Applied Microbiology and Biotechnology

, Volume 88, Issue 5, pp 1027–1042 | Cite as

Sulfur-driven autotrophic denitrification: diversity, biochemistry, and engineering applications

  • Ming-Fei Shao
  • Tong Zhang
  • Herbert Han-Ping Fang


Sulfur-driven autotrophic denitrification refers to the chemolithotrophic process coupling denitrification with the oxidation of reduced inorganic sulfur compounds. Ever since 1904, when Thiobacillus denitrificans was isolated, autotrophic denitrifiers and their uncultured close relatives have been continuously identified from highly diverse ecosystems including hydrothermal vents, deep sea redox transition zones, sediments, soils, inland soda lakes, etc. Currently, 14 valid described species within α-, β-, γ-, and ε-Proteobacteria have been identified as capable of autotrophic denitrification. Autotrophic denitrification is also widely applied in environmental engineering for the removal of sulfide and nitrate from different water environments. This review summarizes recent researches on autotrophic denitrification, highlighting its diversity, metabolic traits, and engineering applications.


Autotrophic denitrification Sulfide Nitrate Chemolithotroph Proteobacteria Anoxic 



The authors wish to thank the Hong Kong Research Grants council for the financial support of this study (HKU7122/08E, HKU7122/10E), and Dr. Ming-Fei Shao wishes to thank The University of Hong Kong for postgraduate studentship and the postdoctoral fellowship.


  1. Alain K, Zbinden M, Le Bris N, Lesongeur F, Quérellou J, Gaill F, Cambon-Bonavita MA (2004) Early steps in microbial colonization processes at deep-sea hydrothermal vents. Environ Microbiol 6(3):227–241CrossRefGoogle Scholar
  2. Beijerinck MW (1904) Ueber die Bakterien, welche sich im Dunkeln mit Kohlensaure als Kohlenstoffquelle ernahren konnen. Centralbl Bakteriol Parasitenkd Infektionskr Hyg Abt II 11:593–599Google Scholar
  3. Beller HR, Chain PSG, Letain TE, Chakicherla A, Larimer FW, Richardson PM, Coleman MA, Wood AP, Kelly DP (2006a) The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans. J Bacteriol 188(4):1473–1488CrossRefGoogle Scholar
  4. Beller HR, Letain TE, Chakicherla A, Kane SR, Legler TC, Coleman MA (2006b) Whole-genome transcriptional analysis of chemolithoautotrophic thiosulfate oxidation by Thiobacillus denitrificans under aerobic versus denitrifying conditions. J Bacteriol 188(19):7005–7015CrossRefGoogle Scholar
  5. Beller HR, Legler TC, Bourguet F, Letain TE, Kane SR, Coleman MA (2009) Identification of c-type cytochromes involved in anaerobic, bacterial U (IV) oxidation. Biodegradation 20(1):45–53CrossRefGoogle Scholar
  6. Bezbaruah AN, Zhang TC (2003) Performance of a constructed wetland with a sulfur/limestone denitrification section for wastewater nitrogen removal. Environ Sci Technol 37(8):1690–1697CrossRefGoogle Scholar
  7. Bisogni JJ, Driscoll CT (1977) Denitrification using thiosulfate and sulfide. J Environ Eng Div 103:593–604Google Scholar
  8. Boon AG, Vincent AJ, Boon KG (1997) Avoiding the problems of septic sewage. Water Sci Technol 37(1):223–231Google Scholar
  9. Brannan DK, Caldwell DE (1980) Thermothrix thiopara: growth and metabolism of a newly isolated thermophile capable of oxidizing sulfur and sulfur compounds. Appl Environ Microbiol 40(2):211–216Google Scholar
  10. Brettar I, Rheinheimer G (1991) Denitrification in the Central Baltic: evidence for H2S-oxidation as motor of denitrification at the oxic–anoxic interface. Mar Ecol Prog Ser 77:157–169CrossRefGoogle Scholar
  11. Brettar I, Rheinheimer G (1992) Influence of carbon availability on denitrification in the central Baltic Sea. Limnol Oceanogr 37(6):1146–1163CrossRefGoogle Scholar
  12. Brettar I, Labrenz M, Flavier S, Botel J, Kuosa H, Christen R, Hofle MG (2006) Identification of a Thiomicrospira denitrificans-like epsilonproteobacterium as a catalyst for autotrophic denitrification in the central Baltic Sea. Appl Environ Microbiol 72(2):1364–1372CrossRefGoogle Scholar
  13. Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4:458–468CrossRefGoogle Scholar
