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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

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. 1

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

  2. 2

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

  3. 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).

  4. 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).

  5. 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).

  6. 6

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

  7. 7

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

  8. 8

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

  9. 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).

  10. 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).

  11. 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.

  12. 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).

  13. 13

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

  14. 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.

  15. 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).

  16. 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).

  17. 17

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

  18. 18

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

  19. 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).

  20. 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).

  21. 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).

  22. 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).

  23. 23

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

  24. 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).

  25. 25

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

  26. 26

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

  27. 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).

  28. 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).

  29. 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.

  30. 30

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

  31. 31

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

  32. 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).

  33. 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).

  34. 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).

  35. 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).

  36. 36

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

  37. 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).

  38. 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).

  39. 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).

  40. 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).

  41. 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).

  42. 42

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

  43. 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).

  44. 44

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

  45. 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).

  46. 46

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

  47. 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.

  48. 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).

  49. 49

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

  50. 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).

  51. 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).

  52. 52

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

  53. 53

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

  54. 54

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

  55. 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).

  56. 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).

  57. 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.

  58. 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).

  59. 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).

  60. 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).

  61. 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).

  62. 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).

  63. 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).

  64. 64

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

  65. 65

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

  66. 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.

  67. 67

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

  68. 68

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

  69. 69

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

  70. 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).

  71. 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).

  72. 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).

  73. 73

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

  74. 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).

  75. 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).

  76. 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).

  77. 77

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

  78. 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).

  79. 79

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

  80. 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).

  81. 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).

  82. 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).

  83. 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).

  84. 84

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

  85. 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).

  86. 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).

  87. 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).

  88. 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).

  89. 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).

  90. 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).

  91. 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.

  92. 92

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

  93. 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).

  94. 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.

  95. 95

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

  96. 96

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

  97. 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).

  98. 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).

  99. 99

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

  100. 100

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

  101. 101

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

  102. 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).

  103. 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).

  104. 104

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

  105. 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).

  106. 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).

  107. 107

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

  108. 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).

  109. 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).

  110. 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).

  111. 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).

  112. 112

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

  113. 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).

  114. 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).

  115. 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).

  116. 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).

  117. 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).

  118. 118

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

  119. 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).

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

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

Further reading