For centuries the primary source of life’s energy has been as well established as any precept in biology. Every high-school textbook proclaims what we all have accepted as intuitively obvious: All life depends ultimately on the Sun’s radiant energy. Nor has there been reason to doubt that claim until recently. But new discoveries of deep life—life-forms at the darkest ocean depths and microbes buried miles beneath Earth’s surface in solid rock, forever beyond the Sun’s influence—have toppled this comfortable certainty.

If science has taught us anything, it’s that cherished notions about our place in the natural world often turn out to be dead wrong. We observe that the Sun rises in the morning and sets at night. An obvious conclusion, reached by almost all observers until relatively recently in human history, is that the Sun circles the Earth. Yet we now know that sunrise and sunset are consequences of Earth’s rotation; Earth orbits the Sun, and we are not at the physical center of the universe. We observe mountains and oceans as grand unchanging attributes of the globe—on the scale of a human life, these features are for all intents and purposes permanent. Yet we have learned that through the inexorable processes of plate tectonics, every topographic feature on Earth is transient over geological time and that our war-contested political boundaries are destined eventually to disappear.

The great power of science as a way of knowing is that it leads us to conclusions about the physical universe that are not self-evident. Repeatedly, the history of science has been punctuated by the overthrow

of the obvious. Could our intuitive view of life’s original energy source be in error as well?

All living cells require a continuous source of energy. Without energy, organisms cannot seek out and consume food, manufacture their cellular structures, or send nerve impulses from one place to another. Lacking energy, they cannot grow, move, or reproduce. Reliable energy input is also essential to maintain the genetic infrastructure of cells, which are constantly subjected to damage by nuclear radiation, toxic chemicals, and other environmental hazards.

Metabolism, the means by which organisms obtain and use energy, is an ancient chemical process that takes place in every living cell, including all of the tens of trillions of cells in our bodies. Until recently, scientists claimed that the metabolic pathways of virtually all life-forms rely directly or indirectly on photosynthesis. At the base of the food web, we find plants and a host of one-celled organisms that use the Sun’s light energy to convert water and carbon dioxide into the chemical energy of sugar molecules (carbohydrates) plus oxygen. Plants manufacture carbohydrates, such as the starch of potatoes and the cellulose of celery, to build leaves, stems, roots, and other physical structures. They also process sugar molecules to provide a source of chemical energy that powers the plant cell’s molecular machinery.

While plants synthesize their own carbohydrates, animals and other nonphotosynthetic life higher up the food chain must find another source of sugar. That’s why we eat plants, or eat animals that eat plants. Plants synthesize sugar molecules and oxygen from water plus carbon dioxide. Our bodies convert sugar molecules along with the oxygen we breathe to produce water plus the waste gas carbon dioxide. There’s an elegant chemical symmetry to this story; the biological world seemed much simpler when the Sun was life’s only important energy source.

Our view of life on Earth changed forever in February 1977, when Oregon State University marine geologist Jack Corliss and two crewmates guided the submersible Alvin to the deep volcanic terrain of the East

Pacific Rise, 8,000 feet down. This undersea ridge off the Galápagos Islands was known to be a zone of constant volcanic activity associated with the formation of new ocean crust. Oceanographers have documented thousands of miles of similar volcanic ridges, including the sinuous Mid-Atlantic Ridge that bisects the Atlantic Ocean—the longest mountain range on Earth.

On this particular dive, just one of hundreds that Alvin had logged, the scientists hoped to locate and examine a submarine hydrothermal vent, a kind of submarine geyser where hot water jets upward into the cool surrounding ocean. What Corliss and crew discovered was a vibrant and totally unexpected ecosystem with new species of spindly albino crabs, football-sized clams, and bizarre 6-foot tubeworms. One-celled organisms also abounded, coating rock surfaces and clouding the water. These communities, thriving more than a mile and a half beneath the sea, never see the light of the Sun.

In these deep undersea zones, microbes serve as the primary energy producers, playing the same ecological role as plants do on Earth’s sunlit surface. These one-celled vent organisms exploit the fact that the cold oxygen-infused ocean water, the hot volcanic water, and the sulfur-rich mineral surfaces over which these mixing fluids flow are not in chemical equilibrium. This situation is similar to the disequilibrium between a piece of coal and the oxygen-rich air. Just as you can heat your house or power machinery by burning coal (thus combining unstable carbon and oxygen to make stable carbon dioxide), so too can these deep microbes obtain energy by the slow alteration of unstable minerals.

