Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Feast and famine — microbial life in the deep-sea bed

Key Points

  • The seabed is a highly diverse and dynamic environment that ranges from the desert-like deep-sea floor to the rich oases at cold seeps, hydrothermal vents and large food falls.

  • As well as the sedimentation of organic material from above, plate tectonics and other geological processes transport chemical energy to the seafloor from below, which provides a significant fraction of the deep-sea energy flux.

  • Where chemical energy, such as hydrogen sulphide, methane or hydrogen, is transported from the subsurface up to the seafloor, rich and diverse microbial communities can proliferate.

  • Most of the prokaryotes on Earth can be found in the sub-seafloor and survive in conditions of extreme energy limitation, with apparent generation times of up to thousands of years.

  • In the most energy-depleted deep biosphere, life might be based on the cleavage of water by natural radioisotopes or on other, unknown energy sources.

  • The only environmental variable that appears to set the ultimate limit for life in the seabed is temperature.

  • The diversity and distribution of the three domains of life — Bacteria, Archaea and Eukaryotes — in the seabed remain poorly understood.

Abstract

The seabed is a diverse environment that ranges from the desert-like deep seafloor to the rich oases that are present at seeps, vents, and food falls such as whales, wood or kelp. As well as the sedimentation of organic material from above, geological processes transport chemical energy — hydrogen, methane, hydrogen sulphide and iron — to the seafloor from the subsurface below, which provides a significant proportion of the deep-sea energy. At the sites on the seafloor where chemical energy is delivered, rich and diverse microbial communities thrive. However, most subsurface microorganisms live in conditions of extreme energy limitation, with mean generation times of up to thousands of years. Even in the most remote subsurface habitats, temperature rather than energy seems to set the ultimate limit for life, and in the deep biosphere, where energy is most depleted, life might even be based on the cleavage of water by natural radioisotopes. Here, we review microbial biodiversity and function in these intriguing environments.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Vertical section of the seabed and seafloor structures.
Figure 2: Global trends of microbial biomass in the ocean and seabed.
Figure 3: Microbial life at seep ecosystems.

References

  1. Zobell, C. E. & Morita, R. Y. in Galathea Report Vol. 1 139–154 (Danish Science, Copenhagen, 1959).

    Google Scholar 

  2. Corliss, J. B. et al. Submarine thermal springs on the Galapagos Rift. Science 203, 1073–1083 (1979).

    CAS  Article  PubMed  Google Scholar 

  3. 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).

    Article  Google Scholar 

  4. Froelich, P. N. et al. Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis. Geochim. Cosmochim. Acta 43, 1075–1090 (1979).

    CAS  Article  Google Scholar 

  5. Jahnke, R. A. & Jackson, G. A. in Deep-Sea Food Chains and the Global Carbon Cycle (eds Rowe, G. T. & Pariente, V.) 295–308 (Kluwer Academic, Dordrecht, 1992).

    Book  Google Scholar 

  6. Mayer, L. in Organic Geochemistry: Principles and Applications (eds Engel, M. H. & Macko, S.) 171–184 (Plenum, New York, 1993).

    Book  Google Scholar 

  7. Hedges, J. I. & Keil, R. G. Sedimentary organic matter preservation: an assessment and speculative synthesis. Mar. Chem. 49, 81–115 (1995).

    CAS  Article  Google Scholar 

  8. Deming, J. W. & Baross J. A. in Organic Geochemistry (eds Engel, M. H. & Macko, S. A.) 119–144 (Plenum, New York, 1993).

    Book  Google Scholar 

  9. Smith, C. R. et al. Latitudinal variations in benthic processes in the abyssal equatorial Pacific: control by biogenic particle flux. Deep-Sea Res. II 44, 2295–2317 (1997).

    CAS  Article  Google Scholar 

  10. Boetius, A. & Damm, E. Benthic oxygen uptake, hydrolytic potentials and microbial biomass at the Arctic continental slope. Deep-Sea Res. I 45, 239–275 (1998).

