Seafloor oxygen consumption fuelled by methane from cold seeps

Nature Geoscience

Volumn 6, Issue 9, 2013, Pages 725-734

  Boetius, Antje ^a,b,c   Wenzhöfer, Frank ^a,b  

^a ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^b MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^c UNIVERSITY OF BREMEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COLD SEEP; CONTINENTAL SLOPE; FLUID FLOW; HYDROTHERMAL VENT COMMUNITY; METHANE; OXYGEN; SEAFLOOR;

ANIMALIA;

EID: 84883315635     PISSN: 17520894     EISSN: 17520908     Source Type: Journal    
DOI: 10.1038/ngeo1926     Document Type: Review

References (100)

1. Ryan, P. R. (ed.) Deep-sea hot springs and cold seeps. Oceanus 27, 32-33 (1984).
2. Levin, L. A. Ecology of cold seep sediments: interactions of fauna with flow, chemistry and microbes. Oceanogr. Mar. Biol. 43, 1-46 (2005).
3. Dubilier, N., Bergin, C. & Lott, C. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nature Rev. Microbiol. 6, 725-740 (2008).
4. Paull, C. K. et al. Biological communities at the Florida Escarpment resemble hydrothermal vent taxa. Science 226, 965-967 (1984).
5. Suess, E. et al. Biological communities at vent sites along the subduction zone off Oregon. Biol. Soc. Wash. Bull. 6, 475-484 (1985).
6. Levin, L. A. & Sibuet, M. Understanding continental margin biodiversity: a new imperative. Annu. Rev. Mar. Sci. 4, 79-112 (2012).
7. Kvenvolden K. & Rogers B. Gaia's breath: global methane exhalations. Mar. Petrol. Geol. 22, 579-590 (2005).
8. Judd, A. G., Hovland, M., Dimitrov, L. I., Garcia-Gil, S. & Jukes, V. The geological methane budget at continental margins and its influence on climate change. Geofluids 2, 109-126 (2002).
9. Suess, E. in Handbook of Hydrocarbon and Lipid Microbiology (ed. Timmis, K. N.) 188-203 (Springer-Verlag, 2010).
10. Wallmann, K. et al. The global inventory of methane hydrate in marine sediments: a theoretical approach. Energies 5, 2449-2498 (2012).
11. Buffett, B. & Archer, D. Global inventory of methane clathrate: sensitivity to changes in the deep ocean. Earth Planet. Sci. Lett. 227, 185-199 (2004).
12. Judd, A. G. & Hovland, M. Seabed fluid flow: the impact of geology, biology and the marine environment (Cambridge Univ. Press, 2007).
13. Foucher, J. P. et al. Structure and drivers of cold seep ecosystems. Oceanography 22, 92-109 (2009).
14. Milkov, A. V., Sassen, R., Apanasovich, T. V. & Dadashev F. G. Global gas flux from mud volcanoes: a significant source of fossil methane in the atmosphere and the ocean. Geophys. Res. Lett. 30, 1037 (2003).
15. Jenkins R. G. in Encyclopedia of Geobiology (eds Thiel, V. & Reitner, J.) 278-288 (Springer, 2011).
16. Mascle J. et al. Morphostructure of the Egyptian continental margin: insights from swath bathymetry surveys. Mar. Geophys. Res. 27, 49-59 (2006).
17. Bohrmann, G. et al. Mud volcanoes and gas hydrates in the Black Sea: new data from Dvurechnskii and Odessa mud volcanoes. Geo-Mar. Lett. 23, 239-49 (2003).
18. Fisher, C., Roberts, H., Cordes, E. & Bernard, B. Cold seeps and associated communities of the Gulf of Mexico. Oceanography 20, 119-129 (2007).
19. Brothers, L. L. et al. Evidence for extensive methane venting on the southeastern US Atlantic margin. Geology 41, 807-810 (2013).
20. Archer, D. E. & Buffett, B. A. A two-dimensional model of the methane cycle in a sedimentary accretionary wedge. Biogeosciences 9, 3323-3336 (2012).
