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What is the Deep Biosphere?

In a 1992 essay, Thomas Gold postulated the existence of a "deep, hot biosphere", supported by geological energy sources (Gold 1992). Whitman et al. (1998) expanded this provocative concept by collating all available data on aquatic, soil, and subsurface prokaryotes, and concluded that a majority of biomass may be harbored in the subsurface. The ramifications of a hidden biosphere are numerous, leading to paradigm shifts in the biosciences and geosciences (Edwards et al. 2005). The potential contribution to the global budget and cycling of carbon is just one of many examples. To date, deep biosphere studies have focused, often by necessity, on enumerating cells in relatively shallow marine sediments or in terrestrial mines, wells, and drill-core samples. However, these data do not permit a true global census of subsurface life. Even less is known about the activities of this biosphere – in function or in magnitude – or the identity of these microbial communities. The last decade has produced a tremendous increase in deep biosphere studies, proposals, publications, working groups, and field opportunities (e.g., Cowen et al. 2003; Kormas et al. 2003; D'Hondt et al. 2004; Biddle et al. 2006; Inagaki et al. 2006; Roussel et al. 2008; Teske and Sørensen 2008). Although the field is still in its infancy, it is starting to mature from predominantly opportunistic investigations (often piggy-backing on other science) to targeted research. The next fundamental step is to collect the necessary environmental data and to conduct experiments to confirm, dispel, or re-write the short but turbulent history of the deep, hot biosphere and its importance – or lack thereof – in the Earth system.

The largest potential subsurface biome is also the least accessible – the deep ocean subsurface. It also has the greatest potential for influencing global-scale biogeochemical processes, including the carbon, energy, and nutrient cycles. The potential for this biome to influence global processes scales, in part, to its vast size. Depending on geothermal gradients and physico-chemical limits of life, the subsurface biosphere may extend to a depth of 5-10 km, or more, and occupy a volume several orders of magnitude greater than the continental biosphere. Gas seeps, hydrothermal vents, and fresh rock outcrops serve as windows into this subsurface, and determining the biological processes and rates there is now at the forefront of deep biosphere studies. Additionally, these rock outcrops serve as conduits of fluid flow between the "sub-seafloor ocean" and our oceans basins (Fisher 1998; Fisher and Becker 2000). Fluid flow in the oceanic aquifer in ridge flanks largely balances and controls elemental exchange between crust and seawater, and as consequence, global ocean chemistry (Bach et al. 2004 and references therein). The porous rock medium that provides conduits for the superhighway of fluids may also provide safe havens for life. Examinations of the rock-hosted oceanic deep biosphere is a realm of study just beginning (e.g., Fisk et al. 1998), but similar to deeply buried sedimentary habitats (e.g., D'Hondt et al. 2004), it holds promise for revealing new and remarkable information about remote life here on Earth.


References

Bach, W., Humphris, S. E., and Fisher, A. T. 2004. Fluid flow and fluid-rock interaction within the oceanic crust: Reconciling geological, geochemical, and geophysical observations. In Wilcock, W. S. D., DeLong, E. F., Kelley, D. S., Baross, J. A., and Cary, S. C. (eds), The Subseafloor Biosphere at Mid-Ocean Ridges, Geophys Monogr Ser 144. American Geophysical Union, Washington DC. 99-117.

Biddle, J. F., Lipp, L. S., Lever, M. A., Lloyd, K. G., Sorensen, K. B., Anderson, R., Fredricks, H. F., Elvert, M., Kelly, T. J., Schrag, D. P., Sogin, M. L., Brenchley, J. E., Teske, A., House, C. H., and Hinrichs, K.-U. 2006. Heterotrophic archaea dominate sedimentary subsurface ecosystems off Peru. Proc Natl Acad Sci USA 103, 3846-3851.

Cowen, J. P., Giovannoni, S. J., Kenig, F., Johnson, H. P., Butterfield, D. A., Rappe, M. S., Hutnak, M., and Lam, P. 2003. Fluids from aging ocean crust that support microbial life. Science 203, 120-123.

D'Hondt, S., Jorgensen, B. B., Miller, D. J., Batzke, A., Blake, R., Cragg, B. A., Cypionka, H., Dickens, G. R., Ferdelman, T., Hinrichs, K.-U., Holm, N. G., Mitterer, R., Spivack, A. J., Guizhi, W., Benkins, B., Engelen, B., Ford, K., Gettemy, G., Rutherford, S. D., Sass, H., Skilbeck, C. G., Aiello, I. W., Guerin, G., House, C. H., Inagaki, F., Meister, P., Naehr, T., Niitsuma, S., Parkes, R. J., Schippers, A., Smith, D. C., Teske, A., Wiegel, J., Padilla, C. N., and Acosta, J. L. 2004. Distributions of microbial activities in deep subseafloor sediments. Science 306, 2216-2221.

Edwards, K. J., Bach, W., and McCollom, T. M. 2005. Geomicrobiology in oceanography: Microbe-mineral interactions at and below the seafloor. Trends Microbiol 13, 449-456.

Fisher, A.T. 1998. Permeability within basaltic ocean crust. Rev Geophys 36, 143-182.

Fisher, A., and Becker, K. 2000. Channelized fluid flow in oceanic crust reconciles heat flow and permeability data. Nature 403, 71-74.

Fisk, M. R., Giovannoni, S. J., and Thoreth, I. H. 1998. Alteration of oceanic volcanic glass: Textural evidence of microbial activity. Science 281, 978-980.

Gold, T. 1992. The deep, hot biosphere. Proc Natl Acad Sci USA 89, 6045-6049.

Inagaki, F., Nunoura, T., Nakagawa S., Teske A., Lever M., Lauer, A., Suzuki, M., Takai, K., Delwiche, M., Colwell, F. S., Nealson, K. H., Horikoshi, K., D'Hondt, S., and Jørgensen, B. B. 2006. 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.

Kormas, K. A., Smith, D. C., Edgcomb, V., and Teske, A. 2003. Molecular analysis of deep subsurface microbial communities in Nankai Trough sediments (ODP Leg 190, Site 1176). FEMS Microbiol Ecol 45, 115-125.

Roussel, E. G., Bonavita, M. C., Querellou, J., Cragg, B. A., Webster, G., Prieur, D., and Parkes, R. J. 2008. Extending the sub-sea-floor biosphere. Science 320, 1046.

Teske, A., and Sørensen, K. B. 2008. Uncultured Archaea in the deep marine subsurface sediments: Have we caught them all? ISME J 2,3-18.

Whitman, W. B., Coleman, D. C., and Wiebe, W. J. 1998. Prokaryotes: The unseen majority. Proc Natl Acad Sci USA 95, 6578-6583.


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