  14. Cardoso RB, Sierra-Alvarez R, Rowlette P, Flores ER, Gómez J, Field JA (2006) Sulfide oxidation under chemolithoautotrophic denitrifying conditions. Biotechnol Bioeng 95(6):1148–1157CrossRefGoogle Scholar
  15. Chen C, Ren N, Wang A, Yu Z, Lee DJ (2008) Simultaneous biological removal of sulfur, nitrogen and carbon using EGSB reactor. Appl Microbiol Biotechnol 78(6):1057–1063CrossRefGoogle Scholar
  16. Christensen PB, Rysgaard S, Sloth NP, Dalsgaard T, Schwaerter S (2000) Sediment mineralization, nutrient fluxes, denitrification and dissimilatory nitrate reduction to ammonium in an estuarine fjord with sea cage trout farms. Aquat Microb Ecol 21(1):73–84CrossRefGoogle Scholar
  17. Dahl C, Hell R, Leustek T, Knaff D (2008) Introduction to sulfur metabolism in phototrophic organisms. In: Hell R, Dahl C, Knaff D, Leustek T (eds) Introduction to sulfur metabolism in phototrophic organisms. Springer, Netherlands, pp 1–14CrossRefGoogle Scholar
  18. Detmer AE, Giesenhagen HC, Trenkel VM, Auf dem Venne H, Jochem FJ (1993) Phototrophic and heterotrophic pico- and nanoplankton in anoxic depths of the central Baltic Sea. Mar Ecol Prog Ser 99:197–197CrossRefGoogle Scholar
  19. Driscoll CT, Bisogni JJ (1978) The use of sulfur and sulfide in packed bed reactors for autotrophic denitrification. J Water Pollut Control Fed 50(3):569–577Google Scholar
  20. Eichholzer M, Gutzwiller F (1998) Dietary nitrates, nitrites, and N-nitroso compounds and cancer risk: a review of the epidemiologic evidence. Nutr Rev 56(4):95–105CrossRefGoogle Scholar
  21. Eisenmann E, Beuerle J, Sulger K, Kroneck PM, Schumacher W (1995) Lithotrophic growth of Sulfurospirillum deleyianum with sulfide as electron donor coupled to respiratory reduction of nitrate to ammonia. Arch Microbiol 164(3):180–185CrossRefGoogle Scholar
  22. Engel AS, Porter ML, Stern LA, Quinlan S, Bennett PC (2004) Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfidic springs dominated by chemolithoautotrophic Epsilonproteobacteria. FEMS Microbiol Ecol 51(1):31–53CrossRefGoogle Scholar
  23. Flere JM, Zhang TC (1999) Nitrate removal with sulfur-limestone autotrophic denitrification processes. J Environ Eng 125(8):721–729CrossRefGoogle Scholar
  24. Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 67(7):2873–2882CrossRefGoogle Scholar
  25. Friedrich CG, Bardischewsky F, Rother D, Quentmeier A, Fischer J (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8(3):253–259CrossRefGoogle Scholar
  26. Gallardo VA (1977) Large benthic microbial communities in sulphide biota under Peru–Chile subsurface countercurrent. Nature 268:331–332CrossRefGoogle Scholar
  27. Garcia-de-Lomas J, Corzo A, Gonzalez JM, Andrades JA, Iglesias E, Montero MJ (2005) Nitrates promote biological oxidation of sulfide in wastewaters: experiment at plant-scale. Biotechnol Bioeng 93:801–811CrossRefGoogle Scholar
  28. Garcia-de-Lomas J, Corzo A, Carmen Portillo M, Gonzalez JM, Andrades JA, Saiz-Jimenez C, Garcia-Robledo E (2007) Nitrate stimulation of indigenous nitrate-reducing, sulfide-oxidising bacterial community in wastewater anaerobic biofilms. Water Res 41(14):3121–3131CrossRefGoogle Scholar
  29. Gevertz D, Telang AJ, Voordouw G, Jenneman GE (2000) Isolation and characterization of strains CVO and FWKO B, two novel nitrate-reducing, sulfide-oxidizing bacteria isolated from oil field brine. Appl Environ Microbiol 66(6):2491–2501CrossRefGoogle Scholar
  30. Glaubitz S, Lueders T, Abraham WR, Jost G, Jürgens K, Labrenz M (2009) 13C-isotope analyses reveal that chemolithoautotrophic Gamma- and Epsilonproteobacteria feed a microbial food web in a pelagic redoxcline of the central Baltic Sea. Environ Microbiol 11(2):326–337CrossRefGoogle Scholar
  31. Gocke K (1977) Untersuchungenüber die heterotrophe Aktivität in der zentralen Ostsee. Mar Biol 40(1):87–94CrossRefGoogle Scholar
  32. Gommers PJF, Kuenen JG (1988) Thiobacillus strain Q, a chemolithoheterotrophic sulphur bacterium. Arch Microbiol 150(2):117–125CrossRefGoogle Scholar
  33. Grote J, Labrenz M, Pfeiffer B, Jost G, Jurgens K (2007) Quantitative distributions of Epsilonproteobacteria and a Sulfurimonas subgroup in pelagic redoxclines of the central Baltic Sea. Appl Environ Microbiol 73(22):7155–7161CrossRefGoogle Scholar