21. Archer, D. E., Buffett, B. A. & McGuire, P. C. A two-dimensional model of the passive coastal margin deep sedimentary carbon and methane cycles. Biogeosciences 9, 2859-2878 (2012).
22. Cicerone, R. J. & Oremland R. S. Biogeochemical aspects of atmospheric methane. Glob. Biogeochem. Cycles 2, 299-327 (1988).
23. Dickens, G. R. Rethinking the global carbon cycle with a large, dynamic and microbially mediated gas hydrate capacitor. Earth Planet. Sci. Lett. 213, 169-183 (2003).
24. Reeburgh, W. S. Oceanic methane biogeochemistry. Chem. Rev. 107, 486-513 (2007).
25. Camilli, R. et al. Tracking hydrocarbon plume transport and biodegradation at Deepwater Horizon. Science 330, 201-204 (2010).
26. Joye, S. B., MacDonald, I. R., Leifer, I. & Asper, V. Magnitude and oxidation potential of hydrocarbon gases released from the BP oil well blowout. Nature Geosci. 4, 160-164 (2011).
27. Tryon, M. D. & Brown, K. M. Complex flow patterns through Hydrate Ridge and their impact on seep biota. Geophys. Res. Lett. 28, 2863-2866 (2001).
28. Leifer, I. & Patro, R. K. The bubble mechanism for methane transport from the shallow sea bed to the surface: a review and sensitivity study. Cont. Shelf Res. 22, 2409-2428 (2002).
29. Leifer, I., Luyendyk, B. P., Boles, J. & Clark, J. F. Natural marine seepage blowout: contribution to atmospheric methane. Glob. Biogeochem. Cycles 20, GB3008 (2006).
30. Nikolovska, A., Sahling, H. & Bohrmann, G. Hydroacoustic methodology for detection, localization, and quantification of gas bubbles rising from the seafloor at gas seeps from the eastern Black Sea. Geochem. Geophys. Geosyst. 9, Q10010 (2008).
31. Römer, M., Sahling, H., Pape, T., Bohrmann, G. & Spie, V. Quantification of gas bubble emissions from submarine hydrocarbon seeps at the Makran continental margin (offshore Pakistan). J. Geophys. Res. 117, C10015 (2012).
32. Linke, P. et al. In situ measurement of fluid flow from cold seeps at active continental margins. Deep-Sea Res. I, 41, 721-739 (1994).
33. Linke, P., Wallmann, K., Suess, E., Hensen, C. & Rehder, G. In situ benthic fluxes from an intermittently active mud volcano at the Costa Rica convergent margin. Earth Planet. Sci. Lett. 235, 79-95 (2005).
34. Tryon, M., Brown, K., Dorman, L. R. & Sauter A. A new benthic aqueous flux meter for very low to moderate discharge rates. Deep-Sea Res. I 48, 2121-2146 (2001).
35. Torres, M. E. et al. Fluid and chemical fluxes in and out of sediments hosting methane hydrate deposits on Hydrate Ridge, OR. I: Hydrological provinces. Earth Planet. Sci. Lett. 201, 525-540 (2002).
36. Sommer, S., Turk, M., Kriwanek, S. & Pfannkuche, O. Gas exchange system for extended in situ benthic chamber flux measurements under controlled oxygen conditions: first application-sea bed methane emission measurements at Captain Arutyunov mud volcano. Limnol. Oceanogr.-Meth 6, 23-33 (2008).
37. Wankel, S. D. et al. New constraints on methane fluxes and rates of anaerobic methane oxidation in a Gulf of Mexico brine pool via in situ mass spectrometry. Deep-Sea Res. II 57, 2022-2029 (2010).
38. Valentine, D. Emerging topics in marine methane biogeochemistry. Annu. Rev. Mar. Sci. 3, 147-171 (2010).
39. Hinrichs, K. U. & Boetius, A. in Ocean Margin Systems (eds Wefer, G. et al.) 457-477 (Springer Berlin, 2002).
40. Niemann, H. et al. Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink. Nature 443, 854-858 (2006).
41. Sommer, S. et al. Efficiency of the benthic filter: biological control of the emission of dissolved methane from sediments containing shallow gas hydrates at Hydrate Ridge. Glob. Biogeochem. Cycles 20, GB2019 (2006).
