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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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