Proc. Natl. Acad. Sci. USAVol. 89, pp. 6045-6049, July 1992Microbiology

The deep, hot biosphere(geochemistry/planetology)

THOMAS GOLDCornell University, Ithaca, NY 14853

Contributed by Thomas Gold, March 13, 1992

ABSTRACT There are strong indications that microbiallife is widespread at depth in the crust of the Earth, just as suchlife has been identified in numerous ocean vents. This life is notdependent on solar energy and photosynthesis for its primaryenergy supply, and it is essentially independent of the surfacecircumstances. Its energy supply comes from chemical sources,due to fluids that migrate upward from deeper levels in theEarth. In mass and volume it may be comparable with allsurface life. Such microbial life may account for the presenceof biological molecules in all carbonaceous materials in theouter crust, and the inference that these materials must havederived from biological deposits accumulated at the surface istherefore not necessarily valid. Subsurface life may be wide-spread among the planetary bodies of our solar system, sincemany of them have equally suitable conditions below, whilehaving totally inhospitable surfaces. One may even speculatethat such life may be widely disseminated in the universe, sinceplanetary type bodies with similar subsurface conditions maybe common as solitary objects in space, as well as in othersolar-type systems.

We are familiar with two domains of life on the Earth: thesurface of the land and the body of the oceans. Both domainsshare the same energy source-namely, sunlight, used in theprocess of photosynthesis in green plants and microorga-nisms. In this process the molecules of water and of CO2 aredissociated, and the products of this then provide chemicalenergy that supports all the other forms of life. Most of thisenergy is made available through the recombination ofcarbonand hydrogen compounds concentrated in the plants with theoxygen that became distributed into the atmosphere andoceans by the same photosynthetic process. The end productis again largely water and CO2, thereby closing the cycle.

This was the general concept about life and the sources ofits energy until -12 years ago, when another domain of lifewas discovered (1). This domain, the "ocean vents", foundfirst in some small regions of the ocean floor, but now foundto be widespread (2), proved to have an energy supply for itslife that was totally independent of sunlight and all surfaceenergy sources. There the energy for life was derived fromchemical processes, combining fluids-liquids and gasses-that came up continuously from cracks in the ocean floor withsubstances 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 thecondition of the lowest chemical energy. The Earth wasformed by the accumulation of solid materials, condensed ina variety ofcircumstances from a gaseous nebula surroundingthe sun. Much of this material had never been hot after itscondensation, and it contained substances that would beliquid or gaseous when heated. In the interior of the Earth,heat is liberated by radioactivity, by compression, and bygravitational sorting; and this caused partial liquefaction and

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 ofthe energy so liberated will increase the heating of thelocality, and this in turn will liberate more fluids there and soaccelerate the processes that release more heat. Hot regionswill become hotter, and chemical activity will be furtherstimulated there. This may contribute to, or account for, theactive and hot regions in the Earth's crust that are so sharplydefined.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 potentialenergy source. There will often be circumstances wherechemical reactions with surrounding materials might be pos-sible and would release energy, but where the temperature istoo low for the activation of the reactions. This is just thecircumstance 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 theprocess of drawing on this form of chemical energy; forexample, methane and hydrogen are oxidized to CO2 andwater, with oxygen available from local sulfates and metaloxides. Hydrogen sulfide is also frequently present and leadsto the production of water and metal sulfides; there may bemany other reactions of which we are not yet aware. Of allthe forms of life that we now know, bacteria appear torepresent the one that can most readily utilize energy from agreat 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 thatwere discovered first? After all, the discovery of these isrecent, and we may well expect that other locations that areharder to investigate would have escaped detection so far.

Bacteria can live at higher temperatures than any otherknown organisms; 110'C has been verified, and some biolo-gists consider that the upper temperature limit may be as highas 150'C (providing always that the pressure is sufficient toraise the boiling point of water above this temperature).There can be little doubt that venting of liquids and gases

from areas of the Earth's mantle beneath the crust is notlimited to a few cracks in the ocean floor. Indeed fossilized"dead" ocean vents have already been discovered (3), show-ing that the phenomenon is widespread and occurred indifferent geologic epochs. A similar supply of fluids seems tobe widespread also in land areas, where it is much harder toinvestigate, but it has been noted that many areas of base-ment rocks contain methane and other hydrocarbons. Thishas been seen in numerous mining and tunneling operationsfor a long time. Major fault lines have been noted to be highspots of hydrocarbon seepage (4). Hydrocarbons have alsobeen encountered in deep drilling in basement rocks, as in theSoviet superdeep well in the Kola peninsula and in the pilothole of the German Continental Deep Drilling Project. Thelarge quantities of methane hydrates (methane/water ices)found in many areas ofthe ocean floor, and thought to contain

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

more methane than all other known methane deposits (5, 6),suggest a widely distributed methane supply from below.

In land areas, deep in the rocks, it would be much harderto discover and investigate biological activity than in theocean vents. The pore spaces in the rocks are quite sufficientto accommodate bacterial life, and the rocks themselves maycontain many of the chemicals that can be nutrients togetherwith the ascending fluids. But, of course, there would be nospace for larger life forms. Just as bacterial life in the oceanvents would not have been discovered had the secondarylarger life forms not drawn attention to it, so any activebacterial life deep in the solid crust could have gone largelyunnoticed.The remains of bacteria in the form of molecules-

"hopanoids" (derived from hopanes)-a material comingfrom bacterial cell walls, have however been found in all ofthe several hundred samples of oil, coal, and kerogen (dis-tributed carbonaceous material in the crust) examined byOurisson et al. (7). These authors note the widespread orapparently ubiquitous presence of these molecules in thesedimentary rocks, and they give an estimate of the totalquantity as of the order of 1013 or 1014 tons, more than theestimated 1012 tons of organic carbon in all living organismson or near the surface. They also note the virtually identicalpattern of the chromatogram of these molecules in oil and incoal. Further they note that some of the molecules mostcommonly used to identify the presence of biological materialin petroleum, such as pristane and phytane, are not neces-sarily derived from plant chlorophyll as is commonly be-lieved, but could well be products of the same bacterialcultures as those that gave rise to the hopanoids. Thepresence of these biomolecules can therefore not be taken toprove a derivation of the bulk substance from surface bio-logical debris.What are the depths to which active bacterial life may have

penetrated? Could bacteria get down into the deep rocks?Would this represent just a minor branch of all the surfacebiological activity, or could it be comparable with it in thetotal amount of chemical processing caused by it? Howimportant would such life have been for the chemical evo-lution of the crust of the Earth?An upper limit of the temperature of 110-150'C would

place a limit on the depth of between 5 and 10 km in mostareas ofthe crust. The mere question of access to such depthsfor bacteria would be no problem. Even just the rate ofgrowth of bacterial colonies along cracks and pore spaces inwhich the requisite nutrients are available would take themdown in a few thousand years-a very small fraction of thetime span available. In fact, fluid movements in pore spaceswould provide still much faster transport. The tidal pumpingof ground water alone would be sufficient to distributebacteria down to 10 km in less than a thousand years.Probably longer times would have been required to allow forthe adaptation to the high temperatures.The total pore space available in the land areas of the Earth

down to 5 km de