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Authors: Stephen Jay Gould

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I shall present this new information by snippets in chronological order—a good way to mark successive claims for "internal" bacteria: first around deep sea vents, then in oil reservoirs, and finally in ordinary interior rocks, a finding that, at one extreme of interpretation, makes our surficial biota puny and exceptional, and suggests that interior bacterial biotas may be life’s standard and universal mode.

In the late 1970s, marine biologists discovered the bacterial basis of food chains for deep-sea vent faunas—and the unique dependence of this community upon energy from the earth’s interior, rather than from a solar source (as discussed on page 185). Two kinds of vents had been described: cracks and small fissures with warm water emerging at temperatures of 40° to 70°F; and large conical sulfide mounds, up to thirty feet in height, and spouting superheated waters at temperatures that can exceed 600°F. Bacteria had been identified in waters from small fissures of the first category, but, unsurprisingly, they "had previously not been thought to exist in the superheated waters associated with sulfide chimneys" (Baross et al., 1982, page 366).

But, in the early 1980s, John Baross and his colleagues discovered a bacterial biota, including both oxidative and anaerobic species, in superheated waters emanating from the sulfide mounds (also known as "smokers"). They cultured bacteria from waters collected at 650°F and then grew vigorous communities in a laboratory chamber with waters heated to 480°F at a pressure of 265 atmospheres. Thus, bacteria can (and do) live in high temperatures (and pressures) of waters flowing beneath the earth’s surface (Baross et al., 1982; Baross and Deming, 1983).

Writing about this work in a commentary for Nature, Britain’s leading journal of professional science, A. E. Walsby (1983) commented, "I must admit that my first reaction on reading the manuscript of Baross and Deming, arriving as it did on the eve of April Fool’s day, was one of incredulity." Walsby began his comment by noting that these deep-sea bacteria grow at a heat exceeding the title of Ray Bradbury’s famous story, Fahrenheit 451—the temperature at which paper ignites (and thought can therefore be more easily controlled by destruction of radical literature). Pressure is the key to an otherwise paradoxical situation. Life needs liquidity, not necessarily coolness. At the enormous pressures of the sea floor, water does not boil at temperatures tolerated by these bacteria. Baross and Deming end their article, prophetically as we shall see, by noting (1983, page 425):

These results substantiate the hypothesis that microbial growth is limited not by temperature but by the existence of liquid water, assuming that all other conditions necessary for life are provided. This greatly increases the number of environments and conditions both on Earth and elsewhere in the Universe where life can exist.

Then, in the early 1990s, several groups of scientists found and cultured bacteria from oil drillings and other environments beneath oceans and continents—thus indicating that bacteria may live generally in the earth’s interior, and not only in limited areas where superheated waters emerge at the surface: from four oil reservoirs nearly two miles below the bed of the North Sea and below the permafrost surface of Alaska’s North Slope (Stetter et al., 1993); from a Swedish borehole nearly four miles deep (Szewzyk et al., 1994); and from four wells about a mile deep in France’s East Paris Basin (L’Haridon et al., 1995). Water migrates extensively through cracks and joints in subsurface rocks, and even through pore spaces between grains of sediments themselves (an important property of rocks, known as "porosity" and vital to the oil industry as a natural mechanism for concentrating underground liquids-and, as it now appears, bacteria as well). Thus, although such data do not indicate global perva
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siveness or interconnectivity of subsurface bacterial biotas, we certainly must entertain the proposition that much of the earth deep beneath our feet teems with microbial life.

The most obvious and serious caution in these data emerges from another general property of bacteria: their almost ineradicable ubiquity. How do we know that these bacteria, cultured from waters collected at depth, really live in these underground environments? Perhaps they were introduced into deeper waters by the machinery used to dig the oil wells and boreholes that provided sites for sampling; perhaps (with even more trepidation) they just represent contamination from ubiquitous and ordinary bacteria of our surface environments, stubbornly living in laboratories despite all attempts to carry out experiments in sterile conditions. (A fascinating, and very long, book could be written about remarkable claims for bacteria in odd places—on meteorites, living in geological dormancy within 400-million-year-old salt deposits—that turned out to be ordinary surface contaminants. I well remember the first "proven" extraterrestrial life on meteorites, later exposed as ordinary ragweed pollen. Ah-choo!)

