Exobiology in the Solar System & The Search for Life on Mars - ESA

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I.3.6 Subterranean <strong>Life</strong>
to <strong>in</strong>vent specific devices to adapt to high pressure (<strong>for</strong> review, see Prieur, 1992).
High pressure seems to <strong>in</strong>crease <strong>the</strong> growth rate of some hyper<strong>the</strong>rmophiles, but this
phenomenon is not general and not very spectacular. Although some prote<strong>in</strong>s from
hyper<strong>the</strong>rmophiles are more active at high pressure, high pressure does not <strong>in</strong>crease
<strong>the</strong> <strong>the</strong>rmal stability of macromolecules (Bernhardt et al., 1984).
For a long time, it was believed that deep subterranean environments were sterile. It
has now been recognised that bacteria (and probably archaea, too) actually thrive <strong>in</strong>
<strong>the</strong> terrestrial crust. Subterranean microorganisms are usually detected <strong>in</strong> subterranean
oil-fields or <strong>in</strong> <strong>the</strong> course of drill<strong>in</strong>g experiments (Parkes & Maxwell, 1993;
Parkes et al., 1994; Stevens & McK<strong>in</strong>ley, 1995). For example, recent research
conducted with<strong>in</strong> <strong>the</strong> International Ocean Drill<strong>in</strong>g Program (ODP) has demonstrated
that procaryotes are present much deeper <strong>in</strong> mar<strong>in</strong>e sediments than was previously
thought possible, extend<strong>in</strong>g to at least 750 m below <strong>the</strong> sea floor, and probably much
deeper (Parkes et al., 1994). <strong>The</strong>se microbial populations are substantial (e.g 10 7 cells
cm -3 at 500 m below sea floor) and likely to be widespread. To depths of at least
432 m, microbes have been identified as alter<strong>in</strong>g volcanic glass, which comprises a
substantial volume of <strong>the</strong> volcanic component of <strong>the</strong> ocean crust (Furnes et al.,1996),
and may have significance <strong>for</strong> chemical exchange between <strong>the</strong> oceanic crust and
ocean water. <strong>The</strong>se data provide a prelim<strong>in</strong>ary, and probably conservative, estimate of
<strong>the</strong> biomass <strong>in</strong> this important new ecosystem: about 10% of <strong>the</strong> surface biosphere.
<strong>The</strong>se discoveries have radically changed our perception of mar<strong>in</strong>e sediments and
<strong>in</strong>dicate <strong>the</strong> presence of a largely unexplored deep bacterial biosphere that may even
rival <strong>the</strong> Earth’s surface biosphere <strong>in</strong> size and diversity!
Elevated procaryotic populations and activities are also associated with gas
hydrates. This, toge<strong>the</strong>r with <strong>the</strong> presence of large microbial populations <strong>in</strong> oil
reservoir fluids (Stetter et al., 1993, Haridon et al., 1995, Bernard, et al., 1992, Rueter
et al., 1994), suggests that deep bacterial processes may even be <strong>in</strong>volved <strong>in</strong> oil and
gas <strong>for</strong>mation by comparison with <strong>the</strong> key catalytic role of near-surface procaryotic
communities. Procaryotes are also likely to drive deep geochemical reactions such as
m<strong>in</strong>eral <strong>for</strong>mation and dissolution, be responsible <strong>for</strong> <strong>the</strong> magnetic record via
production of magnetic m<strong>in</strong>erals, produce deep methane gas essential <strong>for</strong> hydrate
<strong>for</strong>mation.
Procaryotes <strong>in</strong> <strong>the</strong> deep biosphere must be uniquely adapted to live <strong>in</strong> this extreme
environment, and populations have even been shown to <strong>in</strong>crease at depth (>200 m) as
<strong>the</strong>y exploit deep geochemical fluxes such as geo<strong>the</strong>rmal methane and br<strong>in</strong>e
<strong>in</strong>cursions.
Heterotrophic subterranean communities use ei<strong>the</strong>r remnant organic carbon
deposited with sediments or dissolved oxygen as a metabolite term<strong>in</strong>al electron
acceptor. <strong>The</strong>y are thus actually <strong>in</strong>directly dependent on photosyn<strong>the</strong>tic activity.
Hence <strong>the</strong>y can become ext<strong>in</strong>ct when <strong>the</strong>ir nutrients are exhausted. However,
evidence has also been obta<strong>in</strong>ed <strong>for</strong> <strong>the</strong> existence of anaerobic subsurface
litoautotrophic microbial systems <strong>in</strong> basalt aquifers (Stevens & McK<strong>in</strong>ley, 1995).
<strong>The</strong>se communities apparently derived <strong>the</strong>ir energy from geochemically-produced
hydrogen. Because <strong>the</strong> energy sources and <strong>in</strong>organic nutrients are both supplied by
geochemical means, such a subsurface lithoautotrophic microbial ecosystem
(SLiME) could a priori persist <strong>in</strong>def<strong>in</strong>itely even if <strong>the</strong> conditions on <strong>the</strong> Earth’s
surface became alien to life.
S<strong>in</strong>ce <strong>the</strong> temperature <strong>in</strong>creases with depth, it has been suggested that
hyper<strong>the</strong>rmophiles, <strong>in</strong> particular chemiolitoautotrophs, are abundant <strong>in</strong> subterranean
environments, <strong>for</strong>m<strong>in</strong>g a deep hot biosphere (Gold, 1992). Indeed, procaryotic
activity has even been reported up to 120ºC and possibly even higher (Cragg
&Parkes, 1994), i.e. above <strong>the</strong> upper temperature limit def<strong>in</strong>ed <strong>in</strong> <strong>the</strong> laboratory. <strong>The</strong>
challenge now is to cultivate <strong>the</strong>se putative novel hyper<strong>the</strong>rmophiles. Up to now, all
microbes sampled from subsurface environments have turned out to be close
relatives of well-known bacteria, but <strong>the</strong>se studies have been ra<strong>the</strong>r limited and one