Colorless Sulfur Bacteria

  • Gerard Muyzer
  • J. Gijs Kuenen
  • Lesley A. Robertson


Since its recognition in the late nineteenth century, the ability to gain metabolically useful energy from the oxidation of reduced sulfur compounds by bacteria has been regarded as of such significance that it has been used as a primary characteristic in taxonomy. Essentially, any Gram-negative rod that could grow with a reduced sulfur compound as its primary energy source was automatically called “Thiobacillus.” Similar bacteria with a spiral shape became “Thiomicrospira,” and so on. As research progressed over the years, this approach has become steadily less satisfactory, and the development of genetic methods for identification has finally confirmed that the ability to metabolize reduced sulfur compounds is of no more taxonomic significance than the utilization of any other specialized substrate.

This chapter describes the scientific stages taken to reach this point, reviews the reorganization that has been necessary among the colorless sulfur bacteria, and considers the fact that while the metabolic trait is of less taxonomic significance than previously believed, this grouping is important ecologically and should be retained.


Hydrothermal Vent Acidithiobacillus Ferrooxidans Reduce Sulfur Compound Organic Sulfide Acidithiobacillus Thiooxidans 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Agate AD, Vishniac WV (1973) Characterization of thiobacillus species by gas-liquid chromatography of cellular fatty acids. Arch Microbiol 89:257–267Google Scholar
  2. Alain K, Querellou J (2009) Cultivating the uncultured: limits, advances and future challenges. Extremophiles 13:583–594PubMedCrossRefGoogle Scholar
  3. Amann R, Fuchs BM (2008) Single-cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nat Rev Microbiol 6:339–348PubMedCrossRefGoogle Scholar
  4. Aminuddin N, Nicholas DJD (1973) Sulphide oxidation linked to the reduction of nitrate and nitrite in Thiobacillus denitrificans. Biochim Biophys Acta 325:81–93PubMedCrossRefGoogle Scholar
  5. Andreae MC, Barnard WR (1984) The marine chemistry of dimethylsulfide. Marine Chem 14:267–279CrossRefGoogle Scholar
  6. Arkestein GJMW (1980) Contribution of microorganisms to the oxidation of pyrite. PhD Thesis, Agricultural University of Wageningen, The NetherlandsGoogle Scholar
  7. Bak F, Pfennig N (1987) Chemolithotrophic growth of Desulfovibrio sulfodismutans sp.nov. by disproportionation of inorganic sulfur compounds. Arch Microbiol 147:184–189CrossRefGoogle Scholar
  8. Banciu HL, Sorokin DY, Tourova TP, Galinski EA, Muntyan MS, Kuenen JG, Muyzer G (2008) Influence of salts and pH on growth and activity of a novel facultatively alkaliphilic, extremely salt-tolerant, obligately chemolithoautotrophic sulfur-oxidizing Gammaproteobacterium Thioalkalibacter halophilus gen. nov., sp. nov. from South-Western Siberian soda lakes. Extremophiles 12:391–404PubMedCrossRefGoogle Scholar
  9. Beijerinck MW (1904) Phenomenes de reduction produits par les microbes. Archives Neerlandaises Sciences Exactes et Naturelles (Sect. 2) 9:131–157Google Scholar
  10. Beller HR, Letain TE, Chakicherla A, Kane SR, Legler TC, Coleman MA (2006) Whole-genome transcriptional analysis of chemolithoautotrophic thiosulfate oxidation by Thiobacillus denitrificans under aerobic versus denitrifying conditions. J Bacteriol 188:7005–7015PubMedCrossRefGoogle Scholar
  11. Beudeker RF, Cannon GC, Kuenen JG, Shively JM (1980) Relations between d-ribulose-1, 5-bisphosphate carboxylase, carboxysomes, and CO2- fixing capacity in the obligate chemolithotroph Thiobacillus neapolitanus grown under different limitations in the chemostat. Arch Microbiol 124:185–189CrossRefGoogle Scholar
  12. Beudeker RF, de Boer W, Kuenen JG (1981) Heterolactic fermentation of intracellular polyglucose by the obligate chemolithotroph Thiobacillus neapolitanus under anaerobic conditions. FEMS Microbiol Lett 12:337–342CrossRefGoogle Scholar
  13. Boden RD, Cleveland PN, Green Y, Katayama Y, Uchino J, Murrell C, Kelly DP (2011) Phylogenetic assessment of culture collection strains of Thiobacillus thioparus, and definitive 16S rRNA gene sequences for T. thioparus, T. denitrificans, and Halothiobacillus neapolitanus. Arch Microbiol. doi:10.1007/s00203-011-0747-0Google Scholar
  14. Bonnet-Smits EM, Robertson LA, van Dijken JP, Senior E, Kuenen JG (1988) Carbon dioxide fixation as the initial step in the metabolism of acetone by Thiosphaera pantotropha. J Gen Microbiol 134:2281–2289Google Scholar
  15. Bos P, Kuenen JG (1983) Microbiology of sulphur oxidizing bacteria. Microbial Corrosion. The Metals Society, London, pp 18–27Google Scholar
  16. Bos P, Kuenen JG (1990) Microbial treatment of coal. In: Ehrlich H, Brierley C (eds) Microbial mineral recovery. McGraw-Hill, New York, pp 344–377Google Scholar
  17. Bos P, Huber TF, Luyben KCAM, Kuenen JG (1988) Feasibility of a Dutch process for microbial desulphurization of coal. Resour Conserv Recycl 1:279–291CrossRefGoogle Scholar
  18. 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 40:211–216PubMedGoogle Scholar
  19. Brierley CL (1982) Microbiological mining. Sci Am 247:42–51CrossRefGoogle Scholar
  20. Brierley JA, Lockwood SL (1977) The occurrence of thermophilic iron-oxidizing bacteria in a copper leaching system. FEMS Microbiol Lett 2:163–165CrossRefGoogle Scholar
  21. Brock TD, Gustafson J (1976) Ferric iron reduction by sulfur and iron oxidizing bacteria. Appl Environ Microbiol 32:567–571PubMedGoogle Scholar
  22. Brock TD, Brock KM, Belly RT, Weiss RL (1972) Sulfolobus: A new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch Mikrobiol 84:54–68PubMedCrossRefGoogle Scholar
  23. Buisman CJN (1989) Biotechnological sulphide removal with oxygen. PhD Thesis, Agricultural University of Wageningen, The NetherlandsGoogle Scholar