This well-known possibility sends shivers down the spine of any scientist working in this area. I am no expert and cannot make any general statement. I would not doubt (and neither do the authors of these articles) that some reports may be based on contamination. But all known and possible precautions have been taken, and best procedures for assuring sterility have been followed. Most persuasively, many of the bacteria isolated from these deep environments are anaerobic hyperthermophiles (jargon for bacteria growing at very high temperatures in the absence of oxygen) that could thrive in subterranean conditions, and cannot be laboratory contaminants because they die in ordinary surface environments of "low" temperature and pressure and abundant oxygen.

Writing in The New York Times on December 28, 1993, William J. Broad summarized the case nicely:

Some scientists say the microbes may be ubiquitous throughout the upper few miles of the Earth’s crust, inhabiting fluid-filled pores, cracks, and interstices of rocks while living off the Earth’s interior heat and chemicals. Their main habitats would be in the hot aquifers beneath the continents and in oceanic abysses, fed perpetually by the nutrients carried by the slow circulation of fluids like oil and deep ground water.

We might ask one further question that would clinch the case for underground ubiquity: Moving away from the specialized environments of deep-sea vents and oil reservoirs, do bacteria also live more generally in ordinary rocks and sediments (provided that some water seeps through joints and pore spaces)? New data from the mid-1990s seem to answer this most general question in the affirmative as well.

R. J. Parkes et al. (1994) found abundant bacteria in ordinary sediments of five Pacific Ocean sites at depths up to 1,800 feet. Meanwhile, the United States Department of Energy, under the leadership of Frank J. Wobber, had been digging deep wells to monitor contamination of groundwater from both inorganic and potentially microbial sources (done largely to learn if bacteria might affect the storage of nuclear wastes in deep repositories!). Wobber’s group, taking special pains to avoid the risk of contamination from surface bacteria introduced into the holes, found bacterial populations in at least six sites, including a boring in Virginia at 9,180 feet under the ground!

William J. Broad wrote another article for the Times (October 4,1994), this time even more excited, and justifiably so:

Fiction writers have fantasized about it. Prominent scientists have theorized about it. Experimentalists have delved into it. Skeptics have ridiculed it. But for decades, nobody has had substantial evidence one way or another on the question of whether the depths of the rocky earth harbor anything that could be considered part of the spectacle of life—until now.... Swarms of microbial life thrive deep within the planet.

Stevens and McKinley (1995) then described rich bacterial communities living more than three thousand feet below the earth’s surface in rocks of the Columbia River Basalt in the northwestern United States. These bacteria are anaerobic and seem to get energy from hydrogen produced in a reaction between minerals in the basaltic rocks and groundwater seeping through. Thus, like the biotas of the deep-sea vents, these bacteria live on energy from the earth’s interior, entirely independent of the photosynthetic, and ultimately solar, base of all conventional ecosystems. To confirm their findings in the field, Stevens and McKinley mixed crushed basalt with water free from dissolved oxygen. This mixture did generate hydrogen. They then sealed basalt together with groundwaters containing the deep bacteria. In these laboratory conditions, simulating the natural situation at depth, the bacteria thrived for up to a year.

Following a scientific tradition for constructing humorous and memorable acronyms, Stevens and McKinley have named these deep bacterial floras, independent of solar energy, and cut off from contact with surficial communities, SLiME (for subsurface lithoautotrophic microbial ecosystem—the second word is just a fancy way of saying "getting energy from rocks alone"). Jocelyn Kaiser (1995), writing a comment for Science magazine on the work of Stevens and McKinley, used a provocative title: "Can deep bacteria live on nothing but rocks and water?" The answer seems to be yes.

