IF Hell is a deep hole somewhere uncomfortably warm in the Earth鈥檚 interior,
then one thing鈥檚 certain. There鈥檚 precious little room for tormented human
souls. Most of the space is filled with strange life forms that relish the heat,
the crushing pressures and the starvation diet. If you could peel away the
planet鈥檚 surface fuzz, siphon off the oceans and delve far beneath the surface,
you would discover an incredible new world: a planet within a planet. This deep,
dark biosphere inside the Earth may well contain as much life as the airy,
sunlit world on the outside.
The resident microorganisms don鈥檛 look strikingly different from those living
in the world above but their existence changes our perception of Earth鈥檚
interior as a lifeless realm where chemistry reigns, aided and abetted by
immense physical forces. These tiny organisms with their quirky survival
strategies may be the creators of rich seams of minerals, nuggets of gold even,
and perhaps the reservoirs of oil and gas the world has come to depend on. More
than that, their weird tricks for dealing with isolation in the depths of the
Earth increase the chances of finding life on other planets鈥攏ot on the
surface but hidden inside.
The idea of a deep biosphere, a world that stretches down for kilometre after
kilometre, is still in its infancy. For most of this century, microbiologists
believed that bacteria lived down to about 1.5 metres in the topsoil or ocean
mud, then quickly fizzled out. Where geologists dug deeper and claimed they had
found bacteria, they were written off as contaminants carried down from the
surface with the drilling equipment. Some geochemists insisted that there were
changes going on in the geosphere that looked like the work of microorganisms,
but no one could produce any likely suspects.
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Besides, the deep Earth was considered no fit place for living things. The
further down you go, the hotter it gets as the radioactive interior warms the
layers above. Convention has it that microorganisms near the surface quickly
consumed any organic remains buried in the sediment, and the leftovers were a
poor food source. The most persuasive of all arguments was that when people
hunted for these putative organisms, they found nothing. 鈥淧eople dismissed the
idea because it was impossible to grow any organisms in the laboratory, not
because they weren鈥檛 there,鈥� says John Parkes, a microbiologist at the
University of Bristol who is investigating life in deep ocean sediments.
They couldn鈥檛 have been more wrong. Several things happened all at once to
dispel the idea of a sterile subterranean zone. People in the US began to worry
about the safety of the water in their deep aquifers. Half the population
depends on aquifers for drinking water and there were fears that pollution could
contaminate supplies. Also, the US Department of Energy (DOE) was interested in
storing nuclear waste in rocky underground caverns. So it was vital to know if
microorganisms could survive so far down, where they might alter the chemistry
of groundwater or influence the movement of any radionuclides that leaked from
storage drums. In 1987, as part of its Subsurface Science Program, the DOE
drilled three holes into the sedimentary rocks beneath its nuclear site at
Savannah River in South Carolina.
At the same time, microbiologists acquired a battery of new techniques for
detecting bacteria. Even if they could not isolate and culture them, they could
show that they were there with nucleic acid probes and fluorescent dyes that
make DNA glow. Oceanographers exploring the hot vents along mid-ocean ridges
laid another myth to rest when they discovered bacteria that could tolerate
temperatures up to 113 掳C.
The cores from Savannah River provided indisputable evidence that there was
life in the deep subsurface, at least down to 500 metres where the deepest core
ended. Since then, microorganisms have been turning up everywhere, not just in
sedimentary rocks鈥攃onsolidated layers of sediment that began life at the
surface鈥攂ut also in igneous rocks such as granite and basalt, which
solidified from molten magma. Out at sea, cores of sediment collected from every
ocean, down to a depth of 750 metres, showed still more signs of life. 鈥淲e
thought we would be stretching the limits of detection but we found surprisingly
high populations in all our samples,鈥� says Parkes. And the first samples from
the deepest hotspot so far, 3.5 kilometres down a South African gold mine, have
already produced a unique bacterium with some very odd habits (see 鈥淪ome like it
丑辞迟鈥�).