  24. Caldwell DE, Caldwell SJ, Laycock PJ (1976) Thermothrix thiopara gen. et sp. nov. A facultatively anaerobic facultative chemolithotroph living at neutral pH and high temperature. Can J Microbiol 22:1509–1517PubMedCrossRefGoogle Scholar
  25. Caldwell DE, Brannan DK, Kieft TL (1983) Thermothrix thiopara: selection and adaption of a filamentous sulfur-oxidizing bacterium colonizing hot spring tufa at pH 7.0 and 74 C., vol 35. Environmental Geochemistry Ecological Bulletin, Stockholm, pp 129–134Google Scholar
  26. Cavanaugh CM (1983a) Chemoautotrophic bacteria in marine invertebrates from sulfide-rich habitats: a new symbiosis. In: Schenk HEA, Schwemmler W (eds) Endocytobiology. Walter de Gruyter, Berlin/New York, pp 699–708Google Scholar
  27. Cavanaugh CM (1983b) Symbiotic chemoautotrophic bacteria in marine invertebrates from sulphide-rich habitats. Nature 302:58–61CrossRefGoogle Scholar
  28. Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB (1981) Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila. Science 213:340–342PubMedCrossRefGoogle Scholar
  29. Chun J, Lee J-H, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon 2007: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261PubMedCrossRefGoogle Scholar
  30. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–145PubMedCrossRefGoogle Scholar
  31. Corliss JB, Dymond J, Gordon LI, Edmond JM, van Herzen RP, Ballard RD, Green K, Williams D, Bainbridge A, Crane K, van Andel TH (1979) Submarine thermal springs on the Galapagos Rift. Science 203:1073–1083PubMedCrossRefGoogle Scholar
  32. Dando PR, Southward AJ (1986) Chemoautotrophy in bivalve molluscs of the genus Thyasira. J Marine Biol Assoc 66:915–929CrossRefGoogle Scholar
  33. Dattagupta S, Schaperdoth I, Montanari A, Mariani S, Kita N, Valley JW, Macalday JL (2009) A novel symbiosis between chemoautotrophic bacteria and a freshwater cave amphipod. The ISME J 3:935–943CrossRefGoogle Scholar
  34. de Beer D, Sauter E, Niemann H, Kaul N, Foucher J-P, Witte U, Schlüter M, Boetius A (2006) In situ fluxes and zonation of microbial activity in surface sediments of the Håkon Mosby mud volcano. Limnol Oceanogr 51:1315–1331CrossRefGoogle Scholar
  35. de Bruyn JC, Boogerd FC, Bos P, Kuenen JG (1990) Floating filter, a novel method for the isolation and enumeration of acidophilic, thermophilic and other fastidious organisms. Appl Environ Microbiol 56:2891–2894PubMedGoogle Scholar
  36. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072PubMedCrossRefGoogle Scholar
  37. Dubinina GA, Grabovich MY (1984) Isolation, cultivation and characterization of Macromonas bipunctata. Mikrobiologiya 53:748–755Google Scholar
  38. Dubinina GA, Grabovich MY, Churikova VV, Lysenko AM, Chernych NA (1993) Reevaluation of the taxonomic status of the colorless sulphur spirilla belonging to the genus Thiospira and description of new species Aquaspirillum bipunctata comb. nov. Microbiology 62:1101–1112Google Scholar
  39. Ehrlich H, Brierley C (eds) (1990) Microbial metal recovery. McGraw Hill, New YorkGoogle Scholar
  40. Felbeck H (1981) Chemoautotrophic potentials of the hydrothermal vent tube worm, Riftia pachyptila (Ventimentifera). Science 213:336–338PubMedCrossRefGoogle Scholar
  41. Felbeck H, Childress JJ, Somero GN (1981) Calvin-Benson cycle and sulphide oxidation enzymes in animals from sulphide-rich habitats. Nature 293:291–293CrossRefGoogle Scholar
  42. Felsenstein J (2004) Inferring phylogenies. Sinauer, SunderlandGoogle Scholar
  43. Friedrich CG, Mitrenga G (1981) Oxidation of thiosulphate by Paracoccus denitrificans and other hydrogen bacteria. FEMS Microbiol Lett 10:209–212CrossRefGoogle Scholar
  44. Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, Stackebrandt E, van der Peer Y, VanDamme P, Thompson FL, Swings J (2005) Re-evaluating prokaryotic species. Nat Rev Microbiol 3:733–739PubMedCrossRefGoogle Scholar
  45. Glaubitz S, Lueders T, Abraham W-R, Jost G, Jürgens K, Labrenz M (2009) 13C-isotope analyses reveal that chemolithoautotrophic Gamma- and Epsilon proteobacteria feed a microbial food web in a pelagic redoxcline of the central Baltic Sea. Environ Microbiol 11:326–337PubMedCrossRefGoogle Scholar
  46. Golovacheva RS, Val’ekho-Roman KM, Troitskii AV (1995) Sulfurococcus mirabilis gen. nov., sp. nov., a new thermophilic archaebacterium with the ability to oxidize sulfur. Mikrobiologiya 56:100–107Google Scholar
  47. Gommers PJF (1988) Microbiological oxidation of sulfide and acetate in a denitrifying uidized bed reactor. PhD Thesis, Delft University of Technology, HollandGoogle Scholar
  48. Gommers PJF, Kuenen JG (1988) Thiobacillus strain Q, a chemolithoheterotrophic sulphur bacterium. Arch Microbiol 150:117–125CrossRefGoogle Scholar
  49. Gommers PJF, Bijleveld W, Kuenen JG (1988a) Simultaneous sulfide and acetate oxidation in a denitrifying fluidized bed reactor. I. Start up and reactor performance. Water Res 22:1075–1083CrossRefGoogle Scholar
  50. Gommers PJF, Bijleveld W, Zuiderwijk FJM, Kuenen JG (1988b) Simultaneous sulfide and acetate oxidation in a denitrifying fluidized bed reactor: measurements of activities and conversions. Water Res 22:1085–1092CrossRefGoogle Scholar
  51. Gottschal GC, Kuenen JG (1980) Selective enrichment of facultatively chemolithotrophic Thiobacilli and related organisms in continuous culture. FEMS Microbiol Lett 7:241–247CrossRefGoogle Scholar
  52. Gottschal JC, Thingstad TF (1982) Mathematical description of competition between two and three bacterial species under dual substrate limitation in the chemostat. Biotechnol Bioeng 24:1403–1418PubMedCrossRefGoogle Scholar
  53. Gottschal JC, de Vries S, Kuenen JG (1979) Competition between the facultatively chemolithotrophic Thiobacillus A2, an obligately chemolithotrophic Thiobacillus and a heterotrophic spirillum for inorganic and organic substrates. Arch Microbiol 121:241–249CrossRefGoogle Scholar