    Article  Google Scholar 

  11. Deming, J. W. & Yager, P. L. in Deep-Sea Food Chains and the Global Carbon Cycle (eds Rowe, G. T. & Pariente, V.) 11–28 (Kluwer Academic, Dordrecht, 1992). Together with reference 12, this reference was important for the understanding of global patterns in microbial biomass and activity in deep-sea sediments.

    Book  Google Scholar 

  12. Lochte, K. in Deep-Sea Food Chains and the Global Carbon Cycle (eds Rowe, G. T. & Pariente, V.) 1–10 (Kluwer Academic, Dordrecht, 1992).

    Book  Google Scholar 

  13. Lochte, K. & Turley, C. M. Bacteria and cyanobacteria associated with phytodetritus in the deep-sea. Nature 333, 67–69 (1988).

    Article  Google Scholar 

  14. Turley, C. M. & Lochte, K. Microbial response to the input of fresh detritus to the deep-sea bed. Palaeogeogr. Palaeoclimatol. Palaeoecol. 89, 3–23 (1990). This paper was one of the first to provide a quantification of the microbial turnover of phytodetritus at the seafloor and showed that deep-sea microorganisms can be as active as other microorganisms despite cold temperatures and high pressures.

    Article  Google Scholar 

  15. Moodley, L. et al. Bacteria and Foraminifera: key players in a short-term deep-sea benthic response to phytodetritus. Mar. Ecol. Prog. Ser 236, 23–29 (2002).

    Article  Google Scholar 

  16. Witte U. et al. In situ experimental evidence of the fate of a phytodetritus pulse at the abyssal seafloor. Nature 424, 763–766 (2003).

    CAS  Article  PubMed  Google Scholar 

  17. Vetter, Y. A. & Deming, J. Extracellular enzyme activity in the Arctic Northeast Water polynya. Mar. Ecol. Prog. Ser 114, 23–34 (1994).

    CAS  Article  Google Scholar 

  18. Boetius, A. & Lochte, K. Regulation of microbial enzymatic degradation of OM in deep-sea sediments. Mar. Ecol. Prog. Ser 104, 299–307 (1994).

    CAS  Article  Google Scholar 

  19. 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).

    CAS  Article  PubMed  Google Scholar 

  20. DeLong, E. F., Franks, D. G. & Yayanos A. A. Evolutionary relationships of cultivated psychrophilic and barophilic deep-sea bacteria. Appl. Environ. Microbiol. 63, 2105–2108 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Vetriani, C., Jannasch, H. W., MacGregor, B. J., Stahl, D. A. & Reysenbach, A. L. Population structure and phylogenetic characterization of marine benthic archaea in deep-sea sediments. Appl. Environ. Microbiol. 65, 4375–4384 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Inagaki, F. et al. Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin. Proc. Natl Acad. Sci. USA 103, 2815–2820 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Biddle, J. F. et al. Heterotrophic archaea dominate sedimentary subsurface ecosystems off Peru. Proc. Natl Acad. Sci. USA 103, 3846–3851 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Middelboe, M., Glud, R. N., Wenzhöfer, F., Oguri, K., Kitazato, H. Spatial distribution and activity of viruses in the deep-sea sediments of Sagami Bay, Japan. Deep-Sea Res. I 53, 1–13 (2006).

    Article  Google Scholar 

  25. Lonsdale, P. Clustering of suspension-feeding macrobenthos near abyssal hydrothermal vents at oceanic spreading centers. Deep-Sea Res. 24, 857–863 (1977).

    Article  Google Scholar 

  26. Jones, M. L. Hydrothermal vents of the eastern Pacific: an overview. Bull. Biol. Soc. Wash. 6, 545 (1985).

    Google Scholar 

  27. Cavanaugh, C. M. Symbioses of chemoautotrophic bacteria and marine invertebrates from hydrothermal vents and reducing sediments. Bull. Biol. Soc. Wash. 6, 373–388 (1985).

