Anaerobic Hydrocarbon-Degrading Sulfate-Reducing Bacteria at Marine Gas and Oil Seeps

Part of the Springer Oceanography book series (SPRINGEROCEAN)


Microorganisms are key players in our biosphere because of their ability to degrade various organic compounds including a wide range of hydrocarbons. At hydrocarbon seeps, microorganisms with the ability to utilize diverse hydrocarbons (such as methane, short- and long-chain alkanes,  or aromatic hydrocarbons) as carbon and electron source are significantly influencing biogeochemical cycles. Marine hydrocarbon seep sediments are hot spots for microbial activity, particularly for sulfate-reducing bacteria that show elevated respiration rates at these sites. At some seeps, more than 90% of sulfate reduction is potentially coupled to non-methane hydrocarbon oxidation, emphasizing the environmental relevance of these microorganisms and the need to identify key players in situ. Several hydrocarbon-degrading sulfate-reducing bacteria were enriched or isolated from marine sediments, however, in situ active microorganisms were to a large extent represented by uncultivated taxa. Here, we provide an overview of the current understanding of non-methane hydrocarbon-degrading sulfate-reducing bacteria at marine hydrocarbon seeps, including their in situ distribution, abundance, and activity.


  1. Acosta-Gonzalez A, Rossello-Mora R, Marques S (2013) Characterization of the anaerobic microbial community in oil-polluted subtidal sediments: aromatic biodegradation potential after the Prestige oil spill. Environ Microbiol 15:77–92CrossRefGoogle Scholar
  2. Adams MM, Hoarfrost AL, Bose A, Joye SB, Girguis PR (2013) Anaerobic oxidation of short-chain alkanes in hydrothermal sediments: potential influences on sulfur cycling and microbial diversity. Front Microbiol 4:110Google Scholar
  3. Aeckersberg F, Bak F, Widdel F (1991) Anaerobic oxidation of saturated-hydrocarbons to CO2 by a new type of sulfate-reducing bacterium. Arch Microbiol 156:5–14CrossRefGoogle Scholar
  4. Aeckersberg F, Rainey FA, Widdel F (1998) Growth, natural relationships, cellular fatty acids and metabolic adaptation of sulfate-reducing bacteria that utilize long-chain alkanes under anoxic conditions. Arch Microbiol 170:361–369CrossRefGoogle Scholar
  5. Annweiler E, Materna A, Safinowski M, Kappler A, Richnow HH, Michaelis W, Meckenstock RU (2000) Anaerobic degradation of 2-methylnaphthalene by a sulfate-reducing enrichment culture. Appl Environ Microbiol 66:5329–5333CrossRefGoogle Scholar
  6. Bazylinski DA, Farrington JW, Jannasch HW (1988) Hydrocarbons in surface sediments from a Guaymas Basin hydrothermal vent site. Org Geochem 12:547–558CrossRefGoogle Scholar
  7. Becker A, Fritz-Wolf K, Kabsch W, Knappe J, Schultz S, Volker Wagner AF (1999) Structure and mechanism of the glycyl radical enzyme pyruvate formate-lyase. Nat Struct Biol 6:969–975CrossRefGoogle Scholar
  8. Beller HR, Spormann AM (1997) Anaerobic activation of toluene and o-xylene by addition to fumarate in denitrifying strain T. J Bacteriol 179:670–676CrossRefGoogle Scholar
  9. Beller HR, Spormann AM (1998) Analysis of the novel benzylsuccinate synthase reaction for anaerobic toluene activation based on structural studies of the product. J Bacteriol 180:5454–5457CrossRefGoogle Scholar
  10. Biegert T, Fuchs G, Heider J (1996) Evidence that anaerobic oxidation of toluene in the denitrifying bacterium Thauera aromatica is initiated by formation of benzylsuccinate from toluene and fumarate. Eur J Biochem 238:661–668CrossRefGoogle Scholar
  11. Boetius A, Knittel K (2010) Habitats of anaerobic methane oxidizers. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, Heidelberg, pp 2193–2202CrossRefGoogle Scholar