  54. Gottschal GC, Nanninga HJ, Kuenen JG (1981) Growth of Thiobacillus A2 under alternating growth conditions in the chemostat. J Gen Microbiol 126:85–96Google Scholar
  55. Goubem M, Andriamihaja M, Nübel T, Blachier F, Bouillaud F (2007) Sulfide, the first inorganic substrate for human cells. FASEB J 21:1699–1706CrossRefGoogle Scholar
  56. Grote J, Labrenz M, Pfeiffer B, Jost G, Jürgens K (2007) Quantitative distributions of Epsilonproteobacteria and a Sulfurimonas subgroup in pelagic redoxclines of the central Baltic Sea. Appl Environ Microbiol 73:7155–7161PubMedCrossRefGoogle Scholar
  57. Grote J, Jost G, Labrenz M, Herndl GJ, Jürgens 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 74:7546–7551PubMedCrossRefGoogle Scholar
  58. Harrison AP (1984) The acidophilic Thiobacilli and other acidophilic bacteria that share their habitat. Annu Rev Microbiol 38:265–292PubMedCrossRefGoogle Scholar
  59. Harrison AP (1989) The genus Acidiphilium. In: Staley J (ed) Bergey’s manual of systematic bacteriology, vol 3. Williams and Wilkins, Baltimore, pp 1863–1868Google Scholar
  60. Hazeu W, Bijleveld W, Grotenhuis JTC, Kakes E, Kuenen JG (1986) Kinetics and energetics of reduced sulfur oxidation by chemostat cultures of Thiobacillus ferrooxidans. Antonie Van Leeuwenhoek 52:507–518PubMedCrossRefGoogle Scholar
  61. Hazeu W, Batenburg-van der Vegte WH, Bos P, van der Pas RK, Kuenen JG (1988) The production and utilization of intermediary elemental sulfur during the oxidation of reduced sulfur compounds by Thiobacillus ferrooxidans. Arch Microbiol 150:574–579CrossRefGoogle Scholar
  62. Hinck S, Neu TR, Lavik G, Mussmann D, de Beer D, Jonkers HM (2007) Physiological adaptation of a nitrate-storing Beggiatoa sp. to diel cycling in a phototrophic hypersaline mat. Appl Environ Microbiol 73:7013–7022PubMedCrossRefGoogle Scholar
  63. Hinze G (1913) Beitrage zur Kenntnis der farblosen Schwefelbakterien. Berichte der Deutschen Botanischen Gesellschaft 31:189–202Google Scholar
  64. Hirayama H, Takai K, Inagaki F, Nealson KH, Horikoshi K (2005) Thiobacter subterraneus gen. nov., sp. nov., an obligately chemolithoautotrophic, thermophilic, sulfur-oxidizing bacterium from a subsurface hot aquifer. Int J Syst Evol Microbiol 55:467–472PubMedCrossRefGoogle Scholar
  65. Høgslund S, Revsbech NP, Kuenen JG, Jørgensen BB, Gallardo VA, van de Vossenberg J, Nielsen JL, Holmkvist L, Arning ET, Nielsen LP (2009) Physiology and behaviour of marine Thioploca. ISME J 3:647–657PubMedCrossRefGoogle Scholar
  66. Hubert CRJ, Oldenburg TBP, Fustic M, Gray ND, Larter SR, Penn K, Rowan AK, Seshadri R, Perry A, Swainsbury R, Boordouw G, Voordouw JK, Head IM (2011) Massive dominance of Epsilonproteobacteria in formation waters from a Canadian oil sands reservoir containing severely biodegraded oil. Environ Microbiol. Published online.8 AUG 2011 doi: 10.1111/j.1462-2920.2011.02521.xGoogle Scholar
  67. Hutchinson M, Johnstone KI, White D (1969) Taxonomy of the genus Thiobacillus: the outcome of numerical taxonomy applied to the group as a whole. J Gen Microbiol 57:397–410PubMedCrossRefGoogle Scholar
  68. Inagaki F, Takai K, Kobayashi H, Nealson KH, Horikoshi K (2003) Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing eproteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. International Journal of Systemic and Evolutionary Microbiology 53:1801–1805CrossRefGoogle Scholar
  69. Inagaki F, Takai K, Nealson KH, Horikoshi K (2004) Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the e-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. Int J Syst Evol Microbiol 54:1477–1482PubMedCrossRefGoogle Scholar
  70. Ishaque M, Aleem MIH (1973) Intermediates of denitrification in the chemo-autotroph Thiobacillus denitrificans. Arch Microbiol 94:269–282Google Scholar
  71. Ito T, Sugita K, Yumoto I, Nodasaka Y, Okabe YS (2005) Thiovirga sulfuroxydans gen nov sp. nov. a chemolithotrophic sulfur-oxidizing bacterium isolated from a microaerobic waste-water biofilm. Int J Syst Evol Microbiol 55:1059–1064PubMedCrossRefGoogle Scholar
  72. Jannasch HW (1985) The chemosynthetic support of life and the microbial diversity at deep sea hydrothermal vents. Proc Roy Soc Lond B225:277–297CrossRefGoogle Scholar
  73. Jannasch HW (1988) Chemosynthetically sustained ecosystems in the deep sea. In: Schlegel HG, Bowien B (eds) Autotrophic bacteria. Science Tech, Madison, pp 45–65Google Scholar
  74. Jannasch HW, Wirsen CO, Nelson DC, Robertson LA (1985) Thiomicrospira crunogena sp. nov., a colorless sulfur-oxidizing bacterium from a deep-sea hydrothermal vent. Int J Syst Bacteriol 35:422–424CrossRefGoogle Scholar
  75. Janssen AJH, Lens PNL, Stams AJM, Plugge CM, Sorokin DY, Muyzer G, Dijkman H, van Zessen E, Luimes P, Buisman CJN (2009) Application of bacteria involved in the biological sulfur cycle for paper mill effluent purification. Sci Total Environ 407:1333–1343PubMedCrossRefGoogle Scholar
  76. Jensen J, Revsbech NP (1989) Photosynthesis and respiration of a diatom biofilm cultures in a new gradient growth chamber. FEMS Microbiol Ecol 62:29–38CrossRefGoogle Scholar
  77. Johnson DB, Joulian C, d’Hugues P, Hallberg KB (2008) Sulfobacillus benefaciens sp. nov., an acidophilic facultative anaerobic Firmicute isolated from mineral bioleaching operations. Extremophiles 12:789–798PubMedCrossRefGoogle Scholar
  78. Jørgensen BB (1982) Ecology of the bacteria of the sulphur cycle with special reference to anoxic-oxic interface environments. Philoso Trans Roy Soc Lond Ser B 298:543–561CrossRefGoogle Scholar
  79. Jørgensen BB (1988) Biogeochemistry of chemoautotrophic bacteria. In: Schlegel HG, Bowien B (eds) Autotrophic bacteria. Science Tech, Madison, pp 117–146Google Scholar
