Benthic Deep-Sea Life Associated with Asphaltic Hydrocarbon Emissions in the Southern Gulf of Mexico

Part of the Springer Oceanography book series (SPRINGEROCEAN)


At the Campeche Knolls in the southern Gulf of Mexico large-scale hydrocarbon emissions are associated with numerous salt tectonic structures. A notable feature of this area is the expulsion of highly viscous heavy oils, also referred to as asphalts, which form lava-like flows on the seafloor. These oil and asphalt seeps have been detected via satellite imaging of oil slicks at the ocean surface and by acoustically-detected gas emission sites in the water column. Here, we describe the type locality ‘Chapopote’ (Aztec word for tar) where the expelled hydrocarbons provide an energy source for microorganisms and subsequently the deep-sea fauna. In deeper asphalt layers and sediment, 16S rRNA gene sequences of archaea affiliated with Methanosaeta and bacteria of the Syntrophaceae were detected. Together with the observed light methane isotope values this indicates biogenic methanogenesis from aliphatic hydrocarbons at these depths. In shallow oil-soaked sediments gene sequences of hydrocarbon-degrading sulfate-reducing Deltaproteobacteria were found. These sediments showed high sulfate reduction but only minor methane oxidation rates. Asphalts and oil-soaked sediments freshly exposed to the surface were densely covered by microbial mats, signaling high metabolic activity. The surface microbial communities were dominated by diverse Gammaproteobacteria that likely oxidized hydrocarbons and reduced sulfur compounds. Surface asphalts were colonized by tube worms, mussels and sponges that host bacterial symbionts. In addition, grazing invertebrates such as sea cucumbers, shrimps, and crabs evidently fed on the microbial mats. This close link between the microbial and macro-benthic life demonstrates an efficient energy transfer to higher trophic levels from microbial hydrocarbon oxidation at the base of this unique asphalt-hosted ecosystem.



We thank the scientific crew and ROV team of R/V METEOR Expedition M67/2b. The Deutsche Forschungsgemeinschaft (DFG) and the Research Center/Excellence Cluster “The Ocean in the Earth System” are acknowledged for funding. Elva Escobar-Briones and Adriana Gaytán-Caballero are thanked for dissecting the holothurian and providing gut contents. Christiane Berndmeyer and Viola Beier are acknowledged for help in the laboratory and processing data and Kai-Uwe Hinrichs and Antje Boetius for providing laboratory facilities.


  1. 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
  2. Arellano SM, Lee OO, Lafi FF, Yang J, Wang Y, Young CM, Qian P-Y (2013) Deep sequencing of Myxilla (Ectyomyxilla) methanophila, an epibiotic sponge on cold-seep tubeworms, reveals methylotrophic, thiotrophic, and putative hydrocarbon-degrading microbial associations. Microb Ecol 65:450–461CrossRefGoogle Scholar
  3. Berdugo-Clavijo C, Gieg LM (2014) Conversion of crude oil to methane by a microbial consortium enriched from oil reservoir production waters. Front Microbiol 5:197CrossRefGoogle Scholar
  4. Bernard BB, Brooks JM, Sackett WM (1976) Natural gas seepage in the Gulf of Mexico. Earth Plant Sci Lett 31:48–54CrossRefGoogle Scholar
  5. Blumenberg M, Krüger M, Nauhaus K, Talbot HM, Oppermann BI, Seifert R, Pape T, Michaelis W (2004) Biosynthesis of hopanoids by sulfate-reducing bacteria (genus Desulfovibrio). Environ Microbiol 8:1220–1227CrossRefGoogle Scholar
  6. Boetius A, Wenzhöfer F (2013) Seafloor oxygen consumption fuelled by methane from cold seeps. Nat Geosci 6:725–734CrossRefGoogle Scholar
  7. Boetius A, Ravenschlag K, Schubert CJ, Rickert D, Widdel F, Gieseke A, Amann R, Jørgensen BB, Witte U, Pfannkuche O (2000) A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407:623–626Google Scholar
  8. Borrel G, Adam PS, McKay LJ, Chen L-X, Sierra-García IN, Sieber CMK, Letourneur Q, Ghozlane A, Andersen GL, Li W-J, 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