  12. Borrel G, Adam PS, McKay LJ, Chen LX, Sierra-García IN, Sieber CMK, Letourneur Q, Ghozlane A, Andersen GL, Li WJ, Hallam SJ, Muyzer G, de Oliveira VM, Inskeep WP, Banfield JF, Gribaldo S (2019) Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea. Nat Microbiol 4:603–613CrossRefGoogle Scholar
  13. Bose A, Rogers DR, Adams MM, Joye SB, Girguis PR (2013) Geomicrobiological linkages between short-chain alkane consumption and sulfate reduction rates in seep sediments. Front Microbiol 4:386CrossRefGoogle Scholar
  14. Bowles MW, Samarkin VA, Bowles KM, Joye SB (2011) Weak coupling between sulfate reduction and the anaerobic oxidation of methane in methane-rich seafloor sediments during ex situ incubation. Geochim Cosmochim Acta 75:500–519CrossRefGoogle Scholar
  15. Callaghan AV, Wawrik B, Ní Chadhain SM, Young LY, Zylstra GJ (2008) Anaerobic alkane-degrading strain AK-01 contains two alkylsuccinate synthase genes. Biochem Biophys Res Commun 366:142–148CrossRefGoogle Scholar
  16. Callaghan AV, Davidova IA, Savage-Ashlock K, Parisi VA, Gieg LM, Suflita JM, Kukor JJ, Wawrik B (2010) Diversity of benzyl- and alkylsuccinate synthase genes in hydrocarbon-impacted environments and enrichment cultures. Environ Sci Technol 44:7287–7294CrossRefGoogle Scholar
  17. Chen SC, Musat N, Lechtenfeld OJ, Paschke H, Schmidt M, Said N, Popp D, Calabrese F, Stryhanyuk H, Jaekel U, Zhu YG, Joye SB, Richnow HH, Widdel F, Musat F (2019) Anaerobic oxidation of ethane by archaea from a marine hydrocarbon seep. Nature 568:108–111CrossRefGoogle Scholar
  18. Cheng L, Ding C, Li Q, He Q, Dai L-r, Zhang H (2013a) DNA-SIP reveals that Syntrophaceae play an important role in methanogenic hexadecane degradation. PLoS ONE 8:e66784CrossRefGoogle Scholar
  19. Cheng L, Rui J, Li Q, Zhang H, Lu Y (2013b) Enrichment and dynamics of novel syntrophs in a methanogenic hexadecane-degrading culture from a Chinese oilfield. FEMS Microbiol Ecol 83:757–766CrossRefGoogle Scholar
  20. Cravo-Laureau C, Matheron R, Joulian C, Cayol JL, Hirschler-Rea A (2004) Desulfatibacillum alkenivorans sp. nov., a novel n-alkene-degrading, sulfate-reducing bacterium, and emended description of the genus Desulfatibacillum. Int J Syst Evol Microbiol 54:1639–1642CrossRefGoogle Scholar
  21. Didyk BM, Simoneit BRT (1989) Hydrothermal oil of Guaymas Basin and implications for petroleum formation mechanisms. Nature 342:65–69CrossRefGoogle Scholar
  22. Dolfing J, Zeyer J, Binder-Eicher P, Schwarzenbach RP (1990) Isolation and characterization of a bacterium that mineralizes toluene in the absence of molecular oxygen. Arch Microbiol 154:336–341CrossRefGoogle Scholar
  23. Dombrowski N, Seitz KW, Teske AP, Baker BJ (2017) Genomic insights into potential interdependencies in microbial hydrocarbon and nutrient cycling in hydrothermal sediments. Microbiome 5:106CrossRefGoogle Scholar
  24. Dowell F, Cardman Z, Dasarathy S, Kellermann MY, Lipp JS, Ruff SE, Biddle JF, McKay LJ, MacGregor BJ, Lloyd KG, Albert DB, Mendlovitz H, Hinrichs KU, Teske A (2016) Microbial communities in methane- and short chain alkane-rich hydrothermal sediments of Guaymas Basin. Front Microbiol 7:17CrossRefGoogle Scholar
  25. Ehrenreich P, Behrends A, Harder J, Widdel F (2000) Anaerobic oxidation of alkanes by newly isolated denitrifying bacteria. Arch Microbiol 173:58–64CrossRefGoogle Scholar
  26. Evans PN, Parks DH, Chadwick GL, Robbins SJ, Orphan VJ, Golding SD, Tyson GW (2015) Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350:434–438CrossRefGoogle Scholar