  80. Jørgensen BB (2010) Big sulfur bacteria. ISME J 4:1083–1084PubMedCrossRefGoogle Scholar
  81. Jørgensen BB, Caldwell DC (2004) Sulfide oxidation in marine sediments: geochemistry meets microbiology. Geological Society of America Special papers, vol 379, pp 63–81Google Scholar
  82. Jørgensen BB, Des Marais DJ (1986) Competition for sulfide among colorless and purple sulfur bacteria in cyanobacterial mats. FEMS Microbiol Ecol 38:79–186CrossRefGoogle Scholar
  83. Jørgensen BB, Kuenen JG, Cohen Y (1979) Microbial transformations of sulfur compounds in a stratified lake (Solar Lake, Sinai). Limnol Oceanogr 24:799–822CrossRefGoogle Scholar
  84. Kamp A, Stief P, Schulz-Vogt HN (2006) Anaerobic sulfide oxidation with nitrate by a freshwater Beggiatoa enrichment culture. Appl Environ Microbiol 72:4755–4760PubMedCrossRefGoogle Scholar
  85. Kämpher P, Glaeser SP (2012) Prokaryotic taxonomy in the sequencing era and the role of MLSA in classification. Microbiology (Australia) 14:291–317Google Scholar
  86. Kanagawa T, Kelly DP (1986) Breakdown of dimethyl sulphide by mixed cultures and by Thiobacillus thioparus. FEMS Microbiol Lett 34:13–19Google Scholar
  87. Kanagawa T, Mikami E (1989) Removal of methanethiol, dimethyl sulfide, dimethyl disulfide, and hydrogen sulfide from contaminated air by Thiobacillus thioparus TK-m. Appl Environ Microbiol 55:555–558PubMedGoogle Scholar
  88. Katayama-Fujimura Y, Tsuzaki N, Kuraishi H (1982) Ubiquinone, fatty acid and DNA base composition determination as a guide to the taxonomy of the genus Thiobacillus. J Gen Microbiol 128:1599–1611Google Scholar
  89. Katayama-Fujimura Y, Kawashima I, Tsuzaki N, Kuraishi H (1984) Physiological characteristics of the facultatively chemolithotrophic Thiobacillus species Thiobacillus delicatus nom. rev., emend., Thiobacillus perometabolis and Thiobacillus intermedius. Int J Syst Bacteriol 34:139–144CrossRefGoogle Scholar
  90. Kelly DP (1988a) Oxidation of sulphur compounds. Society for General Microbiology Symposium, vol 42, pp 65–98Google Scholar
  91. Kelly DP (1988b) Physiology and biochemistry of unicellular sulfur bacteria. In: Schlegel HG, Bowien B (eds) Autotrophic bacteria. Science Tech, Madison, pp 193–218Google Scholar
  92. Kelly DP, Harrison AP (1989) The genus Thiobacillus. In: Staley J (ed) Bergey’s manual of systematic bacteriology, vol 3. Williams and Wilkins, Baltimore, pp 1842–1858Google Scholar
  93. Kelly DP, Kuenen JG (1984) Ecology of the colourless sulphur bacteria. In: Codd GA (ed) Aspects of microbial metabolism and ecology. Academic, London, pp 211–240Google Scholar
  94. Kelly DP, Tuovinen OH (1972) Recommendation that the names Ferrobacillus ferrooxidans Leathen and Braley and Ferrobacillus sulfooxidans Kinsel be recognised as synonyms of Thiobacillus ferrooxidans Temple and Colmer. Int J Syst Bacteriol 22:170–172CrossRefGoogle Scholar
  95. 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 Bacteriol 50:511–516Google Scholar
  96. Kelly DP, Wood AP, Stackebrandt E (2005) Thiobacillus. In: Brenner DJ, Krieg NR, Staley J (eds) Bergey’s manual of systematic bacteriology, vol 2. Springer, New York, pp 764–770CrossRefGoogle Scholar
  97. Kimura M (1980) A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  98. Kluyver AJ, van Niel CB (1936) Prospects for a natural system of classification of bacteria. Zentralblad Bakteriol Abt II 94:369–402Google Scholar
  99. Kock D, Schippers A (2008) Quantitative microbial community analysis of three different sulfidic mine tailing dumps generating acid mine drainage. Appl Environ Microbiol 74:5211–5219PubMedCrossRefGoogle Scholar
  100. Kodama T, 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 54:2297–2300PubMedCrossRefGoogle Scholar
  101. Kojima H, Fukui M (2010) Sulfuricella denitrificans gen. nov. sp., nov., a sulfur-oxidizing autotroph isolated from a freshwater lake. Int J Syst Evol Microbiol 60:2862–2866PubMedCrossRefGoogle Scholar
  102. Kojima H, Fukui M (2011) Sulfuritalea hydrogenivorans gen. nov., sp. nov., a facultative autotroph isolated from a freshwater lake. Int J Syst Evol Microbiol 61:1651–1656PubMedCrossRefGoogle Scholar
  103. König H, Stetter KO (1989) Archaebacteria. In: Staley J (ed) Bergey’s manual of systematic bacteriology, vol 3. Williams and Wilkins, Baltimore, pp 2171–2173Google Scholar
  104. Kovaleva OL, Tourova TP, Muyzer G, Kolganova TV, Sorokin DY (2011) Diversity of RuBisCO and ATP citrate lyase genes in soda lake sediments. FEMS Microbiol Ecol 75:37–47PubMedCrossRefGoogle Scholar
  105. Kuenen JG (1975) Colorless sulfur bacteria and the sulfur cycle. Plant Soil 43:49–76CrossRefGoogle Scholar
  106. Kuenen JG (1989) The colorless sulfur bacteria. In: Staley J (ed) Bergey’s manual of systematic bacteriology, vol 3. Williams and Wilkins, Baltimore, pp 1834–1837Google Scholar
  107. Kuenen JG, Beudeker RF (1982) Microbiology of thiobacilli and other sulphur-oxidizing autotrophs, mixotrophs and heterotrophs. Philos Trans Roy Soc Lond Ser B 298:473–497CrossRefGoogle Scholar
  108. Kuenen JG, Bos P (1988) Habitats and ecological niches of chemolitho(auto)trophic bacteria. In: Schlegel HG, Bowien B (eds) Autotrophic bacteria. Science Tech, Madison, pp 53–80Google Scholar
  109. Kuenen JG, Robertson LA (1989a) The genus Thiomicrospira. In: Staley J (ed) Bergey’s manual of systematic bacteriology, vol 3. Williams and Wilkins, Baltimore, pp 1858–1861Google Scholar
  110. Kuenen JG, Robertson LA (1989b) The genus Thiosphaera. In: Staley J (ed) Bergey’s manual of systematic bacteriology, vol 3. Williams and Wilkins, Baltimore, pp 1861–1862Google Scholar
  111. Kuenen JG, Veldkamp H (1972) Thiomicrospira pelophila, gen. nov., sp. nov., a new obligately chemolithotrophic colourless sulfur bacterium. Antonie van Leeuwenhoek J Microbiol Serol 38:241–256CrossRefGoogle Scholar
