Nakatsu CH, Torsvik V, Øvreås L (2000) Soil community analysis using DGGE of 16S rDNA polymerase chain reaction products. Soil Sci Soc Am J 64:1382–1388Google Scholar
  75. Nazina TN, Ivanova AE, Kanchaveli LP, Rozanova EP (1988) A new sporeforming thermophilic methylotrophic sulfate-reducing bacterium, Desulfotomaculum kuznetsovii sp. nov. Mikrobiol 57:823–827Google Scholar
  76. Nazina TN, Tourova TP, Poltaraus AB, Novikova EV, Grigoryan AA, Ivanova AE, Lysenko AM, Petrunyaka VV, Osipov GA, Belyaev SS, Ivanov MV (2001) Taxonomic study of aerobic thermophilic bacilli: descriptions of Geobacillus subterraneus gen. nov., sp. nov. and Geobacillus uzenensis sp. nov. from petroleum reservoirs and transfer of Bacillus stearothermophilus, Bacillus thermocatenulatus, Bacillus thermoleovorans, Bacillus kaustophilus, Bacillus thermoglucosidasius and Bacillus thermodenitrificans to Geobacillus as the new combinations G. stearothermophilus, G. thermocatenulatus, G. thermoleovorans, G. kaustophilus, G. thermoglucosidasius and G. thermodenitrificans. Int J Syst Evol Microbiol 51:433–446Google Scholar
  77. Nemati M, Jenneman GE, Voordouw G (2001) Impact of nitrate-mediated microbial control of souring in oil reservoirs on the extent of corrosion. Biotechnol Prog 17:852–859. Google Scholar
  78. Németh A, Szirányi B, Krett G, Janurik E, Kosáros T, Pekár F, Márialigeti K, Borsodi AK (2014) Prokaryotic phylogenetic diversity of Hungarian deep subsurface geothermal well waters. Acta Microbiol Immunol Hung 61:363–377. Google Scholar
  79. Nilsen RK, Torsvik T, Lien T (1996) Desulfotomaculum thermocisternum sp. nov., a sulfate reducer isolated from a hot north sea oil reservoir. Int J Syst Bacteriol 46:397–402Google Scholar
  80. Okabe S, Ito T, Satoh H, Watanabe Y (2003) Effects of nitrite and nitrate on biogenic sulfide production in sewer biofilms determined by the use of microelectrodes. Water Sci Technol 47:281–288Google Scholar
  81. Orphan VJ, Taylor LT, Hafenbradl D, DeLong EF (2000) Culture-independent characterization of microbial assemblages associated with high-temperature petroleum reservoirs. Appl Environ Microbiol 66:700–711. Google Scholar
  82. Oude Elferink SJWH, Visser A, Hulshoff Pol LW, Stams AJM (1994) Sulfate reduction in methanogenic bioreactors. FEMS Microbiol Rev 15:119–136Google Scholar
  83. Postgate JR (1979) The sulphate reducing bacteria. Cambridge University Press, CambridgeGoogle Scholar
  84. Reed DW, Fujita Y, Delwiche ME, Blackwelder DB, Sheridan PP, Uchida T, Colwell FS (2002) Microbial communities from methane hydrate-bearing deep marine sediments in a forearc basin. Appl Environ Microbiol 68:3759–3770. Google Scholar
  85. Rempel CL, Evitts RW, Nemati M (2006) Dynamics of corrosion rates associated with nitrite or nitrate mediated control of souring under biological conditions simulating an oil reservoir. J Ind Microbiol Biotechnol 33:878–886. Google Scholar
  86. Salter S, Cox M, Turek E, Calus S, Cookson W, Moffatt M, Turner P, Parkhill J, Loman N, Walker A (2014) Reagent contamination can critically impact sequence-based microbiome analyses. BMC Biol 12:87. Google Scholar
  87. Sand W (2003) Microbial life in geothermal waters. Geothermics 32:655–667. Google Scholar
  88. Sawayama S, Tada C, Tsukahara K, Yagishita T (2004) Effect of ammonium addition on methanogenic community in a fluidized bed anaerobic digestion. J Biosci Boeng 97:65–70. Google Scholar
  89. Schwermer CU, Lavik G, Abed RMM, Dunsmore B, Ferdelman TG, Stoodley P, Gieseke A, de Beer D (2008) Impact of nitrate on the structure and function of bacterial biofilm communities in pipelines used for injection of seawater into oil fields. Appl Environ Microbiol 74:2841–2851. Google Scholar
  90. Sercu B, Boon N, Vander Beken S, Verstraete W, Van Langenhove H (2007) Performance and microbial analysis of defined and non-defined inocula for the removal of dimethyl sulfide in a biotrickling filter. Biotechnol Bioeng 96:661–672. Google Scholar
  91. Shlimon AG, Friedrich MW, Niemann H, Ramsing NB, Finster K (2004) Methanobacterium aarhusense sp. nov., a novel methanogen isolated from a marine sediment. Int J Syst Evol Microbiol 54:759–763. Google Scholar
  92. Sorokin DY, Tourova TP, Kolganova TV, Detkova EN, Galinski EA, Muyzer G (2011) Culturable diversity of lithotrophic haloalkaliphilic sulfate-reducing bacteria in soda lakes and the description of Desulfonatronum thioautotrophicum sp. nov., Desulfonatronum thiosulfatophilum sp. nov., Desulfonatronovibrio thiodismutans sp. nov., and Desulfonatronovibrio magnus sp. nov. Extremophiles 15:391–401. Google Scholar