42. Regnier, P. et al. Quantitative analysis of anaerobic oxidation of methane (AOM) in marine sediments: a modeling perspective. Earth Sci. Rev. 106, 105-130 (2011).
43. de Beer, D. et al. In situ fluxes and zonation of microbial activity in surface sediments of the Håkon Mosby mud volcano. Limnol. Oceanogr. 51, 1315-1331 (2006).
44. Caprais, J-C. et al. A new CALMAR benthic chamber operating by submersible: first application in the cold-seep environment of Napoli mud volcano (Mediterranean Sea) Limnol. Oceanogr.-Meth. 8, 304-312 (2010).
45. Jahnke, R. A. The global ocean flux of particulate organic carbon: areal distribution and magnitude. Glob. Biogeochem. Cycles 10, 71-88 (1996).
46. Glud, R. N. Oxygen dynamics of marine sediments. Mar. Biol. Res. 4, 243-289 (2008).
47. Suess, E. et al. Gas hydrate destabilization: enhanced dewatering, benthic material turnover and large methane plumes at the Cascadia convergent margin. Earth Planet. Sci. Lett. 170, 1-15 (1999).
48. Sommer, S. et al. Seabed methane emissions and the habitat of frenulate tubeworms on the Captain Arutyunov mud volcano (Gulf of Cadiz). Mar. Ecol. Prog. Ser. 382, 69-86 (2009).
49. Felden, J., Wenzhöfer, F., Feseker, T. & Boetius, A. Transport and consumption of oxygen and methane in different habitats of the Håkon Mosby mud volcano (HMMV). Limnol. Oceanogr. 55, 2366-2380 (2010).
50. Decker, C., Caprais, J-C., Khripounoff, A. & Olu, K. First respiration estimates of cold-seep vesicomyid bivalves from in situ total oxygen uptake measurements. C. R. Biol. 335, 261-270 (2012).
51. Hourdez, S. & Lallier, F. Adaptations to hypoxia in hydrothermal-vent and cold-seep invertebrates. Rev. Environ. Sci. Biotechnol. 6, 143-159 (2007).
52. Cordes, E. E., Arthur, M. A., Shea, K., Arvidson, R. S. & Fisher, C. R. Modeling the mutualistic interactions between tubeworms and microbial consortia. PLoS Biol. 3, e77 (2005).
53. Sommer, S., Linke, P., Pfannkuche, O., Niemann, H. & Treude, T. Benthic respiration in a seep habitat dominated by dense beds of ampharetid polychaetes at the Hikurangi Margin (New Zealand). Mar. Geol. 272, 223-232 (2010).
54. Soetaert, K. et al. Modelling the impact of siboglinids on the biogeochemistry of the Captain Arutyunov mud volcano (Gulf of Cadiz). Biogeosciences 9, 5341-5352 (2012).
55. Ruff, E. et al. Microbial communities of deep sea methane seeps at Hikurangi continental margin (New Zealand). Plos ONE http://dx.doi.org/10.1371/ journal.pone.0072627 (in the press).
56. Dale, A. et al. Pathways and regulation of carbon, sulfur and energy transfer in marine sediments overlying methane gas hydrates on the Opouawe Bank (New Zealand) Geochim. Cosmochim. Acta 74, 5763-5784 (2010).
57. Barry, J. P., Kochevar, R. E. & Baxter, C. H. The influence of pore-water chemistry and physiology on the distribution of vesicomyid clams at cold seeps in Monterey Bay: implications for patterns of chemosynthetic community organization. Limnol. Oceanogr. 42, 318-328 (1997).
58. Sibuet, M. & Olu, K. Biogeography, biodiversity and fluid dependence of deep-sea cold-seep communities at active and passive margins. Deep-Sea Res. II 45, 517-567 (1998).
59. Goffredi, S. K. & Barry, J. P. Species-specific variation in sulphide physiology between closely related vesicomyid clams. Mar. Ecol. Prog. Ser. 225, 227-238 (2002).