  9. Bowman JP (2006) The methanotrophs–the families Methylococcaceae and Methylocystaceae. Prokaryotes 5:266–289CrossRefGoogle Scholar
  10. Bowman JP, Sly LI, Nichols PD, Hayward AC (1993) Revised taxonomy of the methanotrophs: Description of Methylobacter gen. nov., emendation of Methylococcus, validation of Methylosinus and Methylocystis species, and a proposal that the family Methylococcaceae includes only the Group I methanotrophs. Int J Syst Evol Microbiol 43:735–753Google Scholar
  11. Brüning M, Sahling H, MacDonald IR, Ding F, Bohrmann G (2010) Origin, distribution, and alteration of asphalts at Chapopote Knoll, Southern Gulf of Mexico. Mar Petrol Geol 27:1093–1106CrossRefGoogle Scholar
  12. Bryant WR, Lugo J, Cordova C, Salvador A (1991) Physiography and bathymetry v. J. Boulder, Geological Society of America, Decade of North American Geology, The Gulf of Mexico Basin, pp 13–30Google Scholar
  13. Coelho RR, Hovell I, de Mello Monte MB, Middea A, de Souza AL (2006) Characterisation of aliphatic chains in vacuum residues (VRs) of asphaltenes and resins using molecular modelling and FTIR techniques. Fuel Process Technol 87:325–333CrossRefGoogle Scholar
  14. Ding F, Spiess V, Brüning M, Fekete N, Keil H, Bohrmann G (2008) A conceptual model for hydrocarbon accumulation and seepage processes around Chapopote asphalt site, southern Gulf of Mexico: from high resolution seismic point of view. J Geophys Res Solid Earth 113:B08404CrossRefGoogle Scholar
  15. Dojka MA, Hugenholtz P, Haack SK, Pace NR (1998) Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl Environ Microbiol 64:3869–3877CrossRefGoogle Scholar
  16. Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6:725–740CrossRefGoogle Scholar
  17. Duperron S, Sibuet M, MacGregor BJ, Kuypers MM, Fisher CR, Dubilier N (2007) Diversity, relative abundance and metabolic potential of bacterial endosymbionts in three Bathymodiolus mussel species from cold seeps in the Gulf of Mexico. Environ Microbiol 9:1423–1438CrossRefGoogle Scholar
  18. Elvert M, Niemann H (2008) Occurrence of unusual steroids and hopanoids derived from aerobic methanotrophs at an active marine mud volcano. Org Geochem 39:167–177CrossRefGoogle Scholar
  19. Elvert M, Boetius A, Knittel K, Jørgensen BB (2003) Characterization of specific membrane fatty acids as chemotaxonomic markers for sulfate-reducing bacteria involved in anaerobic oxidation of methane. Geomicrobiol J 20:403–419CrossRefGoogle Scholar
  20. Feng G, Sun W, Zhang F, Karthik L, Li Z (2016) Inhabitancy of active Nitrosopumilus-like ammonia-oxidizing archaea and Nitrospira nitrite-oxidizing bacteria in the sponge Theonella swinhoei. Sci Rep 6:24966CrossRefGoogle Scholar
  21. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299Google Scholar
  22. Gutierrez T, Singleton DR, Berry D, Yang T, Aitken MD, Teske A (2013) Hydrocarbon-degrading bacteria enriched by the Deepwater Horizon oil spill identified by cultivation and DNA-SIP. ISME J 7:2091–2104CrossRefGoogle Scholar
  23. Guzman-Vega M, Mello M (1999) Origin of oil in the Sureste Basin, Mexico. AAPG Bull 83:1068–1095Google Scholar
  24. Habe H, Omori T (2003) Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67:225–243CrossRefGoogle Scholar
  25. Hallam SJ, Konstantinidis KT, Putnam N, Schleper C, Watanabe Y-I, Sugahara J, Preston C, de la Torre J, Richardson PM, DeLong EF (2006) Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc Natl Acad Sci 103:18296–18301CrossRefGoogle Scholar
  26. Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471Google Scholar
  27. Head IM, Jones DM, Röling WF (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4:173–182CrossRefGoogle Scholar
  28. Hinrichs K-U, Hayes JM, Sylva SP, Brewer PG, DeLong EF (1999) Methane-consuming archaebacteria in marine sediments. Nature 398:802–805CrossRefGoogle Scholar