  112. Kuenen JG, Veldkamp H (1973) Effects of organic compounds on growth of chemostat cultures of Thiomicrospira pelophila, Thiobacillus thioparus and Thiobacillus neapolitanus. Arch Microbiol 94:173–190Google Scholar
  113. Kuenen JG, Boonstra J, Schroder HGJ, Veldkamp H (1977) Competition for inorganic substrates among chemoorganotrophic and chemolithotrophic bacteria. Microb Ecol 3:119–130CrossRefGoogle Scholar
  114. Kuenen JG, Robertson LA, van Gemerden H (1985) Microbial interactions among aerobic and anaerobic sulphur oxidizing bacteria. Adv Microb Ecol 8:1–59CrossRefGoogle Scholar
  115. Kurosawa N, Itoh YH, Iwai T, Sugai A, Uda I, Kimura N, Horiuchi T, Itoh T (1998) Sulfurisphaera ohwakuensis gen. nov., sp. nov., a novel extremely thermophilic acidophile of the order Sulfolobales. Int J Syst Evol Microbiol 48:451–456Google Scholar
  116. Kutzing FT (1833) Beitrag zur Kenntnis über die Entstehung und Metamorphose der niedern vegetabilischen Organismen, nebst einer systematischen Zusammenstellung der hierher gehörigen niedern Algenformen. Linnaea 8:335–387Google Scholar
  117. Lane DJ, Stahl DA, Olsen GJ, Heller DJ, Pace NR (1985) Phylogenetic analysis of the genera Thiobacillus and Thiomicrospira by 5S rRNA sequences. J Bacteriol 163:75–81PubMedGoogle Scholar
  118. Lane DJ, Harrison AP, Stahl D, Pace B, Giovannoni SJ, Olsen GJ, Pace NR (1992) Evolutionary relationships among sulfur and iron oxidizing eubacteria. J Bacteriol 174:269–278PubMedGoogle Scholar
  119. Lanzén A, Jørgensen SL, Bengtsson MM, Jonassen I, Øvreas L, Urich T (2011) Exploring the composition and diversity of microbial communities at the Jan Mayen hydrothermal vent field using RNA and DNA. FEMS Microbiol Ecol 77:577–589PubMedCrossRefGoogle Scholar
  120. Larkin JM, Strohl WR (1983) Beggiatoa, Thiothrix, and Thioploca. Annu Rev Microbiol 37:341–367PubMedCrossRefGoogle Scholar
  121. Lauterborn R (1907) Eine neue Gattung der Schwefelbakterien Thioploca schmidlei nov. gen. nov. spec.. Berichte der Deutschen Botanischen Gesellschaft 25:238–242Google Scholar
  122. Le Roux NW, Wakerly DS, Hunt SD (1977) Thermophilic thiobacillus-type bacteria from Icelandic thermal areas. J Gen Microbiol 100:197–201CrossRefGoogle Scholar
  123. Liu C-Q, Plumb J, Hendry P (2006) Rapid specific detection and quantification of Bacteria and Archaea involved in mineral sulphide bioleaching using real time PCR. Wiley Interscience, New YorkGoogle Scholar
  124. Liu Y-G, Zhou M, Zeng G-M, Wang X, Li X, Fan T, Xu W-H (2008) Bioleaching of heavy metals from mine tailings by indigenous sulfur-oxidizing bacteria: effects of substrate concentration. Bioresour Technol 99:4124–4129PubMedCrossRefGoogle Scholar
  125. Lloyd KG, Albert DB, Biddle JF, Chanton JP, Pizarro O, Teske A (2010) Spatial structure and activity of sedimentary microbial communities underlying a Beggiatoa spp. Mat in a Gulf of Mexico hydrocarbon seep. PLoS One 5(1):e8738PubMedCrossRefGoogle Scholar
  126. Ludwich 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, Lüssman R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Research 32:1363–1371Google Scholar
  127. Lundgren DG, Andersen KJ, Penson CC, Mahony RP (1964) Culture structure and physiology of the chemoautotroph Ferrobacillus ferrooxidans. J Gen Microbiol 105:215–218Google Scholar
  128. Maestre JP, Rovira R, Alvarez-Hornos FJ, Fortuny M, Lafuente J, Gamisans X, Gabriel D (2010) Bacterial community analysis of a gas-phase biotrickling filter for biogas mimics desulfurization through the rRNA approach. Chemosphere 80:872–880PubMedCrossRefGoogle Scholar
  129. Martinez-Garcia M, Swan BK, Poulton NJ, Lluesma Gomez M, Masland D, Sieracki ME, Stephanauskas R (2012) High-throughput single-cell sequencing identifies photoheterotrophs and chemoautotrophs in freshwater bacterioplankton. ISME J 6:113–123PubMedCrossRefGoogle Scholar
  130. Mason J, Kelly DP (1988) Thiosulfate oxidation by obligately heterotrophic bacteria. Microb Ecol 15:123–134CrossRefGoogle Scholar
  131. Matin A (1978) Organic nutrition of chemolithotrophic bacteria. Annu Rev Microbiol 32:433–469PubMedCrossRefGoogle Scholar
  132. Meyer B, Kuever J (2007a) Molecular analysis of the distribution and phylogeny of dissimilatory adenosine-5’-phosphosulfate reductase-encoding genes (aprBA) among sulphur-oxidizing prokaryotes. Microbiology 153:3478–3498PubMedCrossRefGoogle Scholar
  133. Meyer B, Kuever J (2007b) Molecular analysis of the diversity of sulphate reducing and sulphur-oxidizing prokaryotes in the environment, using aprA as a functional marker gene. Appl Environ Microbiol 73:7664–7679PubMedCrossRefGoogle Scholar
  134. Meyer B, Imhoff JF, Kuever J (2007) Molecular analysis of the distribution and phylogeny of the soxB gene among sulphur-oxidizing bacteria – evolution of the Sox sulphur oxidation enzyme system. Environ Microbiol 9:2957–2977PubMedCrossRefGoogle Scholar
  135. Migula W (1894) Ueber ein neues system der bakterien. Arbeiten aus dem Bakteriologischen Institut der Technischen Hochschule zu Karlsruhe 1:235–238Google Scholar
  136. Mori K, Suziki K (2008) Thiofaba tepidiphila gen. nov., sp. nov., a novel obligately chemolithoautotrophic, sulfur-oxidizing bacterium of the Gammaproteobacteria isolated from a hot spring. Int J Syst Evol Microbiol 58:1885–1891PubMedCrossRefGoogle Scholar
  137. Mosser JL, Mosser AG, Brock TD (1973) Bacterial origin of sulfuric acid in geothermal habitats. Science 179:1323–1324PubMedCrossRefGoogle Scholar
  138. Mussmann M, Hu FZ, Richter M et al (2007) Insights into the genome of large sulfur bacteria revealed by analysis of single filaments. PLoS Biol 5:1923–1937CrossRefGoogle Scholar
  139. Muyzer G, de Bruyn AC, Schmedding DJM, Bos P, Westbroek P, Kuenen JG (1987) A combined immuno-fluorescence-DNA-fluorescence staining technique for enumeration of Thiobacillus ferrooxidans in a population of acidophilic bacteria. Appl Environ Microbiol 53:660–664PubMedGoogle Scholar