    Google Scholar 

  28. Nelson, D. C., Wirsen, C. O. & Jannasch, H. W. Characterization of large autotrophic Beggiatoa abundant at hydrothermal vents of the Guaymas Basin. Appl. Environ. Microbiol. 55, 2909–2917 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Takai, K., Nakagawa, S., Reysenbach, A. L. & Hoek, J. in Back Arc Spreading Systems: Geological, Biological, Chemical and Physical Interactions (eds Christie, D. M. et al.) 185–214 (AGU Books, Washington DC, 2006). An important contribution to the documentation of the occurrence of uncultivated microorganisms at different hydrothermal vent systems.

    Book  Google Scholar 

  30. Tivey, M. Generation of seafloor hydrothermal vent fluids and associated mineral deposits. Oceanography 20, 50–65 (2007).

    Article  Google Scholar 

  31. Fisher, C. R., Takai, K. & Le Bris, N. Hydrothermal vent ecosystems. Oceanography 20, 14–23 (2007).

    Article  Google Scholar 

  32. Edwards, K. J., Bach, W. & McCollom, T. M. Geomicrobiology in oceanography: microbe–mineral interactions at and below the seafloor. Trends Microbiol. 13, 449–456 (2006).

    Article  CAS  Google Scholar 

  33. Von Damm, K. L. et al. Chemistry of submarine hydrothermal solutions at 21°N, East Pacific Rise. Geochim. Cosmochim. Acta 49, 2197–2220 (1985).

    CAS  Article  Google Scholar 

  34. Charlou, J. L. et al. Geochemistry of high H2 and CH4 vent fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36°14'N, MAR). Chem. Geol. 191, 345–359 (2002).

    CAS  Article  Google Scholar 

  35. Nealson, K. H., Inagaki, F. & Takai, K. Hydrogen-driven subsurface lithoautotrophic microbial ecosystems (SLiMEs): do they exist and why should we care? Trends Microbiol. 13, 405–410 (2005).

    CAS  Article  PubMed  Google Scholar 

  36. Kelley, D. S. et al. A serpentinite-hosted ecosystem: the lost city hydrothermal field. Science 307, 1428–1434 (2005).

    CAS  Article  PubMed  Google Scholar 

  37. Moyer, C. L., Tiedge, J. M., Dobbs, F. C. & Karl, D. M. Diversity of deep-sea hydrothermal vent Archaea from Loihi Seamount, Hawaii. Deep-Sea Res. II 45, 303–317 (1998).

    CAS  Article  Google Scholar 

  38. Emerson, D. & Moyer. C. L. Neutrophilic Fe-oxidizing bacteria are abundant at the Loihi Seamount hydrothermal vents and play a major role in Fe oxide deposition. Appl. Environ. Microbiol. 68, 3085–3093 (2002).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Inagaki, F. et al. Microbial community in a sediment-hosted CO2 lake of the southern Okinawa Trough hydrothermal system. Proc. Natl Acad. Sci. USA 103, 14164–14169 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Fisk, M. R., Giovannoni, S. J. & Thorseth, I. H. Alteration of oceanic volcanic glass: textural evidence of microbial activity. Science 281, 978–980 (1998).

    CAS  Article  PubMed  Google Scholar 

  41. Furnes, H. & Staudigel, H. Biological mediation in ocean crust alteration: how deep is the deep biosphere? Earth Planet. Sci. Lett. 166, 97–103 (1999).

    CAS  Article  Google Scholar 

  42. Thorseth, I. H. et al. Diversity of life in ocean floor basalt. Earth. Planet. Sci. Lett. 194, 31–37 (2001).

    CAS  Article  Google Scholar 

  43. Bach, W. & Edwards, K. J. Iron and sulfide oxidation within the basaltic ocean crust: implications for chemolithoautotrophic microbial biomass production. Geochim. Cosmochim. Acta 67, 3871–3887 (2003).

    CAS  Article  Google Scholar 

  44. Shock, E. L. & Holland M. E. Geochemical energy sources that support the subsurface biosphere. Geophysical Monograph 144, 469–525 (2004).