  27. Formolo MJ, Lyons TW, Zhang C, Kelley C, Sassen R, Horita J, Cole DR (2004) Quantifying carbon sources in the formation of authigenic carbonates at gas hydrate sites in the Gulf of Mexico. Chem Geol 205:253–264CrossRefGoogle Scholar
  28. Fries MR, Zhou J, Chee-Sanford J, Tiedje JM (1994) Isolation, characterization, and distribution of denitrifying toluene degraders from a variety of habitats. Appl Environ Microbiol 60:2802–2810CrossRefGoogle Scholar
  29. Galushko A, Minz D, Schink B, Widdel F (1999) Anaerobic degradation of naphthalene by a pure culture of a novel type of marine sulphate-reducing bacterium. Environ Microbiol 1:415–420CrossRefGoogle Scholar
  30. Gieg LM, Suflita JM (2002) Detection of anaerobic metabolites of saturated and aromatic hydrocarbons in petroleum-contaminated aquifers. Environ Sci Technol 36(17):3755–3762CrossRefGoogle Scholar
  31. Gittel A, Donhauser J, Røy H, Girguis PR, Jørgensen BB, Kjeldsen KU (2015) Ubiquitous presence and novel diversity of anaerobic alkane degraders in cold marine sediments. Front Microbiol 6:1414CrossRefGoogle Scholar
  32. Grundmann O, Behrends A, Rabus R, Amann J, Halder T, Heider J, Widdel F (2008) Genes encoding the candidate enzyme for anaerobic activation of n-alkanes in the denitrifying bacterium, strain HxN1. Environ Microbiol 10:376–385CrossRefGoogle Scholar
  33. Grünke S, Felden J, Lichtschlag A, Girnth AC, de Beer D, Wenzhöfer F, Boetius A (2011) Niche differentiation among mat-forming, sulfide-oxidizing bacteria at cold seeps of the Nile Deep Sea Fan (Eastern Mediterranean Sea). Geobiology 9:330–348CrossRefGoogle Scholar
  34. Gutierrez T, Kleindienst S (this volume) Uncovering microbial hydrocarbon degradation processes: the promise of stable isotope probing. In: Marine Hydrocarbon Seeps, Springer Oceanography, Teske A, Carvalho V (eds.), Springer, BerlinGoogle Scholar
  35. Harms G, Rabus R, Widdel F (1999a) Anaerobic oxidation of the aromatic plant hydrocarbon p-cymene by newly isolated denitrifying bacteria. Arch Microbiol 172:303–312CrossRefGoogle Scholar
  36. Harms G, Zengler K, Rabus R, Aeckersberg F, Minz D, Rosselló-Móra R, Widdel F (1999b) Anaerobic oxidation of o-xylene, m-xylene, and homologous alkylbenzenes by new types of sulfate-reducing bacteria. Appl Environ Microbiol 65:999–1004CrossRefGoogle Scholar
  37. Hassanshahian M, Emtiazi G, Kermanshahi RK, Cappello S (2010) Comparison of oil degrading microbial communities in sediments from the Persian Gulf and Caspian Sea. Soil Sediment Contam: Int J 19:277–291CrossRefGoogle Scholar
  38. Heider J, Schühle K (2013) Anaerobic biodegradation of hydrocarbons including methane. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: prokaryotic physiology and biochemistry. Springer, Berlin, Heidelberg, pp 605–634CrossRefGoogle Scholar
  39. Heider J, Szaleniec M, Martins BM, Seyhan D, Buckel W, Golding BT (2016) Structure and function of benzylsuccinate synthase and related fumarate-adding glycyl radical enzymes. J Mol Microbiol Biotechnol 26:29–44CrossRefGoogle Scholar
  40. Higashioka Y, Kojima H, Nakagawa T, Sato S, Fukui M (2009) A novel n-alkane-degrading bacterium as a minor member of p-xylene-degrading sulfate-reducing consortium. Biodegradation 20:383–390CrossRefGoogle Scholar
  41. Hinrichs K-U, Boetius A (2002) The anaerobic oxidation of methane: new insights in microbial ecology and biogeochemistry. Springer, BerlinGoogle Scholar
  42. Jaekel U, Musat N, Adam B, Kuypers M, Grundmann O, Musat F (2013) Anaerobic degradation of propane and butane by sulfate-reducing bacteria enriched from marine hydrocarbon cold seeps. ISME J 7:885–895CrossRefGoogle Scholar
