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Proc. Natl. Acad. Sci. USA Vol. 89, pp. 6045-6049, July 1992

Microbiology

The deep, hot biosphere

(geochemistry/planetology)

THOMAS GOLD

Cornell University, Ithaca, NY 14853

Contributed by Thomas Gold, March 13, 1992

ABSTRACT

life is widespread at depth in the crust of the Earth, just as such life has been identified in numerous ocean vents. This life is not

dependent on solar energy and photosynthesis for its primary energy supply, and it is essentially independent of the surface circumstances. Itsenergysupplycomesfromchemicalsources, due to fluids that migrate upward from deeper levels in the Earth. In mass and volume it may be comparable with all surface life. Such microbial life may account for the presence of biological molecules in all carbonaceous materials in the outer crust, and the inference that these materials must have derived from biological deposits accumulated at the surface is therefore not necessarily valid. Subsurface life may be wide- spread among the planetary bodies of our solar system, since many of them have equally suitable conditions below, while having totally inhospitable surfaces. One may even speculate that such life may be widely disseminated in the universe, since

planetary type bodies with similar subsurface conditions may

be common as solitary objects in space, as well as in other

solar-type systems.

We are familiar with two domains of life on the Earth: the surface of the land and the body of the oceans. Both domains share the same energy source-namely, sunlight, used in the process of photosynthesis in green plants and microorga- nisms. In this process the molecules of water and of CO2 are dissociated, and the products of this then provide chemical energy that supports all the other forms of life. Most of this energy is made available through the recombination of carbon and hydrogen compounds concentrated in the plants with the oxygen that became distributed into the atmosphere and oceans by the same photosynthetic process. The end product is again largely water and CO2, thereby closing the cycle. This was the general concept about life and the sources of its energy until -12 years ago, when another domain of life was discovered (1). This domain, the "ocean vents", found first in some small regions of the ocean floor, but now found to be widespread (2), proved to have an energy supply for its life that was totally independent of sunlight and all surface energy sources. There the energy for life was derived from

chemical processes, combining fluids-liquids and gasses-

that came up continuously from cracks in the ocean floor with substances available in the local rocks and in the ocean water.

Such sources of chemical energy still exist on the Earth,

because the materials here have never been able to reach the condition of the lowest chemical energy. The Earth was

the accumulation of solid materials, condensed in ofcircumstances from a gaseous nebula surrounding

the sun. Much of this material had never been hot after its

condensation, and it contained substances that would be liquid or gaseous when heated. In the interior of the Earth,

heat is liberated by radioactivity, by compression, and by gravitational sorting; and this caused partialliquefactionand

There are strong indications that microbial

formed by

a variety

The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.

6045

gasification. As liquids, gases, and solids make new contacts, chemical processes can take place that represent, in general, an approach to a lower chemical energy condition. Some of the energy so liberated will increase the heating of the

locality, and this in turn will liberate more fluids there and so accelerate the processes that release more heat. Hot regions will become hotter, and chemical activity will be further stimulated there. This may contribute to, or account for, the

active and hot regions in the Earth's crust that are so sharply defined. Where such liquids or gases stream up to higher levels into

different chemical surroundings, they will continue to repre-

sent a chemical disequilibrium and therefore a potential

energy source. There will often be circumstances where

chemical reactions with surrounding materials might be pos-

sible and would release energy, but where the temperature is

too low for the activation of the reactions. This is just the circumstance where biology can successfully draw on chem- ical energy. The life in the ocean vents is one example of this.

There it is bacterial life that provides the first stage in the

process of drawing on this form of chemical energy; for example, methane and hydrogen are oxidized to CO2 and water, with oxygen available from local sulfates and metal oxides. Hydrogen sulfide is also frequently present and leads

to the production of water and metal sulfides; there may be many other reactions of which we are not yet aware. Of all

the forms of life that we now know, bacteria appear to represent the one that can most readilyutilize energy from a

great variety of chemical sources.

How widespread is life based on such internal energy

sources of the Earth? Are the ocean vents the sole represen-

tatives of this, or do they merely represent the examples that were discovered first? After all, the discovery of these is

recent, and we may well expect that other locations that are

harder to investigate would have escaped detection so far.