The unexpected discovery of this exotic ecosystem was news enough, but Corliss and his Oregon State colleagues soon tried to push the story further. They saw in the vents an ideal environment for the origin of life. Details of this story have become clouded by more than 20 years of sometimes revisionist history. Corliss claims the idea for himself: “I began to wonder what all this might mean, and this sort of naïve idea came to me,” he told an interviewer more than a decade later. “Could the hydrothermal vents be the site of the origin of life?” [Plate 5]

A different history emerges from others close to the story. According to John Baross, a former faculty colleague of Corliss and an expert on microbes in extreme environments, the hydrothermal vent theory of life’s origin was first proposed and developed by a perceptive Or-

egon State graduate student named Sarah Hoffman. She wrote the basic outlines of the hypothesis in 1979, as a project for a biological oceanography seminar taught by Charles Miller, another OSU oceanographer. Hoffman, in frequent consultation with Baross, developed the novel idea as it would appear in print. The two of them claim that the more senior Corliss seized the paper as his own, allowing them, as his coauthors, to expand and polish the prose to conform to the conventions of scientific publishing, after which he submitted the work and placed his name first on the author list. With three coauthors—Corliss, Baross, and Hoffman—the paper would forever be known as “Corliss et al.” Corliss would get the fame, while Hoffman and Baross were effectively relegated to footnote status.

Whoever deserves the credit, the hydrothermal-origins thesis is elegantly simple and correspondingly influential. Modern organisms do, in fact, thrive in deep hydrothermal ecosystems. Fossil microbes recovered from 3.5-billion-year-old hydrothermal deposits reinforce this observation. Even without the energy of sunlight, nutrients and chemical energy abound in hydrothermal systems. The OSU scientists saw hydrothermal systems as “ideal reactors for abiotic synthesis,” and they proposed a sequence of chemical steps for the potentially rapid emergence of life.

The controversial manuscript was not eagerly received; it bounced around for the better part of a year. First it was rejected by Nature, then by Science. At the time, Stanley Miller and his protégés dominated the origin-of-life research game, which had seen more than its fair share of quacks and crackpot theories. They were not about to let such unsupported speculation sully their field. Hydrothermal temperatures were much too hot for amino acids and other essential molecules to survive, they said. “The vent hypothesis is a real loser,” Miller complained to a reporter for Discover magazine. “I don’t understand why we even have to discuss it.”

Miller’s followers found other good reasons to attack the paper. Corliss and co-workers had the ancient ocean chemistry all wrong, they said. Modern hydrothermal ecosystems rely on oxygen-rich ocean water, whose composition is an indirect consequence of plants and photosynthesis. The prebiotic ocean would not have been oxygen-rich, so the proposed life-sustaining chemical reactions would have proceeded slowly, if at all. The bottom line? Decades of Miller-type experiments

confirm what is intuitively obvious: Life began at the surface, so why confuse the issue?

Eventually the Corliss, Baross, and Hoffman manuscript was published, in a supplement to the relatively obscure periodical Oceanologica Acta, a journal that not one in a hundred origin-of-life researchers would see. Nevertheless, good ideas have a life of their own, and copies of the paper, entitled “An Hypothesis Concerning the Relationship Between Submarine Hot Springs and the Origin of Life on Earth,” began circulating. I have seen dog-eared underlined photocopies of copies of copies on several colleagues’ desks, and I have a pretty battered copy of my own.

New support for the idea gradually consolidated, as hydrothermal ecosystems were found to be abundant along ocean ridges in both the Atlantic and Pacific. It was realized that at a time when Earth’s surface was blasted by a continuous meteorite bombardment, deep-ocean ecosystems would have provided a much more benign location than the surface for life’s origin and evolution. New discoveries of abundant primitive microbial life in the deep continental crust further underscored the viability of deep, hot environments. By the early 1990s, the deep-origin hypothesis had become widely accepted as a viable, if unsubstantiated, alternative to the Miller surface scenario.

Of the three authors, only John Baross remains active and influential in the field. In 1985, he accepted a professorship at the University of Washington, where he has developed a leading research program on hydrothermal life. His work on deep-sea-vent microbes, often in collaboration with his wife, Jody Deming, who is also a professor of oceanography at the University of Washington, has placed Baross at the forefront of the highly publicized research field of “extremophile” microbes. Sarah Hoffman’s graduate work in geochemistry was interrupted by illness, and, after her recovery, she pursued a singing career. As for Corliss, always a bit idiosyncratic, in 1983 he left Oregon for the Central European University in Budapest, where he worked briefly on the deep-origins hypothesis, but soon took up research in the more abstract field of complex systems. After a 3-year stint as director of research at the controversial Biosphere 2 environmental station in Arizona, he returned to Budapest, having abandoned studies of the deep ocean.