  34. Grote J, Jost G, Labrenz M, Herndl GJ, Jurgens K (2008) Epsilonproteobacteria represent the major portion of chemoautotrophic bacteria in sulfidic waters of pelagic redoxclines of the Baltic and Black Seas. Appl Environ Microbiol 74(24):7546–7551CrossRefGoogle Scholar
  35. Gu JD, Qiu W, Koenig A, Fan Y, Choi E, Yun Z (2004) Removal of high NO 3-concentrations in saline water through autotrophic denitrification by the bacterium Thiobacillus denitrificans strain MP. Strong Nitrogenous and Agro-Wastewater 49(5):105–112Google Scholar
  36. Hamilton WA, Lee W (1995) Biocorrosion. In: Barton LL (ed) Sulfate-reducing bacteria. Plenum, New York, pp 242–264Google Scholar
  37. Hannig M, Lavik G, Kuypers MMM, Woebken D, Martens-Habbena W, Jürgens K (2007) Shift from denitrification to anammox after inflow events in the central Baltic Sea. Limnol Oceanogr 52(4):1336–1345Google Scholar
  38. Hodges TW, Olson JB (2009) Molecular comparison of bacterial communities within iron-containing flocculent mats associated with submarine volcanoes along the Kermadec Arc. Appl Environ Microbiol 75(6):1650–1657CrossRefGoogle Scholar
  39. Hoek J, Banta A, Hubler F, Reysenbach AL (2003) Microbial diversity of a sulphide spire located in the Edmond deep-sea hydrothermal vent field on the Central Indian Ridge. Geobiology 1(2):119–127CrossRefGoogle Scholar
  40. Hofle MG, Flavier S, Christen R, Botel J, Labrenz M, Brettar I (2005) Retrieval of nearly complete 16S rRNA gene sequences from environmental DNA following 16S rRNA-based community fingerprinting. Environ Microbiol 7(5):670–675CrossRefGoogle Scholar
  41. Huettel M, Forster S, Kloser S, Fossing H (1996) Vertical migration in the sediment-dwelling sulfur bacteria Thioploca spp. in overcoming diffusion limitations. Appl Environ Microbiol 62(6):1863–1872Google Scholar
  42. Jiang G, Sharma KR, Guisasola A, Keller J, Yuan Z (2009) Sulfur transformation in rising main sewers receiving nitrate dosage. Water Res 43(17):4430–4440CrossRefGoogle Scholar
  43. Jorgensen BB (1990) A thiosulfate shunt in the sulfur cycle of marine sediments. Science 249(4965):152–154CrossRefGoogle Scholar
  44. Jorgensen BB, Nelson DC (2004) Sulfide oxidation in marine sediments: geochemistry meets microbiology. In: Amend JP, Edwards KJ, Lyons TW (eds) Sulfur biogeochemistry—past and present. Geological Society of America, Colorado, pp 63–81CrossRefGoogle Scholar
  45. Kellermann C, Griebler C (2009) Thiobacillus thiophilus sp. nov., a chemolithoautotrophic, thiosulfate-oxidizing bacterium isolated from contaminated aquifer sediments. Int J Syst Evol Microbiol 59(3):583–588CrossRefGoogle Scholar
  46. Kelly DP, Wood AP (2000) Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen. nov., Halothiobacillus gen. nov. and Thermithiobacillus gen. nov. Int J Syst Evol Microbiol 50(2):511–516Google Scholar
  47. Kimura K, Nakamura M, Watanabe Y (2002) Nitrate removal by a combination of elemental sulfur-based denitrification and membrane filtration. Water Res 36(7):1758–1766CrossRefGoogle Scholar
  48. Kleerebezem R, Mendez R (2002) Autotrophic denitrification for combined hydrogen sulfide removal from biogas and post-denitrification. Anaerob Dig 45(10):349–356Google Scholar
  49. Kluyver AJ, Donker HJ (1926) Die einheit in der biochemie. Chem Zelle Gewebe 13:134–190Google Scholar
  50. Knowles R (1982) Denitrification. Microbiol Rev 46(1):43–70Google Scholar
  51. Kodama Y, Watanabe K (2004) Sulfuricurvum kujiense gen. nov., sp. nov., a facultatively anaerobic, chemolithoautotrophic, sulfur-oxidizing bacterium isolated from an underground crude-oil storage cavity. Int J Syst Evol Microbiol 54(6):2297–2300CrossRefGoogle Scholar
  52. Koenig A, Liu LH (1996) Autotrophic denitrification of landfill leachate using elemental sulphur. Water Sci Technol 34(5):469–476CrossRefGoogle Scholar
  53. Koenig A, Liu LH (2001) Kinetic model of autotrophic denitrification in sulphur packed-bed reactors. Water Res 35(8):1969–1978CrossRefGoogle Scholar