    Google Scholar 

  45. Blöchl, E. et al. Pyrolobus fumarii gen. and sp. nov., represents a novel group of archaea extending the upper temperature limit for life to 113°C. Extremophiles 1, 14–21 (1997).

    Article  PubMed  Google Scholar 

  46. Kashefi, K. & Lovely, D. R. Extending the upper temperature limit for life. Science 301, 934 (2003).

    CAS  Article  PubMed  Google Scholar 

  47. Reysenbach, A. L. et al. A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents. Nature 442, 444–447 (2006). A perfect example of the successful cultivation of vent-endemic environmentally relevant archaea based on their distribution, the metagenome and the geochemistry of their habitat.

    CAS  Article  PubMed  Google Scholar 

  48. Reysenbach, A. L., Longnecker, K. & Kirshtein, J. Novel bacterial and archaeal lineages from an in situ growth chamber deployed at a Mid-Atlantic ridge hydrothermal vent. Appl. Environ. Microbiol. 66, 3798–3806 (2000).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. Reysenbach, A. L. & Shock, E. L. Merging genomes with geochemistry in hydrothermal ecosystems. Science 296, 1077–1082 (2002).

    CAS  Article  PubMed  Google Scholar 

  50. Campbell, B., Engel, A. S., Porter, M. L. & Takai, K. The versatile ɛ-proteobacteria: key players in sulphidic habitats. Nature Rev. Microbiol. 4, 458–468 (2006).

    CAS  Article  Google Scholar 

  51. Bach, W. et al. Energy in the dark: fuel for life in the deep ocean and beyond. Eos (Washington DC) 87, 73–78 (2006).

    Google Scholar 

  52. Kennicutt, M. C. et al. Vent-type taxa in a hydrocarbon seep region on the Louisiana slope. Nature 317, 351–353 (1985).

    CAS  Article  Google Scholar 

  53. Suess, E. et al. Biological communities at vent sites along the subduction zone off Oregon. Bull. Biol. Soc. Wash. 6, 475–484 (1985).

    Google Scholar 

  54. Kulm, L. D. et al. Oregon subduction zone: venting, fauna, and carbonates. Science 231, 561–566 (1986).

    CAS  Article  PubMed  Google Scholar 

  55. Tryon, M. D. et al. Measurements of transience and downward fluid flow near episodic methane gas vents, Hydrate Ridge, Cascadia. Geology 27, 1075–1078 (1999).

    Article  Google Scholar 

  56. 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).

    CAS  Article  Google Scholar 

  57. 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). This paper combines geochemistry and molecular ecology in situ to provide a quantitative understanding of the environmental factors that control the microbial methane filter.

    CAS  Article  PubMed  Google Scholar 

  58. Orphan, V. J., Haffenbradl, D., Taylor, L. T. & Delong, E. F. Culture-dependent and culture-independent characterization of microbial assemblages associated with high temperature petroleum reservoirs. Appl. Environ. Microbiol. 66, 700–711 (2000).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  59. Widdel, F., Musat, F., Knittel, K. & Galushko, A. in Sulphate-Reducing Bacteria: Environmental and Engineered Systems. (eds Barton, L. L. & Hamilton, W. A.) 265–304 (Cambridge Univ. Press, Cambridge, 2007).

    Book  Google Scholar 

  60. Orphan, V. J., House, C. H., Hinrichs, K. U., McKeegan, K. D. & Delong, E. F. Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc. Natl Acad. Sci. USA 99, 7663–7668 (2002).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. Teske, A. et al. Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities. Appl. Environ. Microbiol. 68, 1994–2007 (2002).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  62. Knittel, K. et al. Activity, distribution, and diversity of sulfate reducers and other bacteria in sediments above gas hydrate (Cascadia Margin, Oregon). Geomicrobiol. J. 20, 269–294 (2003).