  93. Sorokin D, Tourova T, Muyzer G (2013) Isolation and characterization of two novel alkalitolerant sulfidogens from a Thiopaq bioreactor, Desulfonatronum alkalitolerans sp. nov., and Sulfurospirillum alkalitolerans sp. nov. Extremophiles 17:535–543. Google Scholar
  94. Steinberg LM, Regan JM (2008) Phylogenetic comparison of the methanogenic communities from an acidic, oligotrophic fen and an anaerobic digester treating municipal wastewater sludge. Appl Environ Microbiol 74:6663–6671. Google Scholar
  95. Suri N, Voordouw J, Voordouw G (2017) The effectiveness of nitrate-mediated control of the oil field sulfur cycle depends on the toluene content of the oil. Front Microbiol 8:1–13. Google Scholar
  96. Takai K, Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:5066–5072. Google Scholar
  97. Telang AJ, Ebert S, Foght JM, Westlake DWS, Jenneman GE, Gevertz D, Voordouw G (1997) Effect of nitrate injection on the microbial community in an oil field as monitored by reverse sample genome probing. Appl Environ Microbiol 63:1783–1785Google Scholar
  98. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680Google Scholar
  99. Wagner M, Roger AJ, Flax JL, Brusseau GA, Stahl DA (1998) Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. J Bacteriol 180:2975–2982Google Scholar
  100. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. Google Scholar
  101. Westphal A, Lerm S, Miethling-Graff R, Seibt A, Wolfgramm M, Würdemann H (2016) Effects of plant downtime on the microbial community composition in the highly saline brine of a geothermal plant in the North German Basin. Appl Microbiol Biotechnol 100:3277–3290. Google Scholar
  102. Wilms R, Sass H, Köpke B, Cypionka H, Engelen B (2007) Methane and sulfate profiles within the subsurface of a tidal flat are reflected by the distribution of sulfate-reducing bacteria and methanogenic archaea. FEMS Microbiol Ecol 59:611–621. Google Scholar
  103. Winfrey MR, Ward DM (1983) Substrates for sulfate reduction and methane production in intertidal sediments. Appl Environ Microbiol 45:193–199Google Scholar
  104. Wolfe B, Lui S, Cowan J (1994) Desulfoviridin, a multimeric-dissimilatory sulfite reductase from Desulfovibrio vulgaris (Hildenborough). Purification, characterization, kinetics and EPR studies. Eur J Biochem 223:79–89. Google Scholar
  105. Würdemann H, Westphal A, Kleyböcker A, Miethling-Graff R, Teitz S, Kasina M, Seibt A, Wolfgramm M, Eichinger F, Lerm S (2016) Störungen des Betriebs geothermischer Anlagen durch mikrobielle Stoffwechselprozesse und Erfolg von Gegenmaßnahmen. Grundwasser 21:93–106. Google Scholar
  106. Yin B, Wunch K (2017) Combined effects of microbes and nitrate on SRB growth, souring and corrosion. NACE Int Paper 9425:1–11Google Scholar
  107. Zakharyuk A, Kozyreva L, Khijniak T, Namsaraev B, Shcherbakova V (2015) Desulfonatronum zhilinae sp. nov., a novel haloalkaliphilic sulfate-reducing bacterium from soda Lake Alginskoe, Trans-Baikal Region, Russia. Extremophiles 19:673–680. Google Scholar
  108. Zeikus JG, Hegge PW, Anderson MA (1979) Thermoanaerobium brockii gen. nov. and sp. nov., a new chemoorganotrophic, caldoactive, anaerobic bacterium. Arch Microbiol 122:41–48Google Scholar
  109. Zhang T, Fang HHP, Ko BCB (2003) Methanogen population in a marine biofilm corrosive to mild steel. Appl Microbiol Biotechnol 63:101–106. Google Scholar
  110. Zhu ZY, Modi H, Kilbane JJ (2006) Efficacy and risks of nitrate application for the mitigation of SRB induced corrosion. Corros NACExpo 2006:1–41. Google Scholar
  111. Zillig W, Stetter KO, Schäfer W, Janekovic D, Wunderl S, Holz I, Palm P (1981) Thermoproteales: a novel type of extremely thermoacidophilic anaerobic archaebacteria isolated from Icelandic solfataras. Zentralblatt für Bakteriol Mikrobiol und Hyg 2:205–227Google Scholar
  112. Zillig W, Gierl A, Schreiber G, Wunderl S, Janekovic D, Stetter K, Klenk H (1983) The archaebacterium Thermofilum pendens represents, a novel genus of the thermophilic, anaerobic sulfur respiring Thermoproteales. Syst Appl Microbiol 4:79–87. Google Scholar

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Authors and Affiliations

  • Anke Westphal
    • 1
  • Florian Eichinger
    • 2
  • Lorenz Eichinger
    • 2
  • Hilke Würdemann
    • 1
    • 3
    Email author
  1. 1.Section 5.3 GeomicrobiologyGFZ German Research Centre for GeosciencesPotsdamGermany
  2. 2.HYDROISOTOP GmbHSchweitenkirchenGermany
  3. 3.Department of Engineering and Natural SciencesUniversity of Applied Science MerseburgMerseburgGermany

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