  29. Hinrichs K-U, Summons RE, Orphan V, Sylva SP, Hayes JM (2000) Molecular and isotopic analysis of anaerobic methane-oxidizing communities in marine sediments. Org Geochem 31:1685–1701CrossRefGoogle Scholar
  30. Hinrichs K-U, Hmelo LR, Sylva SP (2003) Molecular fossil record of elevated methane levels in late Pleistocene coastal waters. Science 299:1214–1217CrossRefGoogle Scholar
  31. Hoffmann F, Radax R, Woebken D, Holtappels M, Lavik G, Rapp HT, Schläppy M-L, Schleper C, Kuypers MMM (2009) Complex nitrogen cycling in the sponge Geodia barretti. Environ Microbiol 11:2228–2243CrossRefGoogle Scholar
  32. Hostettler FD, Kvenvolden KA (1994) Geochemical changes in crude oil spilled from the Exxon Valdez supertanker into Prince William Sound, Alaska. Org Geochem 21:927–936CrossRefGoogle Scholar
  33. Jørgensen BB (1977) The sulfur cycle of a coastal marine sediment (Limfjorden, Denmark). Limnol Oceanogr 22:814–832CrossRefGoogle Scholar
  34. Kallmeyer J, Ferdelman TG, Weber A, Fossing H, Jørgensen BB (2004) A cold chromium distillation procedure for radiolabeled sulfide applied to sulfate reduction measurements. Limnol Oceanogr-Meth 2:171–180CrossRefGoogle Scholar
  35. Kane MD, Poulsen LK, Stahl DA (1993) Monitoring the enrichment and isolation of sulfate-reducing bacteria by using oligonucleotide hybridization probes designed from environmentally derived 16S rRNA sequences. Appl Environ Microbiol 59:682–686CrossRefGoogle Scholar
  36. Kasai Y, Kishira H, Harayama S (2002) Bacteria belonging to the genus Cycloclasticus play a primary role in the degradation of aromatic hydrocarbons released in a marine environment. Appl Environ Microbiol 68:5625–5633CrossRefGoogle Scholar
  37. Kerger BD, Nichols PD, Antworth CP, Sand W, Bock E, Cox JC, Langworthy TA, White DC (1986) Signature fatty acids in the polar lipids of acid-producing Thiobacillus spp.: methoxy, cyclopropyl, alpha-hydroxy-cyclopropyl and branched and normal monoenoic fatty acids. FEMS Microbiol Lett 38:67–77CrossRefGoogle Scholar
  38. 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
  39. Kleindienst S, Herbst FA, 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
  40. 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
  41. Könneke M, Bernhard A, De la Torre J, Walker C, Waterbury J, Stahl D (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546CrossRefGoogle Scholar
  42. Kvenvolden KA, Cooper CK (2003) Natural seepage of crude oil into the marine environment. Geo Mar Lett 23:140–146CrossRefGoogle Scholar
  43. Larkin J, Henk MC, Aharon P (1994) Beggiatoa in microbial mats at hydrocarbon vents in the Gulf of Mexico and Warm Mineral Springs, Florida. Geo Mar Lett 14:97–103CrossRefGoogle Scholar
  44. 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
  45. Laso-Pérez R, Hahn C, van Vliet DM, Tegetmeyer HE, Schubotz F, Smit NT, Pape T, Sahling H, Bohrmann G, Boetius A (2019) Anaerobic degradation of non-methane alkanes by “Candidatus Methanoliparia” in hydrocarbon seeps of the Gulf of Mexico. MBio 10:e01814–01819Google Scholar
  46. Lin Q, Mendelssohn IA (2012) Impacts and recovery of the Deepwater Horizon oil spill on vegetation structure and function of coastal salt marshes in the northern Gulf of Mexico. Environ Sci Technol 46:3737–3743CrossRefGoogle Scholar
  47. 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
  48. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar N, Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann 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 Res 32:1363–1371CrossRefGoogle Scholar
  49. Luter HM, Whalan S, Webster NS (2010) Exploring the role of microorganisms in the disease-like syndrome affecting the sponge Ianthella basta. Appl Environ Microbiol 76:5736–5744CrossRefGoogle Scholar
  50. MacDonald IR, Reilly Jr JE, Best SE, Venkataramaiah R, Sassen R, Guinasso Jr NL, Amos J (1996) Remote sensing inventory of active oil seeps and chemosynthetic communities in the northern Gulf of Mexico. In: Hydrocarbon Migration and Its Near-surface Expression: Outgrowth of the Aapg Hedberg Research Conference, Vancouver, British Columbia, April 24–28, 1994. American Association of Petroleum Geologists, p 27Google Scholar