Bacteria can live at higher temperatures than any other

110'C has been verified, and some biolo-

known organisms; gists consider that as 150'C (providing

the upper temperature limit may be as high always that the pressure is sufficient to

and gases

the crust is not

raise the boiling point of water above this temperature).

There can be little doubt that venting of from areas of the Earth's mantle beneath

liquids

limited to a few cracks in the ocean floor. Indeed fossilized "dead" ocean vents have alreadybeendiscovered(3),show-

ing that the phenomenon

is widespread and occurred

hydrocarbons.

to be

mining

and tunneling

have been noted

Hydrocarbons

drilling in basement

peninsula

in

different geologic epochs. A similar supply of fluids seems to

land areas, where it is much harder to

but it has been noted that many areas of base-

This

for a long time. Major fault lines

have also

been encountered

The

ment rocks contain methane and other

investigate,

be widespread

also in

has been seen in numerous

operations

high

spots of hydrocarbon seepage (4).

in

deep

Soviet superdeep

rocks, as in the

and in the

Project.

pilot

ices)

well in the Kola

hole of the German Continental Deep Drilling

large quantities of methane hydrates

found in many areas of the ocean

(methane/water

floor, and thought to contain

6046 Microbiology: Gold

more methane than allother known methane deposits (5, 6), suggest a widely distributed methane supply from below. In land areas, deep in the rocks, it would be much harder to discover and investigate biological activity than in the ocean vents. The pore spaces in the rocks are quite sufficient to accommodate bacterial life, and the rocks themselves may contain many of the chemicals that can be nutrients together with the ascending fluids. But, of course, there would be no space for larger life forms. Just as bacterial life in the ocean vents would not have been discovered had the secondary larger life forms not drawn attention to it, so any active bacterial life deep in the solid crust could have gone largely unnoticed. The remains of bacteria in the form of molecules- "hopanoids" (derived from hopanes)-a material coming from bacterial cell walls, have however been found in all of the several hundred samples of oil, coal, and kerogen (dis- tributed carbonaceous material in the crust) examined by Ourisson et al. (7). These authors note the widespread or apparently ubiquitous presence of these molecules in the

sedimentary rocks, and they give an estimate of the total quantity as of the order of 1013 or 1014 tons, more than the

estimated 1012 tons of organic

on or near the surface.

carbon in all

living organisms

identical

in oil and in

They also note the virtually

pattern of the chromatogram of these molecules

coal. Further they note that some of the molecules most

commonly used to identify the presence of biological material

in petroleum, such as pristane and phytane, are not neces-

sarily derived from plant chlorophyll

of the same bacterial

be-

cultures as those that gave rise

presence of these biomolecules can therefore not be taken to prove a derivation of the bulk substance from surface bio-

to which active bacterial life may have

rocks?

surface

total amount of chemical

it? How

comparable with it in the

Would this

penetrated?

as is

commonly

lieved, but could well be products

logical debris.

What are the depths

to the hopanoids. The

Could bacteria get down into the

represent just

deep

a minor branch of all the

caused

by

biological activity, or could it be

processing

important would such life have been lution of the crust of the Earth?

An upper limit of the temperature

place a limit on the depth

of

areas of the crust. The

for the chemical evo-

of 110-150'C would

between 5 and 10 km in most

mere question of access to such

problem.

along

cracks and

depths

Even just the rate of

in

which the requisite nutrients are available would take them

small fraction of the

pore spaces

The tidalpumping

water alone would be sufficient to distribute down to 10 km in less than a thousand years.

bacteria

of ground

would provide stillmuch fastertransport.

time span available. In fact,

down in a few thousand years-a very

for bacteria would be no growth of bacterial colonies

pore spaces

fluid movements in

Probably longer

times would have been

required to allow for

the adaptation to the high temperatures.