    CAS  Article  Google Scholar 

  63. Knittel, K., Lösekann, T., Boetius, A., Kort, R. & Amann, R. Diversity and distribution of methanotrophic archaea at cold seeps. Appl. Environ. Microbiol. 71, 467–479 (2005).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. Hinrichs, K. U. & Boetius, A. in Ocean Margin Systems (eds Wefer, G. et al.) 457–477 (Springer-Verlag, Berlin, 2002).

    Book  Google Scholar 

  65. Reeburgh, W. Oceanic methane biogeochemistry. Chem. Oceanogr. 107, 486–513 (2007).

    CAS  Google Scholar 

  66. Hinrichs, K. U., Hayes, J. M., Sylva, S. P., Brewer, P. G. & DeLong, E. F. Methane-consuming archaebacteria in marine sediments. Nature 398, 802–805 (1999). A classical example of how cultivation-independent molecular methods such as lipid biomarkers and 16S rDNA analyses can help to identify unknown microorganisms and their metabolisms. Also, this paper was the first to provide clues to the identity of anaerobic methanotrophs at seeps.

    CAS  Article  PubMed  Google Scholar 

  67. Boetius, A. et al. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407, 623–626 (2000).

    CAS  Article  PubMed  Google Scholar 

  68. Michaelis, W. et al. Microbial reefs in the Black Sea fueled by anaerobic oxidation of methane. Science 297, 1013–1015 (2002).

    CAS  Article  PubMed  Google Scholar 

  69. Valentine, D. L. & Reeburgh, W. S. New perspectives on anaerobic methane oxidation. Environ. Microbiol. 2, 477–484 (2000).

    CAS  Article  PubMed  Google Scholar 

  70. Ritger, S., Carson, B. & Suess, E. Methane-derived authigenic carbonates formed by subduction-induced pore-water expulsion along the Oregon/Washington margin. Geol. Soc. Am Bull. 98, 147–156 (1987).

    CAS  Article  Google Scholar 

  71. Levin, L. Ecology of cold seep ecosystems: interactions of fauna with flow, chemistry and microbes. Oceanogr. Mar. Biol. Annu. Rev. 43, 1–46 (2005).

    Google Scholar 

  72. MacDonald, I. R. et al. Gulf of Mexico chemosynthetic communities: II. Spatial distribution of seep organisms and hydrocarbons at Bush Hill. Mar. Biol. 101, 235–247 (1989).

    CAS  Article  Google Scholar 

  73. Fisher, C. R. Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev. Aquat. Sci. 2, 399–436 (1990).

    CAS  Google Scholar 

  74. 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).

    Article  Google Scholar 

  75. Sahling, H., Rickert, D., Lee, R. W., Linke, P. & Suess, E. Macrofaunal community structure and sulfide flux at gas hydrate deposits from the Cascadia convergent margin, NE Pacific. Mar. Ecol. Prog. Ser 231, 121–138 (2002).

    Article  Google Scholar 

  76. 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).

    CAS  Article  Google Scholar 

  77. MacDonald, I. R. et al. Asphalt volcanism and chemosynthetic life in the Campeche Knolls, Gulf of Mexico. Science 304, 999–102 (2004).

    CAS  Article  PubMed  Google Scholar 

  78. Treude, T. et al. Consumption of methane and CO2 by methanotrophic microbial mats from gas seeps of the anoxic Black Sea. Appl. Environ. Microbiol. 73, 2271–2283 (2007).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  79. Hovland, M. & Judd, A. G. Seabed Pockmarks and Seepages (Graham and Trotman, London, 1988).

    Google Scholar 

  80. Dupré, S. et al. Seafloor geological studies above active gas chimneys off Egypt (Central Nile Deep Sea Fan). Deep-Sea Res. I 54, 1146–1172 (2007).

    Article  Google Scholar 

  81. de Beer, D., Sauter, E., Niemann, H., Witte, U. & Boetius, A. In situ fluxes and zonation of microbial activity in surface sediments of the Håkon Mosby Mud Volcano. Limnol. Oceanogr. 51, 1315–1331 (2006).