  43. Jaekel U, Vogt C, Fischer A, Richnow HH, Musat F (2014) Carbon and hydrogen stable isotope fractionation associated with the anaerobic degradation of propane and butane by marine sulfate-reducing bacteria. Environ Microbiol 16:130–140CrossRefGoogle Scholar
  44. Joye SB, Boetius A, Orcutt BN, Montoya JP, Schulz HN, Erickson MJ, Lugo SK (2004) The anaerobic oxidation of methane and sulfate reduction in sediments from Gulf of Mexico cold seeps. Chem Geol 205:219–238CrossRefGoogle Scholar
  45. Kallmeyer J, Boetius A (2004) Effects of temperature and pressure on sulfate reduction and anaerobic oxidation of methane in hydrothermal sediments of Guaymas Basin. Appl Environ Microbiol 70:1231–1233CrossRefGoogle Scholar
  46. Khelifi N, Amin Ali O, Roche P, Grossi V, Brochier-Armanet C, Valette O, Ollivier B, Dolla A, Hirschler-Rea A (2014) Anaerobic oxidation of long-chain n-alkanes by the hyperthermophilic sulfate-reducing archaeon, Archaeoglobus fulgidus. ISME J 8:2153–2166CrossRefGoogle Scholar
  47. Kleindienst S (2012) Hydrocarbon-degrading sulfate-reducing bacteria in marine hydrocarbon seep sediments. University of BremenGoogle Scholar
  48. Kleindienst S, Ramette A, Amann R, Knittel K (2012) Distribution and in situ abundance of sulfate-reducing bacteria in diverse marine hydrocarbon seep sediments. Environ Microbiol 14:2689–2710CrossRefGoogle Scholar
  49. Kleindienst S, Herbst F-A, Stagars M, von Netzer F, von Bergen M, Seifert J, Peplies J, Amann R, Musat F, Lueders T, Knittel K (2014) Diverse sulfate-reducing bacteria of the Desulfosarcina/Desulfococcus clade are the key alkane degraders at marine seeps. ISME J 8:2029–2044CrossRefGoogle Scholar
  50. Kleindienst S, Joye SB (2017) Global aerobic degradation of hydrocarbons in aquatic systems. In: Rojo F (ed) Aerobic utilization of hydrocarbons, oils and lipids. Springer International Publishing, Cham, pp 1–18Google Scholar
  51. Kniemeyer O, Fischer T, Wilkes H, Glöckner FO, Widdel F (2003) Anaerobic degradation of ethylbenzene by a new type of marine sulfate-reducing bacterium. Appl Environ Microbiol 69:760–768CrossRefGoogle Scholar
  52. Kniemeyer O, Musat F, Sievert SM, Knittel K, Wilkes H, Blumenberg M, Michaelis W, Classen A, Bolm C, Joye SB, Widdel F (2007) Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria. Nature 449:898–910CrossRefGoogle Scholar
  53. Knittel K, Boetius A, Lemke A, Eilers H, Lochte K, Pfannkuche O, Linke P, Amann R (2003) Activity, distribution, and diversity of sulfate reducers and other bacteria in sediments above gas hydrate (Cascadia margin, Oregon). Geomicrobiol J 20:269–294CrossRefGoogle Scholar
  54. Kropp KG, Davidova IA, Suflita JM (2000) Anaerobic oxidation of n-dodecane by an addition reaction in a sulfate-reducing bacterial enrichment culture. Appl Environ Microbiol 66:5393–5398CrossRefGoogle Scholar
  55. Krüger M, Meyerdierks A, Glöckner FO, Amann R, Widdel F, Kube M, Reinhardt R, Kahnt J, Bocher R, Thauer RK, Shima S (2003) A conspicuous nickel protein in microbial mats that oxidize methane anaerobically. Nature 426:878–881CrossRefGoogle Scholar
  56. Krukenberg V, Harding K, Richter M, Glockner FO, Gruber-Vodicka HR, Adam B, Berg JS, Knittel K, Tegetmeyer HE, Boetius A, Wegener G (2016) Candidatus Desulfofervidus auxilii, a hydrogenotrophic sulfate-reducing bacterium involved in the thermophilic anaerobic oxidation of methane. Environ Microbiol 18:3073–3091CrossRefGoogle Scholar
  57. Laso-Pérez R, Wegener G, Knittel K, Widdel F, Harding KJ, Krukenberg V, Meier DV, Richter M, Tegetmeyer HE, Riedel D, Richnow HH, Adrian L, Reemtsma T, Lechtenfeld OJ, Musat F (2016) Thermophilic archaea activate butane via alkyl-coenzyme M formation. Nature 539:396–401CrossRefGoogle Scholar