  54. Koenig A, Liu LH (2002) Use of limestone for pH control in autotrophic denitrification: continuous flow experiments in pilot-scale packed bed reactors. J Biotechnol 99(2):161–171CrossRefGoogle Scholar
  55. Koenig A, Liu LH (2004) Autotrophic denitrification of high-salinity wastewater using elemental sulfur: batch tests. Water Environ Res 76(1):37–46CrossRefGoogle Scholar
  56. Koenig A, Zhang T, Liu LH, Fang HH (2005) Microbial community and biochemistry process in autosulfurotrophic denitrifying biofilm. Chemosphere 58(8):1041–1047CrossRefGoogle Scholar
  57. Kormas KA, Tivey MK, Von Damm K, Teske A (2006) Bacterial and archaeal phylotypes associated with distinct mineralogical layers of a white smoker spire from a deep-sea hydrothermal vent site (9N, East Pacific Rise). Environ Microbiol 8(5):909–920CrossRefGoogle Scholar
  58. Kuai L, Verstraete W (1999) Autotrophic denitrification with elemental sulphur in small-scale wastewater treatment facilities. Environ Technol 20(2):201–209CrossRefGoogle Scholar
  59. Labrenz M, Brettar I, Christen R, Flavier S, Botel J, Hofle MG (2004) Development and application of a real-time PCR approach for quantification of uncultured bacteria in the central Baltic Sea. Appl Environ Microbiol 70(8):4971–4979CrossRefGoogle Scholar
  60. Labrenz M, Jost G, Pohl C, Beckmann S, Martens-Habbena W, Jurgens K (2005) Impact of different in vitro electron donor/acceptor conditions on potential chemolithoautotrophic communities from marine pelagic redoxclines. Appl Environ Microbiol 71(11):6664–6672CrossRefGoogle Scholar
  61. Labrenz M, Jost G, Jürgens K (2007) Distribution of abundant prokaryotic organisms in the water column of the central Baltic Sea with an oxic–anoxic interface. Aquat Microb Ecol 46(2):177–190CrossRefGoogle Scholar
  62. Larkin JM, Strohl WR (1983) Beggiatoa, Thiothrix, and Thioploca. Annu Rev Microbiol 37(1):341–367CrossRefGoogle Scholar
  63. Lavik G, Stührmann T, Brüchert V, Van der Plas A, Mohrholz V, Lam P, Mussmann M, Fuchs BM, Amann R, Lass U (2008) Detoxification of sulphidic African shelf waters by blooming chemolithotrophs. Nature 457(7229):581–584CrossRefGoogle Scholar
  64. Lee DU, Lee IS, Choi YD, Bae JH (2001) Effects of external carbon source and empty bed contact time on simultaneous heterotrophic and sulfur-utilizing autotrophic denitrification. Process Biochem 36(12):1215–1224CrossRefGoogle Scholar
  65. Letain TE, Kane SR, Legler TC, Salazar EP, Agron PG, Beller HR (2007) Development of a genetic system for the chemolithoautotrophic bacterium Thiobacillus denitrificans. Appl Environ Microbiol 73(10):3265–3271CrossRefGoogle Scholar
  66. Lin X, Wakeham SG, Putnam IF, Astor YM, Scranton MI, Chistoserdov AY, Taylor GT (2006) Comparison of vertical distributions of prokaryotic assemblages in the anoxic Cariaco Basin and Black Sea by use of fluorescence in situ hybridization. Appl Environ Microbiol 72(4):2679–2690CrossRefGoogle Scholar
  67. Liu LH, Koenig A (2002) Use of limestone for pH control in autotrophic denitrification: batch experiments. Process Biochem 37(8):885–893CrossRefGoogle Scholar
  68. Lopez-Garcia P, Gaill F, Moreira D (2002) Wide bacterial diversity associated with tubes of the vent worm Riftia pachyptila. Environ Microbiol 4(4):204–215CrossRefGoogle Scholar
  69. López-Garcia P, Duperron S, Philippot P, Foriel J, Susini J, Moreira D (2003) Bacterial diversity in hydrothermal sediment and epsilonproteobacterial dominance in experimental microcolonizers at the Mid-Atlantic Ridge. Environ Microbiol 5(10):961–976CrossRefGoogle Scholar
  70. Lowson RT (1982) Aqueous oxidation of pyrite by molecular oxygen. Chem Rev 82(5):461–497CrossRefGoogle Scholar
  71. Ludwig W, Mittenhuber G, Friedrich CG (1993) Transfer of Thiosphaera pantotropha to Paracoccus denitrificans. Int J Syst Evol Microbiol 43(2):363–367Google Scholar
  72. Luther GW III (1987) Pyrite oxidation and reduction: molecular orbital theory considerations. Geochim Cosmochim Acta 51:3193–3199CrossRefGoogle Scholar
  73. Luther GW III (1990) The frontier-molecular-orbital theory approach in geotechnical processes. In: Stumm W (ed) Aquatic chemical kinetics. Wiley, New York, pp 173–181Google Scholar