鈥淵ou can probably conclude that bacteria live everywhere that the temperature
is less than 100 掳C, which is a pretty vast part of the crust,鈥� says Martin
Fisk, a geologist at Oregon State University, who has been looking for life in
the glassy basalts beneath the ocean floor. If temperature were the only
limiting factor, then the biosphere could extend down between 5 and 10
kilometres. In igneous rocks life is confined to the fractures, with nothing in
the solid rock between. But in sediments, life gets everywhere, invading the
pores between particles. Some researchers have found as many as 100 million
organisms per gram of sediment. After sampling 15 sites in the Atlantic, Pacific
and Mediterranean, Parkes and his colleagues calculate that the biomass within
ocean sediments down to 500 metres depth is about a tenth that on the surface.
鈥淭here鈥檚 an extra 10 per cent of life down there鈥攂ut that鈥檚 only to 500
metres. In some places sediment is 15 kilometres deep,鈥� says Parkes. Tullis
Onstott of Princeton University, New Jersey, goes further. 鈥淚 calculate that the
biomass is of comparable stature to that on the surface, maybe a little bit
more,鈥� he says.
Not only are there microorganisms everywhere, they come in a huge diversity
of species. David Balkwill, a microbiologist at Florida State University in
Tallahassee, oversees 10 000 strains of microorganisms from the Savannah River
cores. 鈥淲e have characterised only about 400 of them so far, but there are about
40 different genera,鈥� he says. Many belong to known genera, but seem to be new
species. 鈥淎 few strains don鈥檛 match any currently known genus and may be rather
unusual,鈥� says Balkwill. Some seem to belong to species we already know but with
strange adaptations to the peculiar conditions of the muds or rocks they
inhabit.
Even the igneous rocks, created at lethal temperatures, harbour a huge
variety of organisms. Karsten Pedersen and his colleagues at the University of
Gothenburg in Sweden have found several hundred species in granites as far down
as 860 metres. And although Fisk and his colleague Stephen Giovannoni have not
yet isolated the organisms they discovered living in the basalts beneath the
ocean floor, they can see differences under the electron microscope. Different
microorganisms leave telltale tracks as they somehow dissolve a path through the
rock, creating tiny tunnels between 1 and 10 micrometres in diameter. 鈥淭here are
broad, blunt-ended and smooth ones, little chains of buds, mushroom-shaped ones
and thin branching ones鈥攁nd my favourite, which is like a string of little
light bulbs,鈥� says Fisk.
Underworld community
Just as on the surface, the underworld has distinct habitats and niches, each
with its own particular community. 鈥淵ou see some common players in lots of
different places, but there are distinct differences depending, for example, on
whether the environment is sandy or clay, what sort of nutrients are present and
how much moisture there is,鈥� says Balkwill.
And there is more to the deep biosphere than bacteria. There are higher forms
of life in the shape of protozoans. Most are tiny flagellates just 2 or 3
micrometres long which can move through the spaces between mineral particles,
stopping to graze on clumps and films of bacteria. 鈥淚t soon became apparent that
we had quite an active food chain, with protozoa feeding on bacteria,鈥� says Bill
Ghiorse, of Cornell University, one of the pioneers in the Savannah River
studies. So far, protozoans have been collected only down to around 100 metres
in terrestrial sediments. 鈥淏ut it鈥檚 conceivable that you might find them
thousands of metres down,鈥� says Ghiorse.
Rock cakes
The protozoans eat bacteria but what do the bacteria survive on? It all
depends where they live and what sort of chemicals are available. Those found in
sediments and sedimentary rocks live off the remnants of organic material from
the surface, respiring and obtaining energy from oxidised forms of sulphur, iron
and manganese. 鈥淭heir physiology matches the habitat they live in,鈥� says Jim
Fredrickson, an environmental microbiologist at Battelle Pacific Northwest
National Laboratory. Bacteria like these, which live in the absence of oxygen,
work as a close-knit team, breaking down complex organic matter in stages: one
bacterium鈥檚 waste provides a meal for another member of the team.