  58. Liu A, Garcia-Dominguez E, Rhine ED, Young LY (2004) A novel arsenate respiring isolate that can utilize aromatic substrates. FEMS Microbiol Ecol 48:323–332CrossRefGoogle Scholar
  59. 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:e8738Google Scholar
  60. Lösekann T, Knittel K, Nadalig T, Fuchs B, Niemann H, Boetius A, Amann R (2007) Diversity and abundance of aerobic and anaerobic methane oxidizers at the Haakon Mosby Mud Volcano, Barents Sea. Appl Environ Microbiol 73:3348–3362CrossRefGoogle Scholar
  61. Lovley DR, Lonergan DJ (1990) Anaerobic oxidation of toluene, phenol, and p-cresol by the dissimilatory iron-reducing organism, GS-15. Appl Environ Microbiol 56:1858–1864CrossRefGoogle Scholar
  62. Martinez RJ, Mills HJ, Story S, Sobecky PA (2006) Prokaryotic diversity and metabolically active microbial populations in sediments from an active mud volcano in the Gulf of Mexico. Environ Microbiol 8:1783–1796CrossRefGoogle Scholar
  63. Mastalerz V, de Lange GJ, Dählmann A (2009) Differential aerobic and anaerobic oxidation of hydrocarbon gases discharged at mud volcanoes in the Nile deep-sea fan. Geochim Cosmochim Acta 73:3849–3863CrossRefGoogle Scholar
  64. Meckenstock RU, Morasch B, Warthmann R, Schink B, Annweiler E, Michaelis W, Richnow HH (1999) 13C/12C isotope fractionation of aromatic hydrocarbons during microbial degradation. Environ Microbiol 1:409–414CrossRefGoogle Scholar
  65. Meckenstock RU, Annweiler E, Michaelis W, Richnow HH, Schink B (2000) Anaerobic naphthalene degradation by a sulfate-reducing enrichment culture. Appl Environ Microbiol 66:2743–2747CrossRefGoogle Scholar
  66. Meyerdierks A, Kube M, Lombardot T, Knittel K, Bauer M, Glöckner FO, Reinhardt R, Amann R (2005) Insights into the genomes of archaea mediating the anaerobic oxidation of methane. Environ Microbiol 7(12):1937–1951CrossRefGoogle Scholar
  67. Milkov AV, Claypool GE, Lee Y-J, Torres ME, Borowski WS, Tomaru H, Sassen R, Long PE (2004) Ethane enrichment and propane depletion in subsurface gases indicate gas hydrate occurrence in marine sediments at southern Hydrate Ridge offshore Oregon. Org Geochem 35:1067–1080CrossRefGoogle Scholar
  68. Mills HJ, Hodges C, Wilson K, MacDonald IR, Sobecky PA (2003) Microbial diversity in sediments associated with surface-breaching gas hydrate mounds in the Gulf of Mexico. FEMS Microbiol Ecol 46:39–52CrossRefGoogle Scholar
  69. 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
  70. Mills HJ, Martinez RJ, Story S, Sobecky PA (2005) Characterization of microbial community structure in Gulf of Mexico gas hydrates: comparative analysis of DNA- and RNA-derived clone libraries. Appl Environ Microbiol 71:3235–3247CrossRefGoogle Scholar
  71. Miralles G, Grossi V, Acquaviva M, Duran R, Bertrand JC, Cuny P (2007) Alkane biodegradation and dynamics of phylogenetic subgroups of sulfate-reducing bacteria in an anoxic coastal marine sediment artificially contaminated with oil. Chemosphere 68:1327–1334CrossRefGoogle Scholar
  72. Morasch B, Schink B, Tebbe CC, Meckenstock RU (2004) Degradation of o-xylene and m-xylene by a novel sulfate-reducer belonging to the genus Desulfotomaculum. Arch Microbiol 181:407–417CrossRefGoogle Scholar
  73. Musat F, Galushko A, Jacob J, Widdel F, Kube M, Reinhardt R, Wilkes H, Schink B, Rabus R (2009) Anaerobic degradation of naphthalene and 2-methylnaphthalene by strains of marine sulfate-reducing bacteria. Environ Microbiol 11:209–219CrossRefGoogle Scholar
  74. Musat F, Wilkes H, Behrends A, Woebken D, Widdel F (2010) Microbial nitrate-dependent cyclohexane degradation coupled with anaerobic ammonium oxidation. ISME J 4:1290–1301CrossRefGoogle Scholar