The total pore space available

porosity

as an

in the land areas of the Earth

(taking

density

a

bacterial

it would still be

down to 5 km depth

3%

can be estimated as 2 x 1022 cm3 average value). If material of the

this might

be

of water fills these pore spaces, then this would represent

mass of 2 x 1016 tons. What fraction of

mass? If it were 1% or 2 x 1014 tons,

equivalent to a layer

spread

of the order of 1.5 m thick of

living,

living

material if

indeed be more

do not know at present how to make a realistic estimate of the

surface flora and fauna. We

out over all of the land surface. This would

than the existing

subterranean mass of material now

said is that one must consider it

to all the living mass at the surface.

but all that can be

possible that it is comparable

Together

with this consideration would go the consider-

activity

ation of the cumulative amount of chemical

that

could be ascribed to this deep biosphere and with that the

Proc. Natl. Acad. Sci. USA 89 (1992)

importance it may have had for the chemical evolution of the crust, the oceans, and atmosphere and the development of

the surface biology.

The remarkable

concentrated

deposits

degree

of chemical selection

leading

to

of certain minerals has long been an

lead to the produc-

refining

when the

by

enigma. How can

tion of a nugget ofgold or a crystal ofgalena

processes in the crust

process had to concentrate these

to produce

such

complexity

ability

large

ously been thought?

a factor of

more than 1011 from the original elemental mix? How much of the concentrated metal minerals found have so far been

explainedsatisfactorily?What energy sources were available

local decreases of entropy, and how

was the

with their

pro-

cesses, may have had a much

materials

necessary energy applied? Is this not a field where the

to

of carbon

chemistry

and

biology,

be highly selective and to mediate chemical

It is

larger

share than had

previ-

characteristic, after all, for biology

entropy at the

elsewhere.

it

will become a

to generate

expense of energy absorbed and

important local decreases of

deep,

hot

depth?

entropy rejected

biosphere,

If there exists this

imprint

how

much to life at

petroleum

the

deep biosphere

a

thinking

central item in the discussion

branches of the Earth sciences. How much of the

of many, or indeed most,

biological

biological

of material in the sediments is due to surface life and

molecules of

the additions from

rather

the substances

Do the

and coal indicate now

to materials of

merely

primordial origin,

depth.

than indicate

themselves?* Many deductions that are

ical

if there is indeed such an

biological origin

ofthe

present

of the

of the bulk of

may

firmly

have to be

origin

of life.

in the

geolog-

reconsidered,

time

abundance of life at

One cannot discuss these

them with the

is an

considerable

questions

sources that were

time from its

to

examine

origin

process. Presumably

provided by

chemical

and

energy

possibly

speculating

here.

possibilitieswithout connecting

Photosynthesis

extremely complex process,

way

down on the

tap

simpler

to

to

the

path

had

which must lie some

of evolution. to sustain life for

Energy

all the

of

the photosynthetic

energy sources,

perfection

these were

chemical

the substances of the Earth. Now one

whether these were

sources

providing

perhaps

will want

the

the bacterial life in the rocks about which we are

the same as the

life in the ocean vents

The rocks that have

percolating upward

locations for the

first

(9). Deep

hydrogen, methane, and other fluids

rapid response

radiations are low

against

all the

photochemical

by

the

large

broad

sub-

light or even

since a

primitiveandjudged to be

this

may

indi-

in

the

thermophiles,

high temperatures

are

would seem to be the most favorable

generation of self-replicating systems

temperature, pressure,

and chem-

of

to

changing

and

circum-

unchang-

in the rocks the

no

icalsurroundingsare constantforgeologicallylongperiods

time, and, therefore,

stances is needed.

ing.

changes induced

spectrum

of visible

Bacteriologists

Ionizing

No defense is needed

by

ultraviolet

sunlight.

have

speculated that,

most

group the most ancient bacteria-are

cate that

primitive

the first place

of archaebacteria-the

life evolved at such

(10). If it did and if the archaebacteria

*Robert

leum,

Robinson,

after

studying

possibility

composition

the

as

likely.