60. Levin, L. A., Whitcraft, C. R., Mendoza, G. F., Gonzalez, J. P. & Cowie, G. Oxygen and organic matter thresholds for benthic faunal activity on the Pakistan margin oxygen minimum zone (700-1100 m). Deep-Sea Res. II 56, 449-71 (2009).
61. Felden, J. et al. Limitations of microbial hydrocarbon degradation at the Amon mud volcano (Nile deep sea fan). Biogeosciences 10, 3269-3283 (2013).
62. Grünke, S. et al. Niche differentiation among mat-forming, sulfide-oxidizing bacteria at cold seeps of the Nile deep sea fan (eastern Mediterranean Sea). Geobiology 9, 330-348 (2011).
63. Fischer, D. et al. Interaction between hydrocarbon seepage, chemosynthetic communities, and bottom water redox at cold seeps of the Makran accretionary prism: insights from habitat-specific pore water sampling and modeling. Biogeosciences 9, 2013-2031 (2012).
64. Tavormina, P. L., Ussler, W. & Orphan, V. J. Planktonic and sediment-associated aerobic methanotrophs in two seep systems along the North American margin. Appl. Environ. Microbiol. 74, 3985-3995 (2008).
65. Knittel, K. & Boetius, A. Anaerobic oxidation of methane: progress with an unknown process. Annu. Rev. Microbiol. 63, 311-334 (2009).
66. Haroon, M. et al. Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature http://dx.doi.org/10.1038/ nature12375 (2013).
67. Ettwig, K. F. et al. Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464, 543-548 (2010).
68. Beal, E. J., House, C. H. & Orphan, V. J. Manganese-and iron-dependent marine methane oxidation. Science 325, 184-187 (2009).
69. Pop Ristova, P. et al. Bacterial diversity and biogeochemistry of different chemosynthetic habitats of the REGAB cold seep (West African margin, 3160 m water depth). Biogeosciences 9, 5031-5048 (2012).
70. Luff, R. & Wallmann, K. Fluid flow, methane fluxes, carbonate precipitation and biogeochemical turnover in gas hydrate-bearing sediments at Hydrate Ridge, Cascadia Margin: numerical modeling and mass balances. Geochim. Cosmochim. Acta 67, 3403-3421 (2003).
71. Boetius, A. et al. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407, 623-626 (2000).
72. Orphan, V. J., House, C. H., Hinrichs, K-U., McKeegan, K. D. & DeLong, E. F. Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293, 484-87 (2001).
73. Milucka, J. et al. Zero-valent sulphur is a key intermediate in marine methane oxidation. Nature 491, 541-546 (2012).
74. Reeburgh, W. S. Anaerobic methane oxidation: rate depth distributions in Skan Bay sediments. Earth Planet. Sci. Lett. 7, 269-298 (1980).
75. Jørgensen, B. B. & Kasten, S. in Marine Geochemistry (eds Zabel, M. & Schulz, H.) 271-309 (Springer, 2006).
76. Meister, P., Liu, B., Ferdelman, T., Jørgensen, B. B. & Khalili, A. Control of sulphate and methane distributions in marine sediments by organic matter reactivity. Geochim. Cosmochim. Acta 104, 183-193 (2013).
77. Borowski, W. S., Paull, C. K. & Ussler, W. III Global and local variations of interstitial sulfate gradients in deep-water, continental margin sediments: sensitivity to underlying methane and gas hydrates. Mar. Geol. 159, 131-154 (1999).
78. Seiter, K., Hensen, C., Schröter, J. & Zabel, M. Organic carbon content in surface sediments: defining regional provinces. Deep-Sea Res. I 51, 2001-2026 (2004).
79. Treude, T., Boetius, A., Knittel, K., Wallmann, K. & Jørgensen, B. B. Anaerobic oxidation of methane above gas hydrates at Hydrate Ridge, NE Pacific Ocean. Mar. Ecol. Prog. Ser. 264, 1-14 (2003).
80. Boetius, A. & Suess, E. Hydrate Ridge: a natural laboratory for the study of microbial life fueled by methane from near-surface gas hydrates. Chem. Geol. 205, 291-310 (2004).