  140. Nelson DC (1988) Physiology and biochemistry of lamentous sulfur bacteria. In: Schlegel HG, Bowien B (eds) Autotrophic bacteria. Science Tech, Madison, pp 221–238Google Scholar
  141. Nelson DC, Castenholz RW (1981) Use of reduced sulfur compounds by Beggiatoa sp. J Bacteriol 147:140–154PubMedGoogle Scholar
  142. Nelson DC, Jannasch HW (1983) Chemoautotrophic growth of a marine Beggiatoa in sulfide-gradient cultures. Arch Microbiol 136:262–269CrossRefGoogle Scholar
  143. Nelson DC, Wirsen CO, Jannasch HW (1989) Thermophilic Bacillus sp. that shows the denitrification phenotype of Pseudomonas aeruginosa. Appl Environ Microbiol 55:1023–1025Google Scholar
  144. Neufeld JD, Wagner M, Murrell JC (2007) Who eats what, where and when? Isotope-labelling experiments are coming of age. ISME J 1:103–110PubMedCrossRefGoogle Scholar
  145. Nielsen PH, Aquino de Muro M, Nielsen JL (2000) Studies on the in situ physiology of Thiothrix spp. present in activated sludge. Environ Microbiol 2:389–398PubMedCrossRefGoogle Scholar
  146. Nielsen JL, Christensen D, Kloppenborg M, Nielsen PH (2003) Quantification of cell-specific substrate uptake by probe-defined bacteria under in situ conditions by microautoradiography and fluorescence in situ hybridization. Environ Microbiol 5:202–211PubMedCrossRefGoogle Scholar
  147. Okabe S, Odagiri M, Ito T, Satoh H (2007) Succession of sulphur-oxidizing bacteria in the microbial community on corroding concrete in sewer systems. Appl Environ Microbiol 73:971–980PubMedCrossRefGoogle Scholar
  148. Pagani I, Liolios K, Jansson J, Chen I-MA, Smirnova T, Nosrat B, Markowith VM, Kyrpides NC (2012) The genome online database (GOLD) v. 4: status of genomic and metagenomic projects and their associated metadata. Nucl Acids Res 40:D571–D579PubMedCrossRefGoogle Scholar
  149. Pathak A, Dastidar MG, Sreekrishnan TR (2009) Bioleaching of heavy metals from sewage sludge: a review. J Environ Manage 90:2343–2353PubMedCrossRefGoogle Scholar
  150. Preisler A, de Beer D, Lichtenschlag A, Lavik G, Boetius A, Jørgensen BB (2007) Biological and chemical oxidation in a Beggiatoa inhabited marine sediment. ISME J 1:341–353PubMedGoogle Scholar
  151. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196PubMedCrossRefGoogle Scholar
  152. Reigstad LJ, Jorgensen SL, Lauritzen S-E, Schleper C, Urich T (2011) Sulfur-oxidizing chemolithotrophic Proteobacteria dominate the microbiota in high arctic thermal springs on Svalbard. Astrobiology 11:665–678PubMedCrossRefGoogle Scholar
  153. Reno ML, Held NL, Fields CJ, Burke PV, Whitaker RJ (2009) Biogeography of the Sulfolobus islandicus pan-genome. Proc Nat Acad Sci USA 106:8605–8610PubMedCrossRefGoogle Scholar
  154. Revsbech NP, Jørgensen BB (1986) Microelectrodes: their use in microbial ecology. Adv Microb Ecol 9:293–352Google Scholar
  155. Revsbech NP, Ward DM (1984) Microelectrode studies of interstitial water chemistry and photosynthetic activity in a hot spring microbial mat. Appl Environ Microbiol 48:270–275PubMedGoogle Scholar
  156. Revsbech NP, Madsen B, Jørgensen BB (1986) Oxygen production and consumption in sediments determined at high spatial resolution by computer simulation of oxygen microelectrode data. 1986. Limnol Oceanogr 31:293–304CrossRefGoogle Scholar
  157. Robertson LA, Kuenen JG (1983a) Anaerobic and aerobic denitrification by sulphide oxidizing bacteria from waste water. In: van den Brink WJ (ed) Anaerobic waste water treatment. TNO Corporate Communication Department, The Hague, pp 3–12Google Scholar
  158. Robertson LA, Kuenen JG (1983b) Thiosphaera pantotropha gen. nov. sp. nov., a facultatively anaerobic, facultatively autotrophic sulphur bacterium. J Gen Microbiol 129:2847–2855Google Scholar
  159. Robertson LA, Cornelisse R, Zeng R, Kuenen JG (1989) The effect of thiosulphate and other inhibitors of autotrophic nitrification on heterotrophic nitrifiers. Antonie Van Leeuwenhoek 56:301–309PubMedCrossRefGoogle Scholar
  160. Ruby EG, Jannasch HW (1982) Physiological characteristics of Thiomicrospira sp. L-12 isolated from deep sea hydrothermal vents. J Bacteriol 149:161–165PubMedGoogle Scholar
  161. Ruby EG, Wirsen CO, Jannasch HW (1981) Chemolithotrophic sulfur-oxidizing bacteria from the Galapagos Rift hydrothermal vents. Appl Environ Microbiol 42:317–324PubMedGoogle Scholar
  162. Saitou N, Nei M (1988) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  163. Salman V, Amann R, Girnth A-C, Polerecky L, Bailey JV, Høslund S, Jessen G, Pantoja S, Schulz-Vogt HN (2011) A single-cell sequencing approach to the classification of large vacuolated sulphur bacteria. Syst Appl Microbiol 34:243–259PubMedCrossRefGoogle Scholar
  164. Schlegel HG (1981) Allgemeine mikrobiologie. Thieme Verlag, StuttgartGoogle Scholar
  165. Schmidt TM, Arieli B, Cohen Y, Padan E, Strohl WR (1987) Sulfur metabolism in Beggiatoa alba. J Bacteriol 169:5466–5472PubMedGoogle Scholar
  166. Schulz HN, Brinkhoff T, Ferdelman TG, Marine MH, Teske A, Jørgensen BB (1999) Dense populations of a giant sulfur bacterium in Namibian shelf sediments. Science 284:493–495PubMedCrossRefGoogle Scholar
  167. Searcy DG (2006) Rapid hydrogen sulfide consumption by Tetrahymena pyriformis and its implications for the origin of mitochondria. Eur J Protistol 42:221–231PubMedCrossRefGoogle Scholar
  168. Segerer A, Stetter KO (1989) The genus Acidianus. In: Staley J (ed) Bergey’s manual of systematic bacteriology, vol 3. Williams and Wilkins, Baltimore, pp 2251–2253Google Scholar
  169. Seidel H, Wennrich R, Hoffmann P, Loser C (2006) Effect of different types of elemental sulfur on bioleaching of heavy metals from contaminated sediments. Chemosphere 62:1444–1453PubMedCrossRefGoogle Scholar
  170. Shafia F, Wilkinson RF (1969) Growth of Ferrobacillus ferrooxidans on organic matter. J Bacteriol 97:251–260Google Scholar