  51. MacDonald IR, Leifer I, Sassen R, Stine P, Mitchell R, Guinasso N (2002) Transfer of hydrocarbons from natural seeps to the water column and atmosphere. Geofluids 2:95–107CrossRefGoogle Scholar
  52. MacDonald IR, Bohrmann G, Escobar E, Abegg F, Blanchon P, Blinova V, Bruckmann W, Drews M, Eisenhauer A, Han X, Heeschen K, Meier F, Mortera C, Naehr T, Orcutt B, Bernard B, Brooks J, de Farago M (2004) Asphalt volcanism and chemosynthetic life in the Campeche Knolls, Gulf of Mexico. Science 304:999–1002CrossRefGoogle Scholar
  53. Magoon LB, Hudson TL, Cook HE (2001) AAPG Memoir 75, Chapter 4: Pimienta-tamabra—a giant supercharged petroleum system in the Southern Gulf of Mexico. Onshore and Offshore Mexico, pp 83–125Google Scholar
  54. Marcon Y, Sahling H, MacDonald IR, Wintersteller P, dos Santos Ferreira C, Bohrmann G (2018) Slow volcanoes: the intriguing similarities between marine asphalt and basalt lavas. Oceanography 31(2):194–205CrossRefGoogle Scholar
  55. Massana R, Murray AE, Preston CM, DeLong EF (1997) Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl Environ Microbiol 63:50–56CrossRefGoogle Scholar
  56. 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
  57. Muyzer G, Teske A, Wirsen CO, Jannasch HW (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164:165–172CrossRefGoogle Scholar
  58. Nelson K, Fisher C (2000) Absence of cospeciation in deep-sea vestimentiferan tube worms and their bacterial endosymbionts. Symbiosis 28:1–15Google Scholar
  59. Olajire A, Essien J (2014) Aerobic degradation of petroleum components by microbial consortia. J Petrol Environ Biotechnol 5:195CrossRefGoogle Scholar
  60. 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 II 57:2008–2021Google Scholar
  61. Orphan VJ, Hinrichs KU, 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
  62. Orphan VJ, House CH, Hinrichs KU, McKeegan KD, DeLong EF (2002) Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc Natl Acad Sci USA 99:7663–7668CrossRefGoogle Scholar
  63. Pape T, Hoffmann F, Quéric N-V, von Juterzenka K, Reitner J, Michaelis W (2006) Dense populations of Archaea associated with the demosponge Tentorium semisuberites Schmidt, 1870 from Arctic deep-waters. Polar Biol 29:662–667CrossRefGoogle Scholar
  64. Peters KE, Walters CC, Moldowan JM (2005) The biomarker guide. Cambridge University PressGoogle Scholar
  65. Raggi L, Schubotz F, Hinrichs KU, Dubilier N, Petersen JM (2013) Bacterial symbionts of Bathymodiolus mussels and Escarpia tubeworms from Chapopote, an asphalt seep in the southern Gulf of Mexico. Environ Microbiol 15:1969–1987CrossRefGoogle Scholar
  66. Rahn O (1906) Ein Paraffin zersetzender Schimmelpilz. Zentralbl Bakteriol Parasitenk Infekt II. Abt 16:382–384Google Scholar
  67. Rivers AR, Sharma S, Tringe SG, Martin J, Joye SB, Moran MA (2013) Transcriptional response of bathypelagic marine bacterioplankton to the Deepwater Horizon oil spill. ISME J 7:2315–2329CrossRefGoogle Scholar
  68. Rubin-Blum M, Antony CP, Borowski C, Sayavedra L, Pape T, Sahling H, Bohrmann G, Kleiner M, Redmond MC, Valentine DL (2017) Short-chain alkanes fuel mussel and sponge Cycloclasticus symbionts from deep-sea gas and oil seeps. Nat Microbiol 2:17093CrossRefGoogle Scholar
  69. Rütters H, Sass H, Cypionka H, Rullkötter J (2001) Monoalkylether phospholipids in the sulfate-reducing bacteria Desulfosarcina variabilis and Desulforhabdus amnigenus. Arch Microbiol 176:435–442CrossRefGoogle Scholar
  70. Sahling H, Borowski C, Escobar-Briones E, Gaytán-Caballero A, Hsu CW, Loher M, MacDonald IR, Marcon Y, Pape T, Römer M, Rubin-Blum M, Schubotz F, Smrzka D, Wegener G, Bohrmann G (2016) Massive asphalt deposits, oil seepage, and gas venting support abundant chemosynthetic communities at the Campeche Knolls, southern Gulf of Mexico. Biogeosciences 13:4491–4512CrossRefGoogle Scholar