My colleague Tom Gold of Cornell University may be one of America’s most iconoclastic scientists. (One prominent biologist, who shall remain nameless, once said to me that Gold ought to be buried deep within the earth along with all his putative bacteria.) But no one sells him short or refuses to take him seriously—for he has been right far too often (we only threaten to bury alive the people we fear).

In a remarkable article entitled "The deep, hot biosphere" and published in the prestigious Proceedings of the National Academy of Sciences in 1992, Gold set out the full case (truly universal, or at least potentially so) for the importance of bacterial biotas deep within the earth. (He did this, characteristically, a few years before firm data existed for rich bacterial communities in ordinary subsurface rocks. But he was right again, in this factual claim at least, if not necessarily in all his implications. Gold began his case by asking, "Are the ocean vents the sole representatives of this [deep bacterial life], or do they merely represent the examples that were discovered first?")

Of all living things that might expand the range of life beyond conventional habitats of land and oceans, bacteria are the obvious candidates. They are small enough to fit nearly anywhere, and their environmental range vastly exceeds that of all other organisms. Gold writes: "Of all the forms of life that we now know, bacteria appear to represent the one that can most readily utilize energy from a great variety of chemical sources."

Gold then makes a key estimate—for my argument about domination of the modal bacter, at least—of possible bacterial biomass, given the vast expansion of range into rocks and fluids of the earth’s interior. Gold’s effort is, of course, another back-of-the-envelope calculation, and must be treated with all the caution always accorded to this genre (but remember that the estimates may also be too low, rather than inflated). A large num
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ber of assumptions must be made: How deep do bacteria live? At what temperatures? How much of rock volume consists of pore space where bacteria may live in percolating waters? How many bacteria can these waters hold? Since we do not know the actual values for any of these key factors, we must make a "most reasonable" estimate. If actual values differ greatly from the estimate (as they may well do), then the final figure may be very far wrong. (I trust that nonscientific readers will now grasp why, in this enterprise, we are satisfied with "ballpark" estimates that might be "off" by even an order of magnitude or two.)

In any case, Gold based his number for total bacterial biomass on reasonable, even fairly conservative, estimates for key factors—so if most rocks permeable by water do contain bacteria, then his figure is probably in the right ballpark. Gold assumes an upper temperature range of 230° to 300°F and a depth limit of three to six miles. (If bacteria actually live deeper, their biomass might be much higher.) He calculates the mass of water available for bacterial life by assuming that about 3 percent of rock volume consists of pore spaces. Finally, he estimates that bacterial mass might equal about 1 percent of the total mass of available underground water.

Putting all these estimates together, Gold calculates a potential mass of underground bacteria at 2 × 10
14
tons. This figure, he writes, is equivalent to a layer five feet thick spread out over the earth’s entire land surface—an amount of biomass, Gold states, that would "indeed be more than the existing surface flora and fauna." As a cautious conclusion to his calculation of underground bacterial biomass, Gold writes:

We do not know at present how to make a realistic estimate of the subterranean mass of material now living, but all that can be said is that one must consider it possible that it is comparable to all the living mass at the surface.

When one considers how deeply entrenched has been the dogma that most earthly biomass lies in the wood of our forest trees, this potentially greater weight of underground bacteria represents a major revision of conventional biology—and quite a boost for the modal bacter. Not only does the earth contain more bacterial organisms than all others combined (scarcely surprising, given their minimal size and mass); not only do bacteria live in more places and work in a greater variety of metabolic ways; not only did bacteria alone constitute the first half of life’s history, with no slackening in diversity thereafter; but also, and most surprisingly, total bacterial biomass (even at such minimal weight per cell) may exceed all the rest of life combined, even forest trees, once we include the subterranean populations as well. Need any more be said in making a case for the modal bacter as life’s constant center of maximal influence and importance?

But Gold does take one further, and equally striking, step. We are now fairly certain that ordinary life exists nowhere else in our solar system

for no other planetary surface maintains appropriate conditions of temperature and liquid water. Moreover, such earthly surface conditions are probably rare in the universe, making life an unusual cosmic phenomenon.

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