  74. Madrid VM, Taylor GT, Scranton MI, Chistoserdov AY (2001) Phylogenetic diversity of bacterial and archaeal communities in the anoxic zone of the Cariaco Basin. Appl Environ Microbiol 67(4):1663–1674CrossRefGoogle Scholar
  75. Manconi I, Carucci A, Lens P (2007) Combined removal of sulfur compounds and nitrate by autotrophic denitrification in bioaugmented activated sludge system. Biotechnol Bioeng 98(3):551–560CrossRefGoogle Scholar
  76. Mills HJ, Martinez RJ, Story S, Sobecky PA (2004) Identification of members of the metabolically active microbial populations associated with Beggiatoa species mat communities from Gulf of Mexico cold-seep sediments. Appl Environ Microbiol 70(9):5447–5458CrossRefGoogle Scholar
  77. Moon HS, Ahn KH, Lee S, Nam K, Kim JY (2004) Use of autotrophic sulfur-oxidizers to remove nitrate from bank filtrate in a permeable reactive barrier system. Environ Pollut 129(3):499–507CrossRefGoogle Scholar
  78. Moon HS, Chang SW, Nam K, Choe J, Kim JY (2006) Effect of reactive media composition and co-contaminants on sulfur-based autotrophic denitrification. Environ Pollut 144(3):802–807CrossRefGoogle Scholar
  79. Moussard H, Corre E, Cambon-Bonavita MA, Fouquet Y, Jeanthon C (2006) Novel uncultured Epsilonproteobacteria dominate a filamentous sulphur mat from the 13N hydrothermal vent field, East Pacific Rise. FEMS Microbiol Ecol 58:449–463CrossRefGoogle Scholar
  80. Murphy TP, Lawson A, Kumagai M, Babin J (1999) Review of emerging issues in sediment treatment. Aquat Ecosyst Health Manag 2(4):419–434CrossRefGoogle Scholar
  81. Nakagawa S, Takai K (2008) Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. FEMS Microbiol Ecol 65(1):1–14CrossRefGoogle Scholar
  82. Nakagawa S, Takai K, Inagaki F, Hirayama H, Nunoura T, Horikoshi K, Sako Y (2005) Distribution, phylogenetic diversity and physiological characteristics of epsilon-proteobacteria in a deep-sea hydrothermal field. Environ Microbiol 7(10):1619–1632CrossRefGoogle Scholar
  83. Nakagawa S, Takaki Y, Shimamura S, Reysenbach AL, Takai K, Horikoshi K (2007) Deep-sea vent epsilon-proteobacterial genomes provide insights into emergence of pathogens. Proc Natl Acad Sci USA 104(29):12146–12150CrossRefGoogle Scholar
  84. Nehring D (1987) Temporal variations of phosphate and inorganic nitrogen compounds in central Baltic deep waters. Limnol Oceanogr 32(2):494–499CrossRefGoogle Scholar
  85. Nelson DC, Revsbech NP, Jorgensen BB (1986) Microoxic-anoxic niche of Beggiatoa spp.: microelectrode survey of marine and freshwater strains. Appl Environ Microbiol 52(1):161–168Google Scholar
  86. Oh SE, Yoo YB, Young JC, Kim IS (2001) Effect of organics on sulfur-utilizing autotrophic denitrification under mixotrophic conditions. J Biotechnol 92(1):1–8CrossRefGoogle Scholar
  87. Ongcharit C, Sublette KL, Shah YT (1991) Oxidation of hydrogen sulfide by flocculated Thiobaccillus denitrificans in a continuous culture. Biotechnol Bioeng 37(6):497–504CrossRefGoogle Scholar
  88. Otte S, Kuenen JG, Nielsen LP, Paerl HW, Zopfi J, Schulz HN, Teske A, Strotmann B, Gallardo VA, Jorgensen BB (1999) Nitrogen, carbon, and sulfur metabolism in natural Thioploca samples. Appl Environ Microbiol 65(7):3148–3157Google Scholar
  89. Page A, Juniper SK, Olagnon M, Alain K, Desrosiers G, Querellou J, Cambon-Bonavita MA (2004) Microbial diversity associated with a Paralvinella sulfincola tube and the adjacent substratum on an active deep-sea vent chimney. Geobiology 2(4):225–238CrossRefGoogle Scholar
  90. Park JH, Shin HS, Lee IS, Bae JH (2002) Denitrification of high NO3-N containing wastewater using elemental sulfur; nitrogen loading rate and N2O production. Environ Technol 23(1):53–65CrossRefGoogle Scholar
  91. Podgorsek L, Imhoff JF (1999) Tetrathionate production by sulfur oxidizing bacteria and the role of tetrathionate in the sulfur cycle of Baltic Sea sediments. Aquat Microb Ecol 17:255–265CrossRefGoogle Scholar
  92. Pomeroy RD, Boon AG (1990) The problem of hydrogen sulfide in sewers, 2nd edn. Clay Pipe Development Association Ltd, London, pp 1–24Google Scholar