81. Pohlmann, J. W., Bauer, J. E., Waite, W. F., Osburn, C. L. & Chapman N. R. Methane hydrate-bearing seeps as a source of aged dissolved organic carbon to the oceans. Nature Geosci. 4, 37-41 (2011).
82. Lösekann, T. et al. Endosymbioses between bacteria and deep-sea siboglinid tubeworms from an Arctic cold seep (Haakon Mosby mud volcano, Barents Sea). Environ. Microbiol. 10, 3237-3254 (2008).
83. Lichtschlag, A., Felden, J., Brüchert, V., Boetius, A. & deBeer, D. Geochemical processes and chemosynthetic primary production in different thiotrophic mats of the Håkon Mosby mud volcano (Barents Sea). Limnol. Oceanogr. 55, 931-949 (2010).
84. Greinert, J., Artemov, Y., Egorov, V., DeBatist, M. & McGinnis, D. 1300-m high rising bubbles from mud volcanoes at 2080 m in the Black Sea: hydroacoustic characteristics and temporal variability. Earth Planet. Sci. Lett. 244, 1-15 (2006).
85. Greinert, J. et al. Methane seepage along the Hikurangi Margin, New Zealand: overview of studies in 2006 and 2007 and new evidence from visual, bathymetric and hydroacoustic investigations. Mar. Geol. 272, 6-25 (2010).
86. Burdige, D. J. Preservation of organic matter in marine sediments: controls, mechanisms, and an imbalance in sediment organic carbon budgets Chem. Rev. 107, 467-485 (2007).
87. Hedges, J. I. & Keil, R. G. Sedimentary organic matter preservation an assessment and speculative synthesis. Mar. Chem. 49, 81-115 (1995).
88. Jørgensen, B. B. & Boetius, A. Feast and famine: microbial life in the deep-sea bed. Nature Rev. Microbiol. 5, 770-781 (2007).
89. Horsfield, B. et al. Living microbial ecosystems within the active zone of catagenesis: implications for feeding the deep biosphere. Earth Planet. Sci. Lett. 246, 55-69 (2006).
90. Parkes, R. J. et al. Temperature activation of organic matter and minerals during burial has the potential to sustain the deep biosphere over geological timescales. Org. Geochem. 38, 845-852 (2007).
91. Takai, K. et al. Cell proliferation at 122 °C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc. Natl Acad. Sci. USA 105, 10949-10954 (2008).
92. Lipp, J. S., Morono, Y., Inagaki, F. & Hinrichs, K-U. Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 454, 991-994 (2008).
93. Middelburg, J. J. A simple model for organic matter decomposition in marine sediments. Geochim. Cosmochim. Acta 53, 1577-1581 (1989).
94. Joye, S. B. et al. The anaerobic oxidation of methane and sulfate reduction in sediments from Gulf of Mexico cold seeps. Chem. Geol. 205, 219-238 (2004).
95. Suess, E. et al. Fluid venting in the eastern Aleutian subduction zone. J. Geophys. Res. 103, 2597-2614 (1998).
96. Pop-Ristova, P. Biogeochemical Activity and Associated Biodiversity at Reduced Deep-Sea Hotspot Ecosystems PhD thesis, Univ. Bremen (2012).
97. Ritt, B. et al. Diversity and distribution of cold-seep fauna associated with different geological and environmental settings at mud volcanoes and pockmarks of the Nile deep-sea fan. Mar. Biol. 158, 1187-1210 (2011).
98. Loncke, L., Mascle, J. & Parties, F. S. Mud volcanoes, gas chimneys, pockmarks and mounds in the Nile deep-sea fan (eastern Mediterranean): geophysical evidences. Mar. Petrol. Geol. 21, 669-689 (2004).
99. Wenzhöfer, F. & Glud, R. N. Benthic carbon mineralization in the Atlantic: a synthesis based on in situ data from the last decade. Deep-Sea Res. I 49, 1255-1279 (2002).
100. Grunke, S. et al. Mats of psychrophilic thiotrophic bacteria associated with cold seeps of the Barents Sea. Biogeosciences 9, 2947-2960 (2012).