that

He

petroleum

since, demonstrating

petroleum,

of natural

petro-

it

considered this

wrote, "Actually

does

not

present

cannot be too

strongly emphasized

with the

bioproducts

thecompositionpictureexpectedfrom

and all the arguments

well,

or

better,

biological

modifiedbiogenicproducts,

fitequally

primordial hydrocarbon

(8). Although

the

variety

there

of

this can

This

rather

from the constituents of ancient oils

conception

of a

have been added"

mixture to which

has been much detailed work

molecules that exist in most

frequently cited to

bioaddition,

support

none of

make the distinction between the two

work was

than the

put under consideration.

opposing viewpoints.

the

bioorigin theory

as

a widespread microbiology at depth

was not

Microbiology: Gold

earliest forms of bacteria, evolved at some depth in the rocks, they may have spread laterally at depth, and they may have evolved and progressed upwards to survive at lower temper- atures nearer the surface. Some combination of lateral spread

at depth and spread over the surface with subsequent read-

aptation to the conditions at depth will have allowed them to populate all the deep areas that provided suitable conditions

to support such life. Of course now, when the surface is replete with bacteria of all kinds, it may be difficult to unravel

the evolution in each of the domains. If the deep, hot biosphere of microbial life exists in the

rocks as well as at the ocean vents, what would be the consequences? Could we expect to have seen any evidence already?

Many reports have been published in recent times describ-

ing the discovery of bacteria in deep locations where they were not expected. The most striking example is the discov-

ery deep in the granitic rock of Sweden. While drilling to a depth of 6.7 km in an ancient meteorite impact crater called

the Siljan

netite

Ring, very large quantities of a fine-grained mag-

were encountered. Magnetite, a magnetic iron oxide,

exists normally in the granite in the form of large crystals (-1

mm) and at a low mean concentration. What was found was quite different from this. Grains in the micrometer size range

were found in a thick sludge or paste, with a liquid binder that was a light oil. This was seen first at a time when the drilling

fluid was water, with only occasional small additions of a

plant oil as a lubricant. This sludge contained oil to the

complete exclusion of water, and the oil was largely a simple,

light, hydrogen-saturated petroleum, completely different

from plant oils. (It is worth noting that no sediments of any kind had been encountered in the drilling, only granitic and igneous rock.)The magneticgrainswere notonlyparticularly small, but alsohad a differenttrace element content from the coarse magnetite grains in the granite. Neither the magnetite nor the oil had a simple explanation in terms of the material

of the formation or of any of the drilling additives. The

quantities of this sludge found in this first discovery were not small-60 kg of it filled a drillpipe to the almost complete

exclusion of the water-based drilling fluid. Later a pump

pumped up 15 tons of a similar oil, together with about 12 tons of the magnetite (11). Similar oil-magnetite pastes have been reported in several other oil drilling operations, and micro-

organisms

local ferric iron of the formation to the lesser oxidized

magnetite, using the hydrocarbons as the reducing agent

have been identified that mediate the reduction of

(12-14).

Later, when oil-based drilling fluid had been in use for several months, it was discovered that this had become

loaded with many tons, at least 15 and possibly 30, of this

fine-grained magnetite. It became clear that there was a phenomenon that occurred on a large scale and that was a

major process in the rocks at a depth of between 5.5 and 6.7 km.

It is very difficult to see how concentrations of this material

could occur without bacterial action; indeed, samples of it

have allowed several

strains of previously unknown thermophilic, anaerobic bac-

teria to be cultured.t It will therefore be worthwhile to search

for the presence of locations in the rocks

available. The obvious locations for this are the deep oil or

gas wells. Bacterial cultures can be attempted from

samples

is known to be

other deep

taken from a depth of 4 km or

deeper

microorganisms in many

where chemical energy

tU. Szewzyk at the National Bacteriological Laboratory (Stock- holm) has cultured several strains of anaerobic, thermophilic bac- teria from samples taken below 4000 m in the Gravberg borehole,

Siljan

Ring, Central Sweden (personal communication). Also K.

Pedersen at the Department of Marine Biology of the University of Goteborg reports about deep ground water microbiology (15).

Proc. Natl. Acad. Sci. USA 89 (1992)

6047

taken with the necessary precautions (maintenance of tem-

perature, pressure,

culturing

the

places of

Although

bacteria

and exclusion of

oxygen)

and

using

at

of

of

media similar to the local chemical

origin.

surroundings

presence

signs

it had often been said that the

by

in oil can be identified

the chemical

"biodegradation"

ing.