  93. Rainey FA, Kelly DP, Stackebrandt E, Burghardt J, Hiraishi A, Katayama Y, Wood AP (1999) A re-evaluation of the taxonomy of Paracoccus denitrificans and a proposal for the combination Paracoccus pantotrophus comb. nov. Int J Syst Evol Microbiol 49(2):645–651Google Scholar
  94. Ravich-Sherbo J (1930) On the question of the bacterial thin layer in the Black Sea according to the hypothesis of Prof. Egounoff. Travaux de la Station Biologique de Sebastopol 2:127–141Google Scholar
  95. Reyes-Avila J, Razo-Flores E, Gomez J (2004) Simultaneous biological removal of nitrogen, carbon and sulfur by denitrification. Water Res 38(14–15):3313–3321CrossRefGoogle Scholar
  96. Richardson DJ, Ferguson SJ (1992) The influence of carbon substrate on the activity of the periplasmic nitrate reductase in aerobically grown Thiosphaera pantotropha. Arch Microbiol 157:535–537Google Scholar
  97. Robertson LA, Kuenen JG (1983) Thiosphaera pantotropha gen. nov. sp. nov., a facultatively anaerobic, facultatively autotrophic sulphur bacterium. Microbiology 129(9):2847–2855CrossRefGoogle Scholar
  98. Robertson LA, Kuenen JG (2006) The genus Thiobacillus. In: Dworkin M, Falkow E, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes: an evolving electronic resource for the microbial community. Springer, New York, pp 812–827Google Scholar
  99. Sánchez I, Fernández N, Amils R, Sanz JL (2008) Assessment of the addition of Thiobacillus denitrificans and Thiomicrospira denitrificans to chemoithoautotrophic denitrifying bioreactors. Int Microbiol 11(3):179–184Google Scholar
  100. Schindler DW, Armstrong FA, Holmgren SK, Brunkill GJ (1971) Eutrophication of lake 227, experimental lakes area, Northwest Ontario, by addition of phosphorus and nitrates. J Fish Res Board Can 28:1763–82Google Scholar
  101. Schippers A (2004) Biogeochemistry of metal sulfide oxidation in mining environments, sediments and soils. In: Amend JP, Edwards KJ, Lyons TW (eds) Sulfur biogeochemistry—past and present. Geological Society of America, Colorado, pp 49–62CrossRefGoogle Scholar
  102. Schippers A, Jozsa P, Sand W (1996) Sulfur chemistry in bacterial leaching of pyrite. Appl Environ Microbiol 62(9):3424–3431Google Scholar
  103. Scott KM, Sievert SM, Abril FN, Ball LA, Barrett CJ, Blake RA, Boller AJ, Chain PS, Clark JA, Davis CR et al (2006) The genome of deep-sea vent chemolithoautotroph Thiomicrospira crunogena XCL-2. PLoS Biol 4(12):2196–2212CrossRefGoogle Scholar
  104. Shao M, Zhang T, Fang HH (2009) Autotrophic denitrification and its effect on metal speciation during marine sediment remediation. Water Res 43(12):2961–2968CrossRefGoogle Scholar
  105. Sierra-Alvarez R, Beristain-Cardoso R, Salazar M, Gómez J, Razo-Flores E, Field JA (2007) Chemolithotrophic denitrification with elemental sulfur for groundwater treatment. Water Res 41(6):1253–1262CrossRefGoogle Scholar
  106. Sievert SM, Scott KM, Klotz MG, Chain PSG, Hauser LJ, Hemp J, Hugler M, Land M, Lapidus A, Larimer FW, Lucas S, Malfatti SA, Meyer F, Paulsen IT, Ren Q, Simon J (2008) Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl Environ Microbiol 74(4):1145–1156CrossRefGoogle Scholar
  107. Soares MIM (2002) Denitrification of groundwater with elemental sulfur. Water Res 36(5):1392–1395CrossRefGoogle Scholar
  108. Sorensen J, Jorgensen BB (1987) Early diagenesis in sediments from Danish coastal waters: microbial activity and Mn–Fe–S geochemistry. Geochim Cosmochim Acta 51(6):1583–1590CrossRefGoogle Scholar
  109. Sorokin JI (1964) On the primary production and bacterial activities in the Black Sea. ICES J Mar Sci 29(1):41–60CrossRefGoogle Scholar
  110. Sorokin DY (2008) Diversity of halophilic sulfur-oxidizing bacteria in hypersaline habitats. In: Dahl C, Friedrich CG (eds) Microbial sulfur metabolism. Springer, Berlin Heidelberg, pp 225–237CrossRefGoogle Scholar
  111. Sorokin DY, Kuenen JG (2005) Alkaliphilic chemolithotrophs from soda lakes. FEMS Microbiol Ecol 52:287–295CrossRefGoogle Scholar
  112. Sorokin DY, Kuenen JG (2006) Haloalkaliphilic sulfur-oxidizing bacteria in soda lakes. FEMS Microbiol Rev 29(4):685–702CrossRefGoogle Scholar