Following the revolutionary hydrothermal-origins proposal, numerous scientists began the search for life in deep, warm, wet environments. Everywhere they looked, it seems—in deeply buried sediments, in oil wells, even in porous volcanic rocks more than a mile down—microbes abound. Microbes survive under miles of Antarctic ice and deep in dry desert sand. These organisms appear to thrive on mineral surfaces, where interactions between water and chemically unstable rocks provide the chemical energy for life.

One of the most dramatic and difficult pursuits involves deep drilling for life in solid rock. The oil industry has perfected the practice of deep drilling, thanks to decades of experience and vast infusions of cash. They can penetrate several miles into the Earth, drill at angles and around obstacles, and cut through the hardest known rock formations in their quest for black gold. So the problem for geoscientists looking for microbes a mile or more down isn’t how to get there, it’s how to get there without contaminating the drill hole with hoards of surface bugs. Bacteria are everywhere—in the air, in the water, and in the muck used to lubricate and cool diamond drill bits as they cut through layers of rock. It’s relatively easy to bring up rock cores from a couple of miles down, but those slender cylinders of rock will have already been exposed to surface life by the drilling process. What to do?

The commonest retrieval trick is to add a colorful dye or other distinctive chemical tracer to the lubricating fluid. When drillers extract a deep core, it becomes obvious whether or not the rock has been contaminated in the process. Porous sediments or highly fractured formations soak up the dye and thus prove unsuitable for analysis, but many rocks turn out to be impermeable and thus are ideal for recovering deep life.

The search for subsurface microbes began in earnest in 1987, when the Department of Energy decided to drill several 500-meter-deep boreholes in South Carolina near the Savannah River nuclear processing facility. As cores were brought to the surface, drillers quickly isolated them in a sterile plastic enclosure with an inert atmosphere. Researchers then cut away the outer rind of the drill core to reveal pristine rock samples, which were shipped to analytical facilities across the country. The results were spectacular. The deep South Carolina sediments were loaded with microbes that had never seen the light of day.

Subsequent drilling studies have revealed that microbes live in every imaginable warm, wet, deep environment—in granite, in basalt on land and basalt under the ocean, in all variety of sediments, and also in metamorphic rocks that have been altered by high temperature and pressure. Anywhere you live, drill a hole down a mile and the chances are you’ll find an abundance of microscopic life.

Earth’s deep mining and tunneling operations provide the new breed of geobiologist with an invaluable complement to drilling. Mine tunnels have the advantage that researchers can visit microbial populations in their native habitat. Earth’s deepest mines, the fabled gold mines of South Africa’s Witwatersrand District, have thus become the site of the heroic and potentially dangerous efforts of Princeton geologist Tullis Onstott.

The East Driefontein Mine, located about 60 miles southwest of Johannesburg, is a vast network of underground workings, reaching more than 2 miles into the crust. A small army of miners labor around the clock for gold. Despite one of the largest air-conditioning systems in the world, these deep tunnels remain at an oppressive 140°F from the heat of Earth’s interior, while air pressure is twice that of the surface. Onstott learned the dangers of the place on his first descent: “It was ‘Don’t step there, don’t touch that,’” he told a writer for the Princeton Weekly Bulletin. “All I knew is that it was deep and dark and hot.”

Every so often, as miners blast new adits, a small flow of water appears—groundwater that has spent countless thousands of years filtering down from the surface and has accumulated in small cracks and fissures, nurturing a tenuous ecosystem of microbial life. Onstott’s team, typically a half-dozen young and hearty students and postdocs, camp at the surface with a functional array of sterile sample-collection hardware at hand. When news of a fresh water flow comes in, they scramble to the site, though the miles of elevators and tunnels can take almost an hour to traverse. They have to work fast, both to avoid disruption of the mining routine and because prolonged exposure to the hellish conditions can kill them.

They photograph the site, record its location and geological setting, and collect as many gallons of water as possible fresh from the

point of flow. They benefit from the seep’s positive water pressure, which prevents much back contamination from the miners’ activities or their own collection efforts. Exhausted and sweating profusely, they lug the heavy water-filled bottles to the surface for further investigation.