  71. Salvador A (1991) Origin and development of the Gulf of Mexico Basin. In: Salvador A (ed) the Gulf of Mexico Basin, vol 2. Geology of North America, Decade of North American Geology, pp 389–444Google Scholar
  72. Schubotz F (2009) Microbical community characterization and carbon turnover in methane-rich environments—case studies in the Gulf of Mexico and Black Sea. Deparment of Geosciences. University Bremen, Bremen, Bremen, p 222Google Scholar
  73. Schubotz F, Lipp JS, Elvert M, Kasten S, Mollar XP, Zabel M, Bohrmann G, Hinrichs KU (2011a) Petroleum degradation and associated microbial signatures at the Chapopote asphalt volcano, Southern Gulf of Mexico. Geochim Cosmochim Acta 75:4377–4398CrossRefGoogle Scholar
  74. Schubotz F, Lipp JS, Elvert M, Hinrichs KU (2011b) Stable carbon isotopic compositions of intact polar lipids reveal complex carbon flow patterns among hydrocarbon degrading microbial communities at the Chapopote asphalt volcano. Geochim Cosmochim Acta 75:4399–4415CrossRefGoogle Scholar
  75. Söhngen N (1906) Über Bakterien, welche Methan als Kohlenstoffnahrung und Energiequelle gebrauchen. Zentrabl Bakteriol Parasitenk Infektionskr 15:513–517Google Scholar
  76. Sommer S, Linke P, Pfannkuche O, Niemann H, Treude T (2010) Benthic respiration in a seep habitat dominated by dense beds of ampharetid polychaetes at the Hikurangi Margin (New Zealand). Mar Geol 272:223–232CrossRefGoogle Scholar
  77. Speight JG (1999) The chemical and physical structure of petroleum: effects on recovery operations. J Petrol Sci Eng 22:3–15CrossRefGoogle Scholar
  78. Summons RE, Jahnke LL, Roksandic Z (1994) Carbon isotopic fractionation in lipids from methanotrophic bacteria: relevance for interpretation of the geochemical record of biomarkers. Geochim Cosmochim Acta 58:2853–2863CrossRefGoogle Scholar
  79. Teske A, Ramsing NB, Habicht K, Fukui M, Küver J, Jørgensen BB, Cohen Y (1998) Sulfate-reducing bacteria and their activities in cyanobacterial mats of Solar Lake (Sinai, Egypt). Appl Environ Microbiol 64:2943–2951CrossRefGoogle Scholar
  80. Teske A, Hinrichs KU, 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 68:1994–2007CrossRefGoogle Scholar
  81. Treude T, Boetius A, Knittel K, Wallmann K, Jørgensen BB (2003) Anaerobic oxidation of methane above gas hydrates at Hydrate Ridge, NE Pacific Ocean. Mar Ecol Prog Ser 264:1–14CrossRefGoogle Scholar
  82. Van Beilen J, Li Z, Duetz W, Smits T, Witholt B (2003) Diversity of alkane hydroxylase systems in the environment. Oil Gas Sci Technol 58:427–440CrossRefGoogle Scholar
  83. Van Dover CL, Fry B (1994) Microorganisms as food resources at deep-sea hydrothermal vents. Limnol Oceanogr 39:51–57CrossRefGoogle Scholar
  84. Watanabe K (2001) Microorganisms relevant to bioremediation. Curr Opin Biotech 12:237–241CrossRefGoogle Scholar
  85. Watkins JS, Ladd JW, Buffler RT, Shaub FJ, Houston M, Worzel JL (1978) Occurrence and evolution of salt in deep Gulf of Mexico. Framework, facies, and oil-trapping characteristics of the upper continental margin. AAPG Studies in Geology 7:43–65Google Scholar
  86. 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
  87. Wenzhöfer F, Glud RN (2002) Benthic carbon mineralization in the Atlantic: a synthesis based on in situ data from the last decade. Deep-Sea Res I 49:1255–1279CrossRefGoogle Scholar
  88. Widdel F, Rabus R (2001) Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr Opin Biotech 12:259–276CrossRefGoogle Scholar
  89. Zengler K, Richnow HH, Rossello-Mora R, Michaelis W, Widdel F (1999) Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 401:266–269CrossRefGoogle Scholar
  90. Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Max Planck Institute for Marine MicrobiologyBremenGermany
  2. 2.MARUM, Center for Marine Environmental Sciences and Department of Geosciences of the University of BremenBremenGermany

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