  113. Sorokin DY, Lysenko AM, Mityushina LL (1996) Isolation and characterization of alkaliphilic heterotrophic bacteria capable of oxidation of inorganic sulfur compounds to tetrathionate. Microbiology 65:370–383Google Scholar
  114. Sorokin DY, Gijs Kuenen J, Jetten MS (2001a) Denitrification at extremely high pH values by the alkaliphilic, obligately chemolithoautotrophic, sulfur-oxidizing bacterium Thioalkalivibrio denitrificans strain ALJD. Arch Microbiol 175(2):94–101CrossRefGoogle Scholar
  115. Sorokin DY, Lysenko AM, Mityushina LL, Tourova TP, Jones BE, Rainey FA, Robertson LA, Kuenen GJ (2001b) Thioalkalimicrobium aerophilum gen. nov., sp. nov. and Thioalkalimicrobium sibericum sp. nov., and Thioalkalivibrio versutus gen. nov., sp. nov., Thioalkalivibrio nitratis sp. nov. and Thioalkalivibrio denitrificans sp. nov., novel obligately alkaliphilic and obligately chemolithoautotrophic sulfur-oxidizing bacteria from soda lakes. Int J Syst Evol Microbiol 51(2):565–580Google Scholar
  116. Sorokin DY, Tourova TP, Kolganova TV, Sjollema KA, Kuenen JG (2002) Thioalkalispira microaerophila gen. nov., sp. nov., a novel lithoautotrophic, sulfur-oxidizing bacterium from a soda lake. Int J Syst Evol Microbiol 52:2175–2182CrossRefGoogle Scholar
  117. Sorokin DY, Tourova TP, Sjollema KA, Kuenen JG (2003) Thialkalivibrio nitratireducens sp. nov., a nitrate-reducing member of an autotrophic denitrifying consortium from a soda lake. Int J Syst Evol Microbiol 53(6):1779–1783CrossRefGoogle Scholar
  118. Sorokin DY, Tourova TP, Antipov AN, Muyzer G, Kuenen JG (2004) Anaerobic growth of the haloalkaliphilic denitrifying sulfur-oxidizing bacterium Thioalkalivibrio thiocyanodenitrificans sp. nov. with thiocyanate. Microbiol 150:2435–2442CrossRefGoogle Scholar
  119. Sorokin DY, Tourova TP, Braker G, Muyzer G (2007a) Thiohalomonas denitrificans gen. nov., sp. nov. and Thiohalomonas nitratireducens sp. nov., novel obligately chemolithoautotrophic, moderately halophilic, thiodenitrifying Gammaproteobacteria from hypersaline habitats. Int J Syst Evol Microbiol 57(7):1582–1589CrossRefGoogle Scholar
  120. Sorokin DY, Tourova TP, Bezsoudnova EY, Pol A, Muyzer G (2007b) Denitrification in a binary culture and thiocyanate metabolism in Thiohalophilus thiocyanoxidans gen. nov. sp. nov.—a moderately halophilic chemolithoautotrophic sulfur-oxidizing gammaproteobacterium from hypersaline lakes. Arch Microbiol 187(6):441–450CrossRefGoogle Scholar
  121. Sorokin DY, Tourova TP, Galinski EA, Muyzer G, Kuenen JG (2008) Thiohalorhabdus denitrificans gen. nov., sp. nov., an extremely halophilic, sulfur-oxidizing, deep-lineage gammaproteobacterium from hypersaline habitats. Int J Syst Evol Microbiol 58(12):2890–2897CrossRefGoogle Scholar
  122. Spiridonova EM, Berg IA, Kolganova TV, Ivanovsky RN, Kuznetsov BB, Tourova TP (2004) An oligonucleotide primer system for amplification of the ribulose-1, 5-bisphosphate carboxylase/oxygenase genes of bacteria of various taxonomic groups. Microbiology 73(3):316–325CrossRefGoogle Scholar
  123. Stewart V (1988) Nitrate respiration in relation to facultative metabolism in enterobacteria. Microbiol Mol Biol Rev 52(2):190–232Google Scholar
  124. Straub KL, Benz M, Schink B, Widdel F (1996) Anaerobic, nitrate-dependent microbial oxidation of ferrous iron. Appl Environ Microbiol 62(4):1458–1460Google Scholar
  125. Sublette KL, Sylvester ND (1986) Microbial desulfurization of gases. Biotechnol Bioeng Symp Ser 17:543–564Google Scholar
  126. Takai K, Suzuki M, Nakagawa S, Miyazaki M, Suzuki Y, Inagaki F, Horikoshi K (2006) Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas. Int J Syst Evol Microbiol 56(8):1725–1733CrossRefGoogle Scholar
  127. Takashima T, Nishiki T, Konishi Y (2000) Anaerobic oxidation of dissolved hydrogen sulfide in continuous culture of the phototrophic bacterium Prosthecochloris aestuarii. J Biosci Bioeng 89(3):247–251CrossRefGoogle Scholar
  128. Teske A, Hinrichs KU, Edgcomb V, de Vera GA, Kysela D, Sylva SP, Sogin ML, Jannasch HW (2002) Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities. Appl Environ Microbiol 68(4):1994–2007CrossRefGoogle Scholar