With increasing depth, supplies of organic matter should dwindle to nothing:
at least that鈥檚 the dogma. 鈥淚 thought we would see bacteria cunningly surviving
on buried organic material, and as it became rarer you鈥檇 have no more bacteria,鈥�
says Parkes. 鈥淏ut at more and more sites we found activity was stimulated by
depth.鈥� Puzzled, Parkes tried heating samples of ocean sediment to simulate the
increasing temperatures at depth. Chemical analysis of the sediment showed that
as it grew hotter, the amount of acetate, an organic acid, increased. Many
bacteria can break down acetate to extract the carbon and energy they need.
鈥淭his increase was a complete surprise,鈥� says Parkes. 鈥淚f this is a widespread
process then the energy sources may get better the deeper you go and the hotter
you go.鈥� It is even possible that bacteria are responsible for producing the
acetate, as more complex organic matter is made more digestible by heating.
Despite their cunning ways of making the most of the available organic
material, these organisms and the communities that feed off them are ultimately
linked to the surface: the organic matter they rely on is the product of
photosynthesis鈥攁nd solar energy 鈥攁lbeit many thousands or millions
of years ago. But bacteria in igneous rocks must make do without even this
slender connection. There is no buried organic material in igneous rock, only a
few traces in the percolating water, which itself may have been isolated from
the surface for aeons. So it came as a shock when researchers studying the
basalts of the Columbia River Basin in Washington State discovered flourishing
communities of bacteria, far more than the traces of organic material could
possibly support.
The explanation was a revelation. Todd Stevens and James McKinley, of
Battelle Pacific Northwest National Laboratory, found that many of the bacteria
were manufacturing their own organic compounds, using carbon and hydrogen taken
directly from carbon dioxide and hydrogen gas dissolved in the rock, and
producing methane in the process. In this world, these bacteria are the primary
producers, the equivalent of plants and phytoplankton on the surface. This is
the only ecosystem on the planet that is totally independent of the surface
world and solar energy. With such capabilities, it could go on indefinitely.
The varied and innovative means by which the inhabitants of the deep
biosphere acquire nutrients and energy explains how they could have survived cut
off from the outside world for so long. Bacteria that live in sediments and
sedimentary rocks probably originated on the surface, becoming buried ever
deeper as new layers formed above them and eventually compressed the soils and
muds into rock. Onstott speculates that the bacteria at the bottom of the gold
mine in Witwatersrand could have been isolated from the surface for 2 billion
years. Microorganisms that live in igneous rocks must have been carried through
cracks by circulating groundwater, but in places even these might have been cut
off from the surface for millions of years.
No one doubts that the bacteria are alive but most are just ticking over,
reproducing perhaps once every few hundred years. Nutrients are generally in
short supply and a starvation diet doesn鈥檛 encourage fast-living. 鈥淭he long-term
survivors have a slow rate of metabolism and use their reserves sparingly,鈥� says
Tom Kieft of the New Mexico Institute of Mining and Technology. As they
metabolise their stored polymers, they shrink, a process known as dwarfing. 鈥淭he
majority of organisms seen in the deep subsurface are very small,鈥� says Kieft.
No one knows how long they can continue like this because there is no way of
assessing the age of an individual microorganism. 鈥淚t鈥檚 not like you can look at
their teeth and say how old they are,鈥� says Onstott.
The bacteria of the deep biosphere may not live life in the fast lane but
their very existence is forcing researchers to rethink the role of
microorganisms in the geosphere, especially the part they play in cycling
minerals鈥攅ven producing mineral deposits鈥攊n the crust. 鈥淎ctivity is
slow but over hundreds of millions of years the impact could be quite
substantial,鈥� says Onstott. Many of these bacteria might break down organic
pollutants so researchers are keen to find out if they could clean up
contaminated soils and aquifers.