Remarkably, every single sample from Earth’s deepest mines holds microbes that have never seen light, surviving on a meager supply of underground chemical energy. Such deep life lives at a sluggish pace that defies our experience. Isotopic measurements reveal that a single cell may persist for thousands of years, “doing” almost nothing before dividing into two. Colonies of organisms commonly remain isolated from the surface for millions of years. So tenuous are the chemical resources of these deep rocks that reproduction and growth are luxuries seldom indulged. By the same token, deep rocks provide an unvarying safe and reliable environment: no predators, no surprises—unless of course a miner happens to blast into your rocky home of a million years!

The abundance of subterranean one-celled creatures, thriving far from the light of the Sun, inspires the imagination and hints at novel scenarios for life’s origin. Of all the scientists in pursuit of deep life, none displayed greater imagination than the late brilliant and pugnacious iconoclast Thomas Gold.

Austrian-born Tommy Gold began his scientific career as an astrophysicist in Britain, but in 1959 he was lured to Cornell University to head the Center for Radiophysics and Space Research. He would achieve lasting scientific fame with his inspired theory that pulsars, steady pulsating radio sources discovered in 1967, are actually rapidly rotating neutron stars. Many honors, including election to the Royal Society of London and the National Academy of Sciences, soon followed.

Most scientists would have been content to excel in one chosen area, but Gold throughout his career repeatedly ventured into new and controversial academic domains. In the 1940s, he conducted experiments on hearing and the structure of the mammalian inner ear. Speculative papers on dramatic instabilities of Earth’s rotation axis, on steady-state cosmological models of the universe, and on the potential

danger to astronauts of deep powdery lunar soils peppered his lengthy curriculum vitae.

In 1977, Gold, by then a safely tenured professor at Cornell, rattled the well-established field of petroleum geology. Geologists had long declared that petroleum is a fossil fuel, formed when huge quantities of decaying cells accumulate over millions of years, to be buried and processed by Earth’s heat and pressure. The evidence is overwhelming: Petroleum occurs in sedimentary layers that once held abundant life; petroleum is rich in distinctive biological molecules; petroleum’s carbon isotopes also point to a biological source. Armed with these and a dozen other lines of evidence, the case for fossil fuels was open and shut.

Gold disagreed. Petroleum holds lots of distinctive biomolecules, to be sure, but oil fields also contain, along with methane, an abundance of helium gas—a light gas that quickly escapes into space and so could only come from deep within the Earth. How could one reconcile the mixing of deep helium with surface biology? Gold’s conclusion: The organic molecules that eventually become petroleum are produced deep underground by purely chemical processes and are then modified by the action of subsurface microbes.

In this scenario, vast sources of primordial hydrocarbons—the major molecular components of oil—exist in Earth’s mantle. Because they are lighter than the surrounding rocks, these hydrocarbons slowly but surely rise toward the surface, constantly refilling petroleum reservoirs. In Gold’s heretical view, oil is thus a renewable resource instead of a finite one built up over millions of years by the burial and decay of once-living cells. In an extraordinary move, Gold first published this novel idea as an op-ed piece in the June 8, 1977, issue of the Wall Street Journal. An oil-hungry nation in the midst of an energy crisis took considerable notice of the radical hypothesis.

A scientific theory is useful only if it is testable, and Gold soon proposed a test of dramatic proportions. Gold’s oil-from-below hypothesis predicts that great oil fields should arise equally in many different types of rock, but all known petroleum has been found in layers of exactly the kind of sedimentary formations that would have collected abundant remnants of past life. Gold countered, logically, that petroleum geologists never look for oil anywhere but in those sedimentary formations. Perhaps, he suggested, immense new oil fields were waiting to be found in igneous and metamorphic rock.

Armed with his provocative theory and a persuasive, dynamic oratorical style, he presented a simple (and expensive) proposal to the Swedish State Power Board in 1983. Drill an oil well in solid granite—the last place on Earth a petroleum geologist would look. He had targeted a unique and tempting granitic mass, the Siljan Ring impact site in central Sweden. This highly fractured granite body, formed 368 million years ago when an asteroid shattered the crust, holds tantalizing hints of petroleum in the form of carbon-filled cracks and flammable methane seeps. Gold’s enticing rhetoric, amplified by increasing optimism from Dala Deep Gas, the company formed to do the drilling, lured energy-poor Swedes into spending millions of dollars on exploratory holes.

Seven years and $40 million later, a 6.8-kilometer-deep hole had produced only modest amounts of oil-like hydrocarbons and methane gas—a small enough yield for oil experts to say “I told you so,” but large enough to convince Gold that his theory was right. Where else, he asked, could that trace of organic molecules have come from? Nevertheless, most scientists saw the Siljan experiment as a failure, and no one is likely to drill for oil in granite again, at least anytime soon.