  75. Musat F (2015) The anaerobic degradation of gaseous, nonmethane alkanes—from in situ processes to microorganisms. Comput Struct Biotechnol J 13:222–228CrossRefGoogle Scholar
  76. Niemann H, Duarte J, Hensen C, Omoregie E, Magalhães VH, Elvert M, Pinheiro LM, Kopf A, Boetius A (2006) Microbial methane turnover at mud volcanoes of the Gulf of Cadiz. Geochim Cosmochim Acta 70:5336–5355CrossRefGoogle Scholar
  77. Ommedal H, Torsvik T (2007) Desulfotignum toluenicum sp. nov., a novel toluene-degrading, sulphate-reducing bacterium isolated from an oil-reservoir model column. Int J Syst Evol Microbiol 57:2865–2869CrossRefGoogle Scholar
  78. Omoregie EO, Mastalerz V, de Lange G, Straub KL, Kappler A, Røy H, Stadnitskaia A, Foucher JP, Boetius A (2008) Biogeochemistry and community composition of iron- and sulfur-precipitating microbial mats at the Chefren mud volcano (Nile Deep Sea fan, Eastern Mediterranean). Appl Environ Microbiol 74:3198–3215CrossRefGoogle Scholar
  79. Omoregie EO, Niemann H, Mastalerz V, de Lange GJ, Stadnitskaia A, Mascle J, Foucher JP, Boetius A (2009) Microbial methane oxidation and sulfate reduction at cold seeps of the deep Eastern Mediterranean Sea. Mar Geology 261:114–127CrossRefGoogle Scholar
  80. Orcutt BN, Joye SB, Kleindienst S, Knittel K, Ramette A, Reitz A, Samarkin V, Treude T, Boetius A (2010) Impact of natural oil and higher hydrocarbons on microbial diversity, distribution, and activity in Gulf of Mexico cold-seep sediments. Deep-Sea Res Part II 57:2008–2021CrossRefGoogle Scholar
  81. Orphan VJ, Hinrichs K-U, Ussler W, Paull CK, Taylor LT, Sylva SP, Hayes JM, DeLong EF (2001) Comparative analysis of methane-oxidizing archaea and sulfate-reducing bacteria in anoxic marine sediments. Appl Environ Microbiol 67:1922–1934CrossRefGoogle Scholar
  82. Pachiadaki MG, Lykousis V, Stefanou EG, Kormas KA (2010) Prokaryotic community structure and diversity in the sediments of an active submarine mud volcano (Kazan mud volcano, East Mediterranean Sea). FEMS Microbiol Ecol 72:429–444CrossRefGoogle Scholar
  83. Pachiadaki M, Kallionaki A, Dählmann A, De Lange G, Kormas K (2011) Diversity and spatial distribution of prokaryotic communities along a sediment vertical profile of a deep-sea mud volcano. Microb Ecol 62:655–668CrossRefGoogle Scholar
  84. Pernthaler A, Dekas AE, Brown CT, Goffredi SK, Embaye T, Orphan VJ (2008) Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics. Proc Natl Acad Sci U S A 105:7052–7057CrossRefGoogle Scholar
  85. Petro C, Jochum LM, Schreiber L, Marshall IPG, Schramm A, Kjeldsen KU (2019) Single-cell amplified genomes of two uncultivated members of the deltaproteobacterial SEEP-SRB1 clade, isolated from marine sediment. Mar Genomics 46:66–69CrossRefGoogle Scholar
  86. Quistad SD, Valentine DL (2011) Anaerobic propane oxidation in marine hydrocarbon seep sediments. Geochim Cosmochim Acta 75:2159–2169CrossRefGoogle Scholar
  87. Rabus R, Nordhaus R, Ludwig W, Widdel F (1993) Complete oxidation of toluene under strictly anoxic conditions by a new sulfate-reducing bacterium. Appl Environ Microbiol 59:1444–1451CrossRefGoogle Scholar
  88. Rabus R, Widdel F (1995) Anaerobic degradation of ethylbenzene and other aromatic-hydrocarbons by new denitrifying bacteria. Arch Microbiol 163:96–103CrossRefGoogle Scholar
  89. Rabus R, Wilkes H, Behrends A, Armstroff A, Fischer T, Pierik AJ, Widdel F (2001) Anaerobic initial reaction of n-alkanes in a denitrifying bacterium: evidence for (1-methylpentyl)succinate as initial product and for involvement of an organic radical in n-hexane metabolism. J Bacteriol 183:1707–1715CrossRefGoogle Scholar