    CAS  Article  Google Scholar 

  82. Treude, T., Boetius, A., Knittel, K., Wallmann, K. & Jørgensen, B. B. Anaerobic oxidation of methane above gas hydrates at Hydrate Ridge, NE Pacific. Mar. Ecol. Prog. Ser 264, 1–14 (2003).

    CAS  Article  Google Scholar 

  83. Kalanetra, K. M., Joye, S. B., Sunseri, N. R. & Nelson, D. C. Novel vacuolate sulfur bacteria from the Gulf of Mexico reproduce by reductive division in three dimensions. Environ. Microbiol. 7, 1451–1460 (2005).

    CAS  Article  PubMed  Google Scholar 

  84. Preisler, A. et al. Biological and chemical sulfide oxidation in a Beggiatoa inhabited sediment. ISME J. 1, 341–353 (2007).

    CAS  Article  PubMed  Google Scholar 

  85. Dickens, G. Rethinking the global carbon cycle with a large, dynamic and microbially mediated gas hydrate capacitor. Earth Planet. Sci. Lett. 213, 169–183 (2003).

    CAS  Article  Google Scholar 

  86. Oremland, R. S., Culbertson, C. & Simoneit, B. R. T. in Init. Repts. DSDP (eds Curray, J. R. et al.) 759–762 (United States Government Printing Office, Washington, 1982).

    Google Scholar 

  87. Cragg, B. A. et al. in Proc. Ocean Drilling Program Sci. (eds Suess, E. & von Huene, R.) Vol. 112, 607–619 (A&M University, Texas, 1990).

    Google Scholar 

  88. Parkes, R. J., Cragg, B. A. & Wellsbury, P. Recent studies on bacterial populations and processes in marine sediments: a review. Hydrogeol. J. 8, 11–28 (2000).

    Article  Google Scholar 

  89. Smith, D. C., Spivack, A. J., Fisk, M. R., Haveman, S. A. & Staudigel, H. Tracer-based estimates of drilling-induced microbial contamination of deep sea crust. Geomicrobiol. J. 17, 207–219 (2000).

    CAS  Article  Google Scholar 

  90. House, C. H., Cragg, B. A. & Teske, A. in Proc. Ocean Drilling Program, Init. Repts. (eds D'Hondt, S. L. et al.) Vol. 201, 1–19 (A&M University, Texas, 2003).

    Google Scholar 

  91. Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: the unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998). A key paper on the global abundance and biomass of prokaryotic cells, which showed their predominance in the deep biosphere.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  92. D' Hondt, S. L. et al. Metabolic activity of subsurface life in deep-sea sediments. Science 295, 2067–2070 (2002).

    CAS  Article  Google Scholar 

  93. D' Hondt, S. L. et al. (eds) in Proc. Ocean Drilling Program, Init. Repts. Vol. 201, 1–86 (Texas A&M University, Texas, 2003).

    Book  Google Scholar 

  94. D' Hondt, S. et al. Distributions of microbial activities in deep subseafloor sediments. Science 306, 2216–2221 (2004). An important overview of the data on microbial diversity and metabolic rates in a range of sediments from the continental shelf to the deep sea.

    CAS  Article  Google Scholar 

  95. Wilhelms, A. et al. Biodegradation of oil in uplifted basins prevented by deep-burial sterilization. Nature 411, 1034–1037 (2001).

    CAS  Article  PubMed  Google Scholar 

  96. Wellsbury, P. et al. Deep bacterial biosphere fuelled by increasing organic matter availability during burial and heating. Nature 388, 573–576 (1997).

    CAS  Article  Google Scholar 

  97. Bale, S. J. et al. Desulfovibrio profundus sp. nov., a novel barophilic sulphate-reducing bacteria from deep sediment layers in the Japan Sea. Int. J. Syst. Bacteriol. 47, 515–521 (1997).