Oil

may

showing

coming

still have

of that oil, we believe that this is mislead-

none of the known

from a

region

signs

of

biodegradation

life,

and

the

The

rich in bacterial

and not

gained biological molecules

suffered

any

other

depth

changes.

is

likely

by

that of

rulethat

general

oxygen

oils

may still be

from this

oil

to be

limited

themolecules of the heavier present in suf-

ficient

with

will not suffer

of

biomolecules and

that nevertheless

contained biomolecules that had been considered as the most

of the oil itself. and a nonbio-

without, however, having

from methane to pentane,

hydrocarbons.

quantity

If the

sources

sufficiently

to exhaust

stances, which are

provinces,

oil will then

is the

finding

of

yet

compelling

This

reason for this is that microbial attack at

by

the

availability

in that

case,

hydrocarbons;

bacteriawouldfirstuse

of

oxygen

it seems to be the

thelighthydrocarbons,

before

attacking any

are

light hydrocarbons

the

locally

available

(ironoxides,sulfates,and perhapsotheroxides

low

oxygen binding energy),

any biodegradation.

probably

then

the

liquid

Under these circum-

depth

in

petroleum

It

common at

commonly

exist with additions

of

oil

biodegradation.

any signs

apparently undegraded

without

evidence for a

biological origin

longer

be

valid,

consideration would no

seems probable.

logical origin

as

for

bodies,

recognition

for the bulk of the terrestrial

hydrocarbons

hydrocarbons,just

planetary

all the abundant

then

on the other

example

of

This is one

where

the

existence of abundant microbial life at

depth may change major considerations in geology and

of the

we find

geochemistry.

Where

subjected

lesser

occurs

ygen

"biodegraded" oil,

of

it must have been

oxygen and

this

ox-

to conditions

of the

greater availability

availability

generally

available in

of the

is

tion

low ambient

It may

that

can

chemical

"infection"

Chemical

liberated

ganisms.

hydrocarbon gases; presumably,

surface where

atmospheric

nearer the

ground

water and where the concentra-

light hydrocarbons is low, as these are gases at the

pressure. be that we shall find a

simplegeneral

rule to

apply:

microbial life exists in all the locations where microbes

survive, that would mean all the locations that have a

and that are at a

energy supply

spontaneously

That means

temperature

adapt.

below

which microbes can

of

There would

protected from

it must not be

for the long periods

energy

must be

geologic time.

but

available,

without

the intervention of the or-

with regions

energy

below

we have to be concerned

processes

that can release

must be

the maximum one to

be no locations on the Earth that have been

in which the chemical

would not run

tion, but that

Research on the

judge the extent of

expect

activity

to

gain

an

petroleum

new information

insight

and its various mineral

minerals and

of

techniques

and natural

spontaneously;thetemperature

that

give

require

intermediate

deep

it

microbial

on the

into

the activation temperature for the

reactions must be involved

reactions, or a set of

out

energy

on

comple-

energy.

one to

steps

that absorb

life would allow

and with that one can

extent to which microbial

Earth,

the

has contributed to the chemical evolution of the crust

deposits. Prospectingtechniques

improved.

be

economic

influence

for

forpetroleummay

is

a

subject

of

great

may profoundly

the

The derivation

importance,

the

and

prospecting

petroleum

quantities of

system

do not have

numerous bod-

of atmospheric

presence

of

and the estimates

gas

of

that remain to be discovered.