  171. Siggins A, Gunnigle E, Abram F (2012) Exploring mixed microbial community functioning: recent advances in metaproteomics. FEMS Microbiol Ecol. doi:10.1111/j.1574-6941.2011.01284.xGoogle Scholar
  172. Smith DW, Finazzo SF (1981) Salinity requirements of a marine Thiobacillus intermedius. Arch Microbiol 129:199–203CrossRefGoogle Scholar
  173. Smith AL, Kelly DP (1979) Competition in the chemostat between an obligately and a facultatively chemolithotrophic Thiobacillus. J Gen Microbiol 115:377–384CrossRefGoogle Scholar
  174. Smith NA, Kelly DP (1988a) Isolation and physiological characterization of autotrophic sulphur bacteria oxidizing dimethyl disulphide as sole source of energy. J Gen Microbiol 134:1407–1417Google Scholar
  175. Smith NA, Kelly DP (1988b) Mechanism of oxidation of dimethyl disulphide by Thiobacillus thioparus strain E6. J Gen Microbiol 134:3031–3039Google Scholar
  176. Smith NA, Kelly DP (1988c) Oxidation of carbon disulphide as the sole source of energy for the autotrophic growth of Thiobacillus thioparus strain TK-m. J Gen Microbiol 134:3041–3048Google Scholar
  177. Smith CR, Kukert H, Wheatcroft RA, Jumars PA, Deming JW (1989) Vent fauna on whale remains. Nature 341:27–28CrossRefGoogle Scholar
  178. Sorokin YI (1970) Interrelations between sulphur and carbon turnover in meromictic lakes. Arch Hydrobiol 66:391–446Google Scholar
  179. Sorokin YI (1972) The bacterial population and the process of hydrogen sulphide oxidation in the Black Sea. Journal du Conseil International pour l'Éxploration de la Mer 34:432–455Google Scholar
  180. Sorokin D-YU (1992) Catenococcus thiocyclus gen. nov., sp. nov. - a new facultatively anaerobic bacterium from a near-shore sulphidic hydrothermal area. J Gen Microbiol 138:2287–2292CrossRefGoogle Scholar
  181. Sorokin DY, Robertson LA, Kuenen JG (1996) Sulfur-cycling in Catenococcus thiocyclus. FEMS Microbiol Ecol 19:117–126CrossRefGoogle Scholar
  182. Sorokin DY, Lysenko AM, Mityushina LL, Tourova TP, Jones BE, Rainey FA, Robertson LA, Kuenen JG (2001) 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 51:565–580PubMedGoogle Scholar
  183. 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 52:2175–2182PubMedCrossRefGoogle Scholar
  184. Sorokin DY, Tourova TP, Spiridonova EM, Rainney FA, Muyzer G (2005) Thioclava pacifica gen. nov., sp. nov., a novel facultatively autotrophic, marine, sulphur-oxidizing bacterium from a near-shore sulfidic hydrothermal area. Int J Syst Evol Microbiol 55:1069–1075PubMedCrossRefGoogle Scholar
  185. Sorokin DY, Tourova TP, Braker G, Muyzer G (2007) 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 57:1582–1589PubMedCrossRefGoogle Scholar
  186. 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 58:2890–2897PubMedCrossRefGoogle Scholar
  187. Sorokin DY, Kovaleva OL, Tourova TP, Muyzer G (2010) Thiohalobacter thiocyanaticus gen. nov., sp. nov., a moderately halophilic, sulfur-oxidizing gammaproteobacterium from hypersaline lakes, that utilizes thiocyanate. Int J Syst Evol Microbiol 60:444–450PubMedCrossRefGoogle Scholar
  188. Southward EC (1986) Gill symbionts in thyasirids and other bivalve molluscs. J Marine Biol Assoc 66:899–914Google Scholar
  189. Stackebrande E, Murray RGE, Truper HG (1988) Proteobacter classis nov., a name for the phylogenetic taxon that includes the “Purple bacteria and their relatives”. Int J Syst Bact 38:321–325CrossRefGoogle Scholar
  190. Stahl DA, Lane DL, Olsen GJ, Heller DJ, Schmidt TM, Pace NR (1987) A phylogenetic analysis of certain sulfide oxidizing and related morphologically conspicuous bacteria by 5S ribosomal RNA sequences. Int J Syst Bacteriol 37:116–122CrossRefGoogle Scholar
  191. Stefess GC, Kuenen JG (1989) Factors in sequencing elemental sulphur production from sulphide or thiosulphate by autotrophic thiobacilli. Forum Mikrobiologie 12:92Google Scholar
  192. Stetter KO (1988) Extremely thermophilic chemolithoautotrophic archaebacteria. In: Schlegel HG, Bowien B (eds) Autotrophic bacteria. Science Tech, Madison, pp 167–176Google Scholar
  193. Steward FJ, Ulloa O, DeLong EF (2012) Microbial metatranscriptomics in a permanent marine oxygen minimum zone. Environ Microbiol 14:23–40CrossRefGoogle Scholar
  194. Sublette KL, Sylvester ND (1987) Oxidation of hydrogen sulfide by Thiobacillus denitrificans: desulfurization of natural gas. Biotechnol Bioeng 29:249–257PubMedCrossRefGoogle Scholar
  195. Sugio T, Domatsu C, Munaka O, Tano T, Imai K (1985) Role of a ferric iron reducing system in sulfur oxidation of Thiobacillus ferrooxidans. Appl Environ Microbiol 49:1401–1406PubMedGoogle Scholar
  196. Suylen GMBH, Kuenen JG (1986) Chemostat enrichment and isolation of Hyphomicrobium EG, a dimethyl sulphide oxidizing methylotroph and reevaluation of Thiobacillus MS1. Antonie Van Leeuwenhoek 52:281–293PubMedCrossRefGoogle Scholar
  197. Suylen GMBH, Stefess GC, Kuenen JG (1986) Chemolithotrophic potential of a Hyphomicrobium species capable of growth on methylated sulphur compounds. Arch Microbiol 146:192–198CrossRefGoogle Scholar
  198. Sweerts JPRA, de Beer D, Nielsen LP, Verdouw H, van den Heuvel JC, Cohen Y, Cappenberg TE (1990) Denitrification by sulphur oxidizing Beggiatoa spp. mats on freshwater sediments. Nature 344:762–763CrossRefGoogle Scholar
  199. Takai K, Kobayashi H, Nealson KH, Horikoshi K (2003) Sulfurihydrogenibium subterraneum gen. nov., sp. nov., from a subsurface hot aquifer. Int J Syst Evol Microbiol 53:823–827PubMedCrossRefGoogle Scholar
  200. Takai K, Miyazaki M, Nunoura T, Hirayama H, Oida H, Furushima Y, Yamamoto H, Horikoshi K (2006) Sulfurivirga caldicuralii gen. nov. sp. nov. a novel microaerobic, thermophilic, thiosulfate-oxidising chemolithoautotroph, isolated from a shallow marine hydrothermal system occurring n a coral reef, Japan. Int J Syst Evol Microbiol 56:1921–1929PubMedCrossRefGoogle Scholar