  90. Rabus R, Boll M, Heider J, Meckenstock RU, Buckel W, Einsle O, Ermler U, Golding B, Gunsalus R, Kroneck P, Krüger M, Lueders T, Martins B, Musat F, Richnow H, Schink B, Seifert J, Szaleniec M, Treude T, Ullmann G, Vogt C, von Bergen M, Wilkes H (2016) Anaerobic microbial degradation of hydrocarbons: from enzymatic reactions to the environment. J Mol Microbiol Biotechnol 26:5–28CrossRefGoogle Scholar
  91. Reeburgh WS (2007) Oceanic methane biogeochemistry. Chem Rev 107:486–513CrossRefGoogle Scholar
  92. Ruff SE, Arnds J, Knittel K, Amann R, Wegener G, Ramette A, Boetius A (2013) Microbial communities of deep-sea methane seeps at Hikurangi continental margin (New Zealand). PLoS ONE 8:e72627CrossRefGoogle Scholar
  93. Ruff SE, Kuhfuss H, Wegener G, Lott C, Ramette A, Wiedling J, Knittel K, Weber M (2016) Methane seep in shallow-water permeable sediment harbors high diversity of anaerobic methanotrophic communities, Elba, Italy. Front Microbiol 7:374CrossRefGoogle Scholar
  94. Sassen R, Joye SB, Sweet ST, DeFreitas DA, Milkov AV, MacDonald IR (1999) Thermogenic gas hydrates and hydrocarbon gases in complex chemosynthetic communities, Gulf of Mexico continental slope. Org Geochem 30:485–497CrossRefGoogle Scholar
  95. Sassen R, Roberts HH, Carney R, Milkov AV, DeFreitas DA, Lanoil B, Zhang C (2004) Free hydrocarbon gas, gas hydrate, and authigenic minerals in chemosynthetic communities of the northern Gulf of Mexico continental slope: relation to microbial processes. Chem Geol 205:195–217CrossRefGoogle Scholar
  96. Savage KN, Krumholz LR, Gieg LM, Parisi VA, Suflita JM, Allen J, Philp RP, Elshahed MS (2010) Biodegradation of low-molecular-weight alkanes under mesophilic, sulfate-reducing conditions: metabolic intermediates and community patterns. FEMS Microbiol Ecol 72:485–495CrossRefGoogle Scholar
  97. Schreiber L, Holler T, Knittel K, Meyerdierks A, Amann R (2010) Identification of the dominant sulfate-reducing bacterial partner of anaerobic methanotrophs of the ANME-2 clade. Environ Microbiol 12:2327–2340Google Scholar
  98. Schubotz F, Lipp JS, Elvert M, Kasten S, Mollar XP, Zabel M, Bohrmann G, Hinrichs K-U (2011) Petroleum degradation and associated microbial signatures at the Chapopote asphalt volcano, Southern Gulf of Mexico. Geochim Cosmochim Acta 75:4377–4398CrossRefGoogle Scholar
  99. So CM, Young LY (1999) Isolation and characterization of a sulfate-reducing bacterium that anaerobically degrades alkanes. Appl Environ Microbiol 65:2969–2976CrossRefGoogle Scholar
  100. Stagars MH, Ruff SE, Amann R, Knittel K (2016) High diversity of anaerobic alkane-degrading microbial communities in marine seep sediments based on (1-methylalkyl)succinate synthase genes. Front Microbiol 6:1511CrossRefGoogle Scholar
  101. Stagars MH, Mishra S, Treude T, Amann R, Knittel K (2017) Microbial community response to simulated petroleum seepage in Caspian Sea sediments. Front Microbiol 8:764CrossRefGoogle Scholar
  102. Tan B, Nesbo C, Foght J (2014) Re-analysis of omics data indicates Smithella may degrade alkanes by addition to fumarate under methanogenic conditions. ISME J 8:2353–2356CrossRefGoogle Scholar
  103. Tan B, Fowler SJ, Abu Laban N, Dong X, Sensen CW, Foght J, Gieg LM (2015) Comparative analysis of metagenomes from three methanogenic hydrocarbon-degrading enrichment cultures with 41 environmental samples. ISME J 9:2028–2045CrossRefGoogle Scholar
  104. Teske A, Hinrichs K-U, Edgcomb V, de Vera Gomez A, 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 68:1994–2007Google Scholar