The otherplanetary

bodies in our solar

favorable circumstances for surface life.The ies that have solid surfaces all have conditions

pressure and temperature unfavorable for the

6048 Microbiology: Gold

liquid water. Mars, deemed the least unfavorable in this respect, has been investigated (by the Viking landers), and no indications of any biological activity have been found. With this, it seemed that there was little or no chance of finding any other life in the solar system. With the possibility of subsurface life, the outlook is quite different. Many planetary bodies will have temperature and pressure regimes in their interiors that would allow liquid water to exist. Hydrocarbons clearly are plentiful not only on all the gaseous major planets but also on the solid bodies (the large satellites, numerous asteroids,theplanetPluto, comets and meteorites); and there is every reason to believe that hydrocarbon compounds were incorporated in all of the planetary bodies at their formation. The circumstances in the interior of most of the solid planetary bodies will not be too different from those at a depth of a few kilometers in the Earth. The depth at which similar pressures and temperatures will be reached will be deeper, as the bodies are smaller than theEarth, butthisfactitselfdoes notconstituteanyhandicap

for microbial life. If in fact such life originated

at

bodies

depth in the

in our solar

system that would have had a similarchance fororiginating

microbial life. Could the space program ever discover this? Is there a

Earth, there are at least 10 other planetary

possibility of finding

the other planetary

life of

bodies?

an independent origin on some of

We shall have to see whether

microorganisms

asteroids,

exist at and in the

depths on the moon, on Mars, in the satellites of the major planets. Such

become central to that

with that they may become a central subject programs.

investigations may

life, and

of

great question of the origin

in future space

There is a chance that an independent origin could indeed

be identified by a number of criteria: the

opposite chiral asymmetries (50-50 chance in

independent origin,

in

just

one

discovery of

case of an

while the observation of the same chi-

rality

different choice of basic molecules, or any of the criteria that have been used to show that all terrestrial life has one

common origin. (Incidentally, as has often been discussed,

this does not imply that there has been only one occurrence

leading to an origin of life: if there had been several, the most

successful would have supplanted

all others, and after that

fresh start in competition

that the space

power to

However, there are other

Valley Marinera on Mars, expose

rifts, such as the that was at one time

program could

other case would be uninformative); a

there would be no

possibility for a

with evolved biology).

It is difficult to foresee at the present

to the

time

proceed

perform very deep drilling operations

sophistication

and

on distant

planets.

options. Deep

terrain

several kilometers below the

from the massive landslides in that

surface. Samples from there,

valley,

could be returned

that living

one

may

fairly

to Earth and analyzed

materials have existed

for chemical evidence there in the past. Similarly,

exposed deep

bodies.

that even the

by

terrestrial

organisms.

sample lunar craters that have

late in the lunar history or deep

of the other solid

planetary

Since we recognize

materials

rifts and young craters on any

seemingly most inhospi-

Manned

table bodies may harbor life, care would now be necessary to

avoid contamination

expe-

ditions, whatever other difficulties there might be with them,

can certainly

such

manned

not

qualify

not be

kept

sterile and would therefore

spoil

researches for all future times. Only very clean un-

space

vehicles

going to planetary

by

bodies that have

previously been visited

to bring back

contaminated vehicles would

meaningful samples of a biology that

Earth.

resembles that of the

If life was restricted to the proximity of the surface of

planetary bodies, then

"panspermia,"

the

material through space over

astronomical

transport

living

distances, would

of

Proc. Natl. Acad. Sci. USA 89 (1992)

material would have to

be very improbable, as such living remain viable in a dormant form for

of the suggested forms of panspermia, it would not be

very long times; in most

protected sufficiently well against the cumulative effects of thecosmicrays.Meteoriticimpactscouldwellhaveexploded

may

both

inside of

cosmic ray bombardment of

there is

chance of

meters of solids from the

another. But unless the

a rock, so as to be shielded

there would be little

large chunks of rock from one planet, and such chunks

have escaped complete vaporization

during expulsion

from one

transferring

and excessive

heating

on

Pansper-

body and accretion

were

deep

materials.

living organisms

by many

space,

functional

living

mia becomes a much more realistic

for a

bombardment

indeed are found

contain carbonaceous material. Can one find traces of

for

its overall energy supply, may be just one strange branch of

to have

circumstances on its surface as would occur afavorableatmosphere, a suitabledistance

from an

etc. The

be

make it

formed in

the materials of molecular

cold bodies have

universe. Astronomical considerations

possibility if

bodies.

abundant life at depth in the planetary

have been a vastly greater

transfer between

planets

number

in earlier

There would