As a kid growing up I learned that all Earth life relied either directly or indirectly upon sunlight and an atmosphere with O2, textbook stuff. Then in the late 1970’s, biologists discovered Riftia pachyptila, chemosynthetic tube worms, living around black smoker vents at the the bottom of the Pacific Ocean not far from the Galapagos Islands, the birthplace of Darwin’s theory of evolution by natural selection.

Life has never been the same since.

In the early 1990’s Bacillus infernus, a bacterium, was discovered 10,000 feet beneath a farmer’s field in Virginia, where it or its ancestors had been living for 200 million years. Since then entire ecosystems have been uncovered residing miles beneath the surface in deep fractures sustained indefinitely by nothing more than the desultory decay of radiogenic uranium, thorium and potassium or the anemic oxidation of iron-bearing minerals.

With all of this life flourishing in what was previously believed to be a sterile dominion, you can’t help but look at the images of the ancient Martian surface and wonder if life also exists beneath its frozen, dessicated surface. If you had openly asked a question like that in the 16th century you would have been burned at the stake, like Giordano Bruno, an Italian Dominican friar, philosopher and the first astrobiologist. More than a hundred years ago, Percival Lowell believed that he could see evidence of an extraterrestrial civilization living on the surface of Mars, but that optical illusion, along with his scientific credibility, was dispelled within fifteen years of his discovery. In 1901 H. G. Wells, a contemporary of Lowell, published The First Men in the Moon, in which he constructed a fantastically sophisticated society of insect-like creatures, Selenites, living beneath the lunar surface. Since then, the concept of extraterrestrial subsurface life has figured frequently in science fiction novels and movies, even episodes of Star Trek and Star Trek: The Next Generation. It is certainly true that if you burrow miles into the Moon or Mars, you will reach a temperature at which fresh liquid water, the essential ingredient for life as we know it, can exist.

But can life survive miles beneath a planet’s surface for billions of years even when that surface is inimical to it? To find out, our team went miles beneath the surface of our own planet, into the mines of South Africa where gold is extracted from the 3 billion year old sedimentary and volcanic rock of the Witwatersrand Basin. This basin has not been metamorphosed since a meteor impacted it 2 billion years ago, creating the colossal Vredefort Impact structure. In the fissures and crevices workers intersected during ultra-deep mining we found saline water that was tens to hundreds of millions of years old, full of hydrogen and methane gas generated by radiation and a natural form of Fischer-Tropsch organic synthesis. And in that water we found complex communities of life forms busily mining nutrients and energy from the rock.

The bedrock of the communities were chemolithoautotrophic Bacteria and Archaea that were fixing CO2 and N2 to make biomass. Feeding off their metabolic waste were other chemolithotrophs engaged in a syntrophic dance by excreting their own waste products to be recycled by the primary producers. Even more abundant were the viruses that were shuttling snippets of genes to be incorporated into the evolving microbial genomes. The most dramatic discovery was the presence of multicellular nematodes feeding on the bacteria and reproducing asexually. Similar subsurface communities and, in some cases, the same species have been reported in seafloor vents even though this part of South Africa has been covered by ocean water for 2.5 billion years. One of our primary producers was bacterial species found to be chemotactic and apparently migrating hundred of kilometers beneath the surface. We named it Desulforudis audaxviator. Audaxviator is derived from Jules Verne’s book, Journey to the Center of the Earth, and is Latin for “bold traveller.”

The longevity and internal sustainability of subsurface ecosystems on Earth means that if life emerged early on Mars, then there is no reason to believe it would not be present beneath the surface today. Drilling down miles through frozen rock to reach liquid water on Mars to obtain samples of the subsurface biosphere will likely have to await human colonization of that planet. But many other worlds such as Europa, Enceladus, and even Pluto, have liquid water at depth, an in the case of Europa and Enceladus vent this water to space as plumes that could be readable sampled for life. Yet these planetary bodies differ from Mars in that their surfaces were never habitable for life as we know it. For life to exist beneath their icy crusts, the processes leading to the origin of life have to be able to occur in the absence of sunlight.

As we do not have a complete picture of how life originated on the Earth, but rather just a few pieces of the puzzle, we cannot say with certainty if life can originate beneath the surface of a world. The late physicist Tommy Gold hypothesized that life may have originated beneath the surface of the Earth and subsequently rose to colonize the surface as ocean-evaporating meteorite impacts waned and the surface became more hospitable. Today regions of ancient continental crust exist where DNA life forms and their remains have been completely eradicated by geological heating in the past, or “paleopastuerization.” They are now cool and contain pockets of saline water that are habitable, and in some cases have been isolated from the surface for hundreds of millions to billions of years.

If Tommy Gold was right, then these Darwinian “warm little ponds” may be the locus of ongoing abiotic synthesis of building blocks for life, peptides and nucelotides. If there were any place on this planet where life forms exist as a “shadow biosphere” and do not have the signature ribosomal RNA, it would be the deep subsurface of our planet. Such a discovery would have enormous implications for life elsewhere in our solar system. We only have to go hunt for them.