The modest production of methane gas and smelly, oily sludge from the Swedish wells inspired Gold to elaborate on his theory. Extrapolating far beyond his peers, he described “the deep hot biosphere” in several articles and a popular 1998 book of that title. The vast, deep hydrocarbon reserves at the heart of Gold’s 1977 hypothesis provide a wonderful food source for deep microbes, which coincidently leave their biological overprint on the otherwise abiotic oil. In entertaining prose, he reviewed the growing and accepted body of evidence for deep life in many types of rock—all very reasonable stuff. Gold’s conclusion: Deep microbial life, much of it nourished by upwelling hydrocarbons, accounts for fully half of Earth’s total biomass. Though living cells represent a tiny fraction of Earth’s total rock mass, the volume of rock is so vast—a few billion cubic kilometers—that it shelters astronomical numbers of microbes. Inevitably, our view of life has been skewed because these microscopic life-forms lie completely hidden from everyday view.

In April 1998, I invited Gold to visit the Geophysical Lab and present his ideas at our regular Monday morning seminar. Seemingly unfazed by more than two decades of impassioned objections to his views, he delivered a polished and forceful account of many lines of

evidence that petroleum is abiotic and rises from the depths. Geology, biology, thermodynamics, experiments on organic molecules, carbon isotopes, observations of diamonds, and, of course, the chemical properties of petroleum itself all came into play. Knowing our special interest in life’s origins, he underscored the possible role of this deep hydrocarbon source in supplying critical molecules for prebiotic processes. Perhaps, he posited, life arose from those deep sources of organic molecules. Throughout the entertaining lecture, he bolstered his controversial conclusions with rhetorical flourishes more suited to a courtroom than a scientific seminar (“the only possible explanation,” “no question remains,” the evidence “persuades one completely,” and the like).

I doubt that anyone was persuaded completely, but we had to admire his creativity and conviction. And Tommy Gold helped to remind us all, once again, how much we don’t know about the interior of our planet just a few miles beneath our feet.

If so many organisms exist beyond the Sun’s radiant reach, then geothermal energy, and the abundant chemically active mineral surfaces that are synthesized in geothermal domains, must be considered as a possible triggering power source for life. To be sure, sunlight remains the leading contender for life’s original energy source. The vast majority of known life-forms do rely, directly or indirectly, on photosynthesis. In many scientific circles, a surface origin of life in a nutrient-rich ocean, under a bright Sun, remains the seemingly unassailable conventional wisdom.

But that nagging problem of macromolecular formation remains. Most known living species depend on the Sun directly or indirectly, but the Sun’s harsh ultraviolet radiation inhibits the emergence of the larger multimolecular structures on which all organisms depend. Furthermore, if the earliest life of almost 4 billion years ago was confined to the sunlit surface, how did it escape the brutal, sterilizing final stages of bombardment by asteroids and comets? As Gold said over and over again, Earth’s surface, bathed in solar radiation and blasted by lightning, is the truly extreme environment.

And there’s another reason to look closely at the possibility of hydrothermal origins. If life is constrained to form in a sun-drenched

pond or ocean surface, then Earth, and perhaps ancient Mars or Venus, are the only possible places where life could have begun in our solar system. If, however, living cells can emerge from deeply buried wet zones, then life may be much more widespread than previously imagined. The possibility of deep origins raises the stakes in our exploration of other planets and moons.

Jupiter’s fourth largest moon, Europa, presents a particularly promising target for exploration. According to recent observations, Europa is covered with a veneer of ice about 10 kilometers thick, covering a deep ocean of liquid water. Hydrothermal activity on the floor of that ocean might be an ideal environment for life-forming chemistry. Saturn’s largest moon, Titan, is another intriguing world. Though much colder than Earth, Titan has an organic-rich atmosphere slightly denser than Earth’s and, like all large bodies, its own sources of internal heat energy.

The idea that life may have arisen in a deep, dark zone of volcanic heat and sulfurous minerals flies in the face of deeply ingrained religious metaphors. To many people, the Sun represents the life-giving warmth of heaven, while sulfurous volcanoes are the closest terrestrial analog to hell. How could life have come from such a dark, hostile environment?

Nature is not governed by our metaphors, however cherished they may be. Life as we know it demands carbon-based chemicals, a water-rich environment, and energy with which to assemble those ingredients into a self-replicating entity. Ongoing laboratory experiments that simulate deep conditions as well as those on the surface—coupled with observations of environments elsewhere in the solar system—will be the ultimate arbiters of truth.