  105. Teske A, Durbin A, Ziervogel K, Cox C, Arnosti C (2011) Microbial community composition and function in permanently cold seawater and sediments from an arctic fjord of Svalbard. Appl Environ Microbiol 77:2008–2018CrossRefGoogle Scholar
  106. von Netzer F, Pilloni G, Kleindienst S, Kruger M, Knittel K, Grundger F, Lueders T (2013) Enhanced gene detection assays for fumarate-adding enzymes allow uncovering of anaerobic hydrocarbon degraders in terrestrial and marine systems. Appl Environ Microbiol 79:543–552CrossRefGoogle Scholar
  107. von Netzer F, Kuntze K, Vogt C, Richnow HH, Boll M, Lueders T (2016) Functional gene markers for fumarate-adding and dearomatizing key enzymes in anaerobic aromatic hydrocarbon degradation in terrestrial environments. J Mol Microbiol Biotechnol 26:180–194CrossRefGoogle Scholar
  108. Watanabe M, Higashioka Y, Kojima H, Fukui M (2017) Desulfosarcina widdelii sp. nov. and Desulfosarcina alkanivorans sp. nov., hydrocarbon-degrading sulfate-reducing bacteria isolated from marine sediment and emended description of the genus Desulfosarcina. Int J Syst Evol Microbiol 67:2994–2997CrossRefGoogle Scholar
  109. Wegener G, Shovitri M, Knittel K, Niemann H, Hovland M, Boetius A (2008) Biogeochemical processes and microbial diversity of the Gullfaks and Tommeliten methane seeps (Northern North Sea). Biogeosciences 5:1127–1144CrossRefGoogle Scholar
  110. Wegener G, Krukenberg V, Ruff SE, Kellermann MY, Knittel K (2016) Metabolic capabilities of microorganisms involved in and associated with the anaerobic oxidation of methane. Front Microbiol 7:46CrossRefGoogle Scholar
  111. Widdel F, Knittel K, Galushko A (2010) Anaerobic hydrocarbon-degrading microorganisms: an overview. In: Timmis KN, McGenity T, van der Meer JR, de Lorenzo V (eds) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, Heidelberg, pp 1997–2021CrossRefGoogle Scholar
  112. Wilkes H, Schwarzbauer J (2010) Hydrocarbons: an introduction to structure, physico-chemical properties and natural occurrence. In: Timmis KN, McGenity T, van der Meer JR, de Lorenzo V (eds) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, Heidelberg, pp 5–48Google Scholar
  113. Wilkes H, Buckel W, Golding BT, Rabus R (2016) Metabolism of hydrocarbons in n-alkane-utilizing anaerobic bacteria. J Mol Microbiol Biotechnol 26:138–151CrossRefGoogle Scholar
  114. Winderl C, Schaefer S, Lueders T (2007) Detection of anaerobic toluene and hydrocarbon degraders in contaminated aquifers using benzylsuccinate synthase (bssA) genes as a functional marker. Environ Microbiol 9:1035–1046CrossRefGoogle Scholar
  115. Yagi JM, Suflita JM, Gieg LM, DeRito CM, Jeon C-O, Madsen EL (2010) Subsurface cycling of nitrogen and anaerobic aromatic hydrocarbon biodegradation revealed by nucleic acid and metabolic biomarkers. Appl Environ Microbiol 76:3124–3134CrossRefGoogle Scholar
  116. Yanagawa K, Morono Y, de Beer D, Haeckel M, Sunamura M, Futagami T, Hoshino T, Terada T, Nakamura K-i, Urabe T, Rehder G, Boetius A, Inagaki F (2013) Metabolically active microbial communities in marine sediment under high-CO2 and low-pH extremes. ISME J 7:555–567CrossRefGoogle Scholar
  117. Zengler K, Heider J, Rosselló-Móra R, Widdel F (1999a) Phototrophic utilization of toluene under anoxic conditions by a new strain of Blastochloris sulfoviridis. Arch Microbiol 172:204–212CrossRefGoogle Scholar
  118. Zengler K, Richnow HH, Rosselló-Móra R, Michaelis W, Widdel F (1999b) Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 401:266–269CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Eberhard Karls UniversityTübingenGermany
  2. 2.Max-Planck Institute for Marine MicrobiologyBremenGermany

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