Bacteria that generate methane during their metabolism could even be
responsible for the planet鈥檚 gas reserves. 鈥淭he evidence suggests there is a
significant microbial contribution to gas reserves,鈥� says Fredrickson. More
controversially, Tom Gold of Cornell University argues that the inhabitants of
the deep biosphere could be wholly responsible for producing oil鈥攁nd that
long-dead plants and animals have nothing to do with it. Others in the field
won鈥檛 go this far but suggest bacteria might play some part in catalysing the
reactions during oil formation.
Alien life
The existence of a whole new biosphere within the Earth inevitably raises the
stakes in the search for life elsewhere in the Universe. Around 3.8 billion
years ago, when Earth was very young, it already harboured substantial
populations of bacteria. The youthful planet was still being bombarded from
space by giant chunks of rock and exposed to killing ultraviolet radiation.
Occasionally an impact was so catastrophic it generated enough heat to sterilise
the entire surface. Yet life reappeared. Parkes and many others believe that
while the surface died, life retreated to the deep biosphere until conditions
improved on the outside.
If this happened here, why not elsewhere? NASA is pondering this question as
it plans its future missions to Mars and contemplates what might lie below the
icy exterior of Jupiter鈥檚 moon Europa. Today the surface of Mars is
uninhabitable, so NASA argues that if it is going to find any sign of
life鈥攑ast or present鈥攖hen it will have to dig for it. If life arose
when the Martian surface was warmer, then it could have retreated below the
surface when conditions became impossible. If that happened, then at the very
least there should be traces of past life in the form of fossils.
鈥淭he long survival of bacteria in the deep subsurface has dramatic
implications for the future exploration of Mars,鈥� says Onstott, who is helping
NASA plan its mission to collect samples from Mars. When the third Mars Lander
reaches the Red Planet in 2002 it will drill 5 centimetres into the Martian
surface. 鈥淭hat鈥檚 very tiny, but it鈥檚 a start,鈥� he says.
* * *
Some like it hot
TULLIS ONSTOTT has been to Hell and brought back samples. For him, Hell is
the bottom of a gold mine in South Africa, an intolerably hot and humid hole 3.5
kilometres below ground. Onstott, a geologist at Princeton University in New
Jersey, is investigating life in the mine as part of a programme on Life in
Extreme Environments run by the US National Science Foundation.
The mine, owned by the South African company Goldfields, would be impossible
to work in without ventilation. 鈥淭he natural temperature is 65 掳C and
humidity is 100 per cent,鈥� says Onstott. With the help of ventilation, miners
sweat out 8-hour shifts in temperatures of 40 掳C. 鈥淚 only lasted an hour and
a half down there,鈥� says Onstott.
He wants to find what sorts of bacteria live in the rock where the pressure
is 400 atmospheres and the temperature more than 60 掳C. Goldfields is also
keen to know what lives in its mine, hoping that some bacteria might be
persuaded to work as mini-miners, mobilising and flushing out gold in parts of
the seam humans can鈥檛 reach. 鈥淲e know there are substantial reserves as far down
as 4 or 5 kilometres,鈥� says Onstott.
Onstott collected his first samples last autumn. His colleague Tom Kieft of
the New Mexico Institute of Mining and Technology has successfully isolated some
of the microorganisms. 鈥淭hey include a pretty remarkable organism,鈥� says
Onstott. This heat-loving, or thermophilic, bacterium belongs to the genus
Thermus, a group found in warm environments on the surface, such as hot
springs. This particular Thermus has an extraordinarily versatile
metabolism, acquiring energy from a whole range of chemical reactions that can
involve the reduction of nitrate, ferric iron, manganese or elemental sulphur.
鈥淚t can also reduce cobalt, and we have conjectured that maybe it can even
reduce and precipitate gold,鈥� says Kieft. If this is true, the big question is
whether the activity of these bacteria is responsible for the formation of the
gold in the seam.