    CAS  Article  PubMed  Google Scholar 

  98. Mikucki, J. A., Liu, Y., Delwiche, M., Colwell, F. S. & Boone, D. R. Isolation of a methanogen from deep marine sediments that contain methane hydrates, and description of Methanoculleus submarinus sp. nov. Appl. Environ. Microbiol. 69, 3311–3316 (2003).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  99. Süss, J. et al. Widespread distribution and high abundance of Rhizobium radiobacter within Mediterranean subsurface sediments. Environ. Microbiol. 8, 1753–1763 (2006).

    Article  PubMed  Google Scholar 

  100. Teske, A. Microbial communities of deep marine subsurface sediments: molecular and cultivation surveys. Geomicrobiol. J. 23, 357–368 (2006).

    CAS  Article  Google Scholar 

  101. Parkes, R. J. et al. Deep subsurface prokaryotes stimulated at interfaces over geologic time. Nature 436, 390–394 (2005).

    CAS  Article  PubMed  Google Scholar 

  102. Schippers, A. & Neretin, L. N. Quantification of microbial communities in near-surface and deeply buried marine sediments on the Peru continental margin using real-time PCR. Environ. Microbiol. 8, 1251–1260 (2006).

    CAS  Article  PubMed  Google Scholar 

  103. Coolen, M. J. L. & Overmann, J. Analysis of subfossil molecular remains of purple sulfur bacteria in a lake sediment. Appl. Environ. Microbiol. 64, 4513–4521 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  104. D'Hondt, S. et al. (eds) in Workshop Report of the Integrated Ocean Drilling Program (A&M University, Texas, in the press).

  105. Sturt, H. F., Summons, R. E., Smith, K., Elvert, M. & Hinrichs, K. U. Intact polar membrane lipids in prokaryotes and sediments deciphered by high-performance liquid chromatography/electrospray ionization multistage mass spectrometry — new biomarkers for biogeochemistry and microbial ecology. Rapid Commun. Mass Spectrom. 18, 617–628 (2004).

    CAS  Article  PubMed  Google Scholar 

  106. Pernthaler, A., Pernthaler, J. & Amann, R. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 68, 3094–3101 (2002).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  107. Schippers, A. et al. Prokaryotic cells of the deep subsurface biosphere identified as living bacteria. Nature 433, 861–864 (2005).

    CAS  Article  PubMed  Google Scholar 

  108. Coolen, M. J. L., Cypionka, H., Sass, A. M., Sass, H. & Overmann, J. Ongoing modification of Mediterranean Pleistocene sapropels mediated by prokaryotes. Science 296, 2407–2410 (2002).

    CAS  Article  PubMed  Google Scholar 

  109. Arndt, S., Brumsack, H. J. & Wirtz, K. W. Cretaceous black shales as active bioreactors: a biogeochemical model for the deep biosphere encountered during ODP Leg 207 (Demerara Rise). Geochim. Cosmochim. Acta 70, 408–425 (2006).

    CAS  Article  Google Scholar 

  110. Jørgensen, B. B., D'Hondt, S. L. & Miller, D. J. in Proc. Ocean Drilling Program, Init. Repts. (eds Jørgensen, B. B., D'Hondt, S. L. & Miller, D. J. ) Vol. 201, 1–45 (Texas A&M University, Texas, 2006).

    Google Scholar 

  111. Schulte, M., Blake, D., Hoehler, T. & McCollom, T. Serpentinization and its implications for life on the early Earth and Mars. Astrobiology 2, 364–376 (2006).

    Article  Google Scholar 

  112. Jørgensen, B. B. & D'Hondt, S. A starving majority deep beneath the seafloor. Science 314, 932–934 (2006).

    Article  PubMed  Google Scholar 

  113. Lin, L. H., Slater, G. F., Lollar, B. S., Lacrampe-Couloume, G. & Onstott, T. C. The yield and isotopic composition of radiolytic H2, a potential energy source for the deep subsurface biosphere. Geochim. Cosmochim. Acta 69, 893–903 (2005).

    CAS  Article  Google Scholar 

  114. Blair, C., D'Hondt, S., Spivack, A. J. & Kingsley, R. H. Radiolytic hydrogen and microbial respiration in a deep sea sediment column. Astrobiology 6, 198 (2006).