  129. Timmer-ten-Hoor A (1975) A new type of thiosulphate oxidizing, nitrate reducing microorganism: the Omicrospira Dentrificans sp. Nov. J Sea Res 9(3–4):344–350Google Scholar
  130. Tosques IE, Shi J, Shapleigh JP (1996) Cloning and characterization of nnrR, whose product is required for the expression of proteins involved in nitric oxide metabolism in Rhodobacter sphaeroides. J Bacteriol 178(16):4958–4964Google Scholar
  131. Tourova TP, Spiridonova EM, Berg IA, Kuznetsov BB, Sorokin DY (2006) Occurrence, phylogeny and evolution of ribulose-1,5-bisphosphate carboxylase/oxygenase genes in obligately chemolithoautotrophic sulfur-oxidizing bacteria of the genera Thiomicrospira and Thioalkalimicrobium. Microbiology 152(7):2159–2169CrossRefGoogle Scholar
  132. Trouve C, Chazal PM, Gueroux B, Sauvaitre N (1998) Denitrification by new strains of Thiobacillus denitrificans under non-standard physicochemical conditions. Effect of temperature, pH, and sulphur source. Environ Technol 19(6):601–610CrossRefGoogle Scholar
  133. Urakawa H, Dubilier N, Fujiwara Y, Cunningham DE, Kojima S, Stahl DA (2005) Hydrothermal vent gastropods from the same family (Provannidae) harbour ɛ- and gamma-proteobacterial endosymbionts. Environ Microbiol 7(5):750–754CrossRefGoogle Scholar
  134. Vaiopoulou E, Melidis P, Aivasidis A (2005) Sulfide removal in wastewater from petrochemical industries by autotrophic denitrification. Water Res 39(17):4101–4109CrossRefGoogle Scholar
  135. Van der Hoek JP, Kappelhof J, Hijnen WAM (1992) Biological nitrate removal from ground water by sulphur/limestone denitrification. J Chem Technol Biotechnol 54(2):197–200Google Scholar
  136. Vetriani C, Tran HV, Kerkhof LJ (2003) Fingerprinting microbial assemblages from the oxic/anoxic chemocline of the Black Sea. Appl Environ Microbiol 69(11):6481–6488CrossRefGoogle Scholar
  137. Wang F, Chapman P (1999) Biological implications of sulfide in sediment—a review focusing on sediment toxicity. Environ Toxicol Chem 18(11):2526–2532Google Scholar
  138. Wang H, Qu J (2003) Combined bioelectrochemical and sulfur autotrophic denitrification for drinking water treatment. Water Res 37(15):3767–3775CrossRefGoogle Scholar
  139. Yavuz B, Türker M, Engin G (2007) Autotrophic removal of sulphide from industrial wastewaters using oxygen and nitrate as electron acceptors. Environ Eng Sci 24(4):457–470CrossRefGoogle Scholar
  140. Zeng H, Zhang TC (2005) Evaluation of kinetic parameters of a sulfur–limestone autotrophic denitrification biofilm process. Water Res 39(20):4941–4952CrossRefGoogle Scholar
  141. Zhang TC, Lampe DG (1999) Sulfur: limestone autotrophic denitrification processes for treatment of nitrate-contaminated water: batch experiments. Water Res 33(3):599–608CrossRefGoogle Scholar
  142. Zhang TC, Shan J (1999) In situ septic tank effluent denitrification using a sulfur–limestone process. Water Environ Res 71(7):1283–1291CrossRefGoogle Scholar
  143. Zhang TC, Zeng H (2006) Development of a response surface for prediction of nitrate removal in sulfur–limestone autotrophic denitrification fixed-bed reactors. J Environ Eng 132:1068–1072CrossRefGoogle Scholar
  144. Zhang Z, Lei Z, He X, Zhang Z, Yang Y, Sugiura N (2009a) Nitrate removal by Thiobacillus denitrificans immobilized on poly (vinyl alcohol) carriers. J Hazard Mater 163(2–3):1090–1095CrossRefGoogle Scholar
  145. Zhang M, Zhang T, Shao MF, Fang HHP (2009b) Autotrophic denitrification in nitrate-induced marine sediment remediation and Sulfurimonas denitrificans-like bacteria. Chemosphere 76(5):677–682CrossRefGoogle Scholar
  146. Zhao Z, Qiu W, Koenig A, Fan X, Gu JD (2004) Nitrate removal from saline water using autotrophic denitrification by the bacterium Thiobacillus denitrificans MP-1. Environ Technol 25(10):1201–1210CrossRefGoogle Scholar
  147. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61(4):533–616Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Ming-Fei Shao
    • 1
  • Tong Zhang
    • 1
  • Herbert Han-Ping Fang
    • 1
  1. 1.Department of Civil EngineeringThe University of Hong KongHong KongChina

Personalised recommendations