  201. Takai K, Miyazaki M, Hirayama H, Nakagawa S, Querellou J, Godfroy A (2009) Isolation and physiological characterization of two novel, piezophilic, thermophilic chemolithoautotrophs from a deep-sea hydrothermal vent chimney. Environ Microbiol 11:1983–1997PubMedCrossRefGoogle Scholar
  202. Tanji Y, Kanagawa T, Mikami E (1989) Removal of dimethyl sulfide, methyl mercaptan and hydrogen sulphide by immobilized Thiobacillus thioparus TK-m. J Ferment Bioengin 67(280):285Google Scholar
  203. Taylor BF, Hoare DS (1969) New facultative Thiobacillus and a reevaluation of the heterotrophic potential of Thiobacillus novellus. J Bacteriol 100:487–497PubMedGoogle Scholar
  204. Timmer ten Hoor A (1975) A new type of thiosulphate oxidizing, nitrate reducing microorganism: Thiomicrospira denitrificans sp. nov. J Sea Res 9:343–351, NetherlandsGoogle Scholar
  205. Timmer ten Hoor A (1977) Denitrificerende kleurloze zwavelbacterien. PhD thesis. University of Groningen, NetherlandsGoogle Scholar
  206. Tourova TP, Spiridonova EM, Berg IA, Kuznetsov BB, Sorokin DYU (2006) Occurrence, phylogeny and evolution of ribulose-1,5-bisphosphate carboxylase/oxygenase in obligately chemolithoautotrophic sulphur-oxidizing bacteria of the genera Thiomicrospira and Thioalkalimicrobium. Microbiology 152:2159–2169PubMedCrossRefGoogle Scholar
  207. Tourova TP, Kovaleva OL, Sorokin DYU, Muyzer G (2010) Ribulose-1,5-biphorphate carboxylase/oxygenase genes as a functional marker for chemolithoautotrophic halophilic sulphur-oxidizing bacteria in hypersaline habitats. Microbiology 156:2016–2025PubMedCrossRefGoogle Scholar
  208. Trevisan V (1842) Prospetto della ora Euganea. Coi Tipi Del Seminario. Padova 1–68Google Scholar
  209. Tringe SG, von Mering C, Kobayashi A, Slamov AA, Chen K, Chang HW, Podar M, Short JM, Mathur EJ, Detter JC, Bork P, Hugenholtz P, Rubin EM (2005) Comparative genomics of microbial communities. Science 308:554–557PubMedCrossRefGoogle Scholar
  210. Tuovinen OH, Kelly DP (1972) Biology of Thiobacillus ferrooxidans in relation to the microbiological leaching of sulphide ores. Z Allg Mikrobiol 12:311–346PubMedCrossRefGoogle Scholar
  211. Tuttle JH, Jannasch HW (1972) Occurrence and types of Thiobacillus-like bacteria in the sea. Limnol Oceanogr 17:532–543CrossRefGoogle Scholar
  212. Tuttle JH, Holmes PE, Jannasch HW (1974) Growth rate stimulation of marine pseudomonads by thiosulfate. Arch Mikrobiol 99:1–14Google Scholar
  213. Tuttle JH, Wirsen CO, Jannasch HW (1983) Microbial activities in the emitted hydrothermal waters of the Galapagos Rift vents. Mar Biol 73:293–299CrossRefGoogle Scholar
  214. Visloukh SM (1914) Spirillum kolkwitzii nov sp Zhurnal Mikrobiologii 1:42–51Google Scholar
  215. Visser JM, Stefess GC, Robertson LA, Kuenen JG (1997) Thiobacillus sp.W5, the dominant autotroph oxidizing sulfide to sulfur in a reactor for aerobic treatment of sulfidic wastes. Antonie Van Leeuwenhoek 72:27–134CrossRefGoogle Scholar
  216. Wendeberg A, Zielinski FU, Borowski C, Dubilier N (2012) Expression patterns of mRNAs for methanotrophy and thiotrophy in symbionts of the hydrothermal vent mussel Bathymodiolus puteoserpentis. ISME J 6:104–112PubMedCrossRefGoogle Scholar
  217. Winogradsky S (1888) Beitrage zur Morphologie und Physiologie der Bakterien. Heft 1. Zur Morphologie und Physiologie der Schwefelbakterien. Arthur Felix Leipzig 1:120Google Scholar
  218. Wirsen CO, Jannasch HW (1978) Physiological and morphological observations on Thiovulum sp. J Bacteriol 136:765–774PubMedGoogle Scholar
  219. Wirsen CO, Tuttle JH, Jannasch HW (1986) Activities of sulfur-oxidizing bacteria at the 21 N East Pacific Rise vent site. Mar Biol 92:449–456CrossRefGoogle Scholar
  220. Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271PubMedGoogle Scholar
  221. Wood AP, Kelly DP (1989) Isolation and physiological characterization of Thiobacillus thyasyris sp. nov., a novel marine facultative autotroph and the putative symbiont of Thyasira flexuosa. Arch Microbiol 152:160–166CrossRefGoogle Scholar
  222. Yamamoto M, Nakagawa S, Shimamura S, Takai K, Horikoshi K (2010) Molecular characterization of inorganic sulphur-compound metabolism in the deep-sea epsilonproteobacterium Sulfurovum sp. NBC37-1. Environ Microbiol 12:1144–1153PubMedCrossRefGoogle Scholar
  223. Yang T, Lyons S, Aguilar C, Cuhel R, Teske A (2011) Microbial communities and chemosynthesis in Yellowstone Lake sublacustrine hydrothermal vent waters. Frontiers Microbiol 2:130Google Scholar
  224. Yarza P, Ludwig W, Euzéby J, Amann R, Schleifer K-H, Oliver Glöckner F, Rosselló-Móra R (2010) Update of the all-species living tree project based on 16S and 23S rRNA sequence analyses. Syst Appl Microbiol 33:291–299PubMedCrossRefGoogle Scholar
  225. Yilmaz S, Singh AK (2011) Single cell genome sequencing. Curr Opin Biotechnol
  226. Zhang CL, Huang Z, Cantu J, Pancost RD, Brigmon RL, Lyons TW, Sassen R (2005) Lipid biomarkers and carbon isotope signatures of a microbial (Beggiatoa) mat associated with gas hydrates in the Gulf of Mexico. Appl Environ Microbiol 71:2106–2112PubMedCrossRefGoogle Scholar
  227. Zopfi J, Kjaer T, Nielsen LP, Jørgensen BB (2001) Ecology of Thioploca spp.: nitrate and sulphur storage in relation to chemical microgradients and influence of Thioploca spp. on sedimentary nitrogen cycle. Appl Environ Microbiol 67:5530–5537PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Gerard Muyzer
    • 1
    • 2
  • J. Gijs Kuenen
    • 1
  • Lesley A. Robertson
    • 1
  1. 1.Department of BiotechnologyDelft University of TechnologyDelftThe Netherlands
  2. 2.Department of Aquatic Microbiology, Institute for Biodiversity and Ecosystem DynamicsUniversity of AmsterdamAmsterdamThe Netherlands

Personalised recommendations