    Google Scholar 

  115. Hinrichs, K. U. et al. Biological formation of ethane and propane in the deep marine subsurface. Proc. Natl Acad. Sci. USA 103, 14684–14689 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  116. Price, P. B. & Sowers, T. Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc. Natl Acad. Sci. USA 101, 4631–4636 (2004).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  117. Johnson, K. S., Childress, J. J. & Beelher, C. L. Short time temperature variability in the Rose Garden hydrothermal vent field: an unstable deep-sea environment. Deep-Sea Res. A 35, 1711–1721 (1988).

    Article  Google Scholar 

  118. Luther, G. W. et al. Chemical speciation drives hydrothermal vent ecology. Nature 410, 813–816 (2001).

    CAS  Article  PubMed  Google Scholar 

  119. Le Bris, N., Zbinden, M. & Gaill, F. Processes controlling the physico-chemical micro-environments associated with Pompeii worms. Deep-Sea Res. I 52, 1071–1083 (2005).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

Financial support for writing this review was provided to the laboratory of B.B.J. by the Max Planck Society and the Fonds der Chemischen Industrie, and to the laboratory of A.B. by the EU FP6 program HERMES (Hot spot ecosystem research on ocean margins of European Seas). We thank K. Edwards, W. Bach, N. Dubilier, J. Harder and F. Wenzhöfer for helpful comments and seafloor images, and A. Schippers for providing published data.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bo Barker Jørgensen.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Bo Barker Jørgensen's homepage

Antje Boetius's homepage

Census of Marine Life

Genomes OnLine Database v 2.0

HERMES

International Census of Marine Microbes

Glossary

Benthic

Relating to or occurring at the seafloor.

Mud volcano

A large seabed formation (hundreds of metres to kilometres in diameter) that is caused by the eruption of subsurface gas, fluid and mud.

Anoxic

The absence of oxygen in the sea.

Oligotrophic

An aquatic environment that has low levels of nutrients and algal photosynthetic production (for example, high mountain lakes or the open ocean).

Terrigenous

Material that is derived from the terrestrial environment.

Detrital

Dead organic material.

Pelagic

Relating to or occurring in the water column.

Abyssal

Related to the deep seafloor (or abyss) that is situated between the continental rise (<3,000 metres) and the deep trenches (>6,000 metres), at an average depth of 4,000 metres.

Phytodetritus

The remains of dead plants, particularly of microalgae that originated from the surface waters.

Bioturbation

The displacement and mixing of sediment particles by benthic fauna (animals).

Humic substance

A degraded and chemically altered organic material.

Heterotrophic

The acquisition of metabolic energy by the consumption of living or dead organic matter.

Hot-spot ecosystem

An ecosystem of high or special biodiversity within a larger area of low or normal biodiversity.

Chemolithoautotrophic

The metabolism of an organism that obtains its energy from the oxidation of inorganic compounds and uses only carbon dioxide as a source of carbon.

Primary producer

An organism that is the original source of organic material in an ecosystem — plants, algae or chemosynthetic microorganisms.

Chemosynthesis

The biological conversion of 1 carbon molecule (usually carbon dioxide or methane) and nutrients into organic matter using the oxidation of inorganic molecules (for example, hydrogen gas or hydrogen sulphide) as a source of energy, rather than sunlight.

Pockmark

A depression in the seafloor 1–100 m in diameter that is presumably caused by eruptions of subsurface gases.

Gas chimney

A vertically extending circular anomaly (or blank) in the 3D seismic record of the seabed that indicates pathways of gas leakage.

Brine pond

A submarine accumulation of dense, salty seawater that leaks from the subsurface and fills depressions in the seabed.

Oil and asphalt seep

A natural leak of hydrocarbon (oil, tar or asphalt) from the deep seabed to the seafloor.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Jørgensen, B., Boetius, A. Feast and famine — microbial life in the deep-sea bed. Nat Rev Microbiol 5, 770–781 (2007). https://doi.org/10.1038/nrmicro1745

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro1745

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing