“THE first ten million years were the worst,” said Marvin, “and the second ten million years, they were the worst too. The third ten million years I didn’t enjoy at all. After that I went into a bit of a decline.”
Poor old Marvin the Paranoid Android, left to wait for eternity in a car park at the Restaurant at the End of the Universe. But if the ordeal of this Douglas Adams character seems trying, consider the real-life fate of microorganisms discovered buried in sediment under the South Pacific in 2010. They had been there for around 100 million years.
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And they were still alive – barely. Their metabolisms had slowed to a crawl and they were using what little energy they had just to stay in the game. But alive they were. “They’re definitely breathing!” says at the University of Rhode Island, who discovered them.
The presence of ancient, zombie microbes entombed deep under Earth’s surface may seem surprising, but D’Hondt and his crew would have been more surprised not to find them. Wherever we drill into the planet, we find life. And while some is zombie-like, most is not. Life underground is rich, dynamic and deeply strange. What it teaches us has important implications for our concept of life itself, not just here on Earth, but on other planets too.
For centuries, nobody thought that Earth’s crust was anything other than inanimate rock. The first hint to the contrary came in 1926, when US geologists extracted water from oil wells nearly 600 metres down and discovered bacteria swimming inside. If true, this would have been a remarkable discovery. Instead, it was widely dismissed as contamination.
Attitudes towards deep life changed in 1977 when scientists aboard a US research submersible discovered hydrothermal vents on the floor of the Pacific Ocean. These “black smokers” were teeming with life fuelled by chemical energy from way underground.
In 1992, inspired by these discoveries, boundary-breaking astrophysicist published a paper called “The deep, hot biosphere”. He reasoned that similar energy sources wouldn’t be confined to vents, and speculated that Earth’s subsurface was teeming with microbial life living in the pores between rocks. The size of this biosphere might equal that of surface life, he said, and such organisms “may be widespread among the planetary bodies of our solar system”.
A quarter of a century on, Gold’s speculations have been vindicated – at least on Earth. Drilling projects on land and at sea, expeditions to deep mines and surveys of ocean vents have confirmed the existence of a deep, hot biosphere of amazing size and diversity.
“There’s an entire living realm beneath our feet,” says , executive director of the at the Carnegie Institution for Science in Washington DC. “A vast biosphere that’s invisible, not just because it’s microscopic, but because it’s literally in solid rock.”
“It’s massive,” says , a deep-life researcher at the Flatiron Institute in New York. She recently compiled data from hundreds of studies around the world to come up with an . Her conclusions are staggering: its volume is twice that of all the oceans combined, about 2 billion cubic kilometres, and it contains an estimated 1030 microbial cells. That is 70 per cent of all microbial life on Earth. “The subsurface biosphere is the largest biosphere on the planet and holds the majority of microbial life,” says Magnabosco.
“Having drilled more than 4 kilometres into the crust under land, scientists have still never hit sterile rock”
Unsurprisingly given its inaccessible location, the deep biosphere remains largely unknown. “We’re getting snapshots, but compared to pretty much any other environment on Earth, we have sampled very little because so much effort has to go into creating a borehole, or drilling a deep drill core out in the ocean or looking at a mine,” says , a geomicrobiologist at the University of Tennessee, Knoxville. However, with improvements in drilling technology and DNA sequencing, she and others are gradually revealing a biosphere some call the “subterranean Galapagos”.
Almost all deep life is simple, single-celled organisms, mostly bacteria and archaea plus a few microeukaryotes and fungi, living in cracks or pores in the rock – although there are a few multicellular animals too. Most have yet to be formally identified. “We call it ‘dark microbial matter’,” says , a geomicrobiologist at Princeton University.
As far as we know, this biosphere extends around the world, under land and oceans alike. It starts a few metres below the surface and goes way, way down.
The limits of life
Having drilled more than 4 kilometres into the crust under land and 2.5 kilometres into the seabed, scientists have still never hit sterile rock. The deepest living biological samples in Magnabosco’s survey were taken from about 5 kilometres down at drill sites in China and Sweden. Everybody agrees that there has to be a cut-off point somewhere, but where it is remains unknown. “At some point, there should be temperatures, and possibly also pressures, that limit life because molecules fall apart,” says Lloyd.
The main limiting factor appears to be heat. On average, the temperature of continental crust rises by about 25°C for every kilometre you go down. In oceanic crust, the gradient is less steep, about 15°C per kilometre.
That would quickly overwhelm the heat tolerance of multicellular organisms, but microbes are made of sterner stuff. Many extremophiles can tough out temperatures well in excess of 100°C, and where high pressure prevents water from boiling, they can go even higher. The current record holder is the archaeon Methanopyrus kandleri, which lives at 110°C in hydrothermal vents in the Gulf of California and has been cultured at 122°C in the lab. The record in the wild is set by another species of vent archaeon, Geogemma barossii, which grows and replicates at 121°C.
It is conceivable that deep in the crust, at extreme pressures, microorganisms survive at even greater temperatures, says Hazen, maybe as high as 150°C.
If so, that would push the theoretical threshold to about 6 kilometres deep on land and 10 kilometres beneath the ocean, perhaps even more. “If you have places with relatively cool rock, you might be able to go down deeper than 10 kilometres and still have temperatures within that limit,” says Hazen. In some thick, ancient crust, 122°C isn’t reached until 23 kilometres down, according to Magnabosco. That pushes the envelope even further, assuming that the microbes can take the pressure.
Finding out for certain, though, is way beyond the reach of current drilling technology. The deepest hole ever sunk is the Kola Superdeep Borehole in Russia, near the border with Norway. Begun in 1970, its scientists aimed to reach 15 kilometres. After grinding away for nearly 20 years, they were forced to stop short, at 12,262 metres, scuppered by higher-than-expected temperatures in the borehole.
Temperature and pressure are big challenges, but they are far from the only ones you face if you live deep underground.
Rock eaters
Another challenge is energy. The two main lifestyles on the surface – photosynthesis and heterotrophy, aka eating food – rely on the presence of light and either organic matter or oxygen. Far below the surface, these are rarely on offer. Instead, microorganisms have to open a box of metabolic tricks. “There are some really novel biochemistries,” says Hazen.
In some places, there is enough organic matter – often fossilised hydrocarbons – to support communities of heterotrophic microbes. Most of these are anaerobic, replacing oxygen with nitrate, sulphate or metal ions and generating myriad waste products for other microbes to feast on.
But by far the most common deep lifestyle is autotrophy, which means making your own food. Under the earth, microbes use the rock itself as a source of energy. Under intense heat and pressure, chemical processes generate energy-rich inorganic molecules that microbes can break down to produce energy. Collectively, these organisms are known as chemolithotrophs, which literally means “chemical rock eaters”.
Almost any inorganic compound can be used as a source of energy, but the most important is hydrogen. This is produced from a range of reactions between rocks and water, as well as from the splitting of water by Earth’s background radiation and from silicate rocks being crushed by tectonic activity.
Hydrogen-eaters also produce waste products that other microbes can consume. The subsurface ecosystem is thus organised into complex food chains, with primary producers at the bottom and networks of consumers feeding off their waste, and that of others. There are also apex predators, sometimes microbe-eating multicellular worms (see “The greatest”).
Nonetheless, it is an environment where the pace of life is slow. “In some places, life is surviving on less energy than we thought possible,” says Lloyd. “I think this changes our conception of how biology works, to be more in step with geological rhythms and processes, not the fast timescales that the surface world seems to function on.” And unlike ecosystems on the surface, this one is pristine. “This deep, subsurface world contains one of the very few ecosystems not yet pervasively altered by humans,” says D’Hondt.
Given the metabolic creativity necessary to live under such conditions, many of the microbes are new to science. “There’s so much diversity,” says Lloyd.
Some microbes belong to previously unknown groups right up to the phylum level: the taxonomic equivalent of discovering arthropods or molluscs. “We’re invariably surprised by what we find,” says Onstott.
It is even possible that an entirely new domain of life is awaiting discovery, says of the Marine Biological Laboratory in Massachusetts, who is co-chair of the Deep Carbon Observatory’s Deep Life project. At present, biologists recognise just three domains – eukaryotes, bacteria and archaea. The discovery of the third of these in 1977 led to a major revision of the tree of life. A fourth would lead to a similar revolution.
The diversity is also geographical. Just as on the surface, there are a handful of global species, but most are local. What lives where depends on the environment and the available energy sources.
The biggest difference is between terrestrial and marine environments, says Magnabosco. Marine sediments all tend to be quite similar, maybe because they are saturated with water, whereas terrestrial ones depend on the type of rock. “There are many different rock types – granite, basalt, sandstones, clays – which all host very different microbial communities all doing different types of metabolism,” says Magnabosco.
Some regions are rich and fecund, in a similar way to the Amazon. Others are deserts with just a few species. “In some ecosystems, there’s only a single kind of organism, which is kind of an alien concept,” says Hazen.
Even more alien, these systems can be entirely separate from life as we know it. “Some of these deep microbial domains seem to have been isolated from the surface for very, very long periods of time,” says Hazen. This is perhaps the most jaw-dropping feature of deep life: in places, it is an entirely separate biosphere, running its own affairs with no connection whatsoever to life upstairs.
“Life could have started underground and then spread upwards”
One of the biggest implications is for our understanding of life’s origins. A tantalising possibility is that the isolated subterranean ecosystems are descended from what biologists call a “second genesis”: an origin-of-life event separate from the one that gave rise to surface life. As yet, however, this doesn’t appear to be the case. All the microbes described so far use the same genetic code and biochemistry as life above ground, so by inference are descended from the same common ancestor, says Hazen.
But what cannot be ruled out is that life got started underground and then spread up to the surface. “Reactions in the subsurface give rise to all the biomolecules that are necessary to support life,” says Lloyd. “As we learn more about the life that is down there, we are looking at it with an eye to determining whether it could be the origin of life too.”
If so, that would have gigantic implications for astrobiology, the study of life on other planets. Plenty of other bodies in the solar system and beyond have a subsurface not unlike Earth’s. If life got going underground – and has prospered there for the best part of 4 billion years – why not on Mars or other rocky planets, even ones with no sunlight?
According to Onstott, there are regions on Mars where subsurface conditions are very similar to places on Earth with abundant deep life. And you don’t even have to posit an underground origin, he says. “On early Mars, surface conditions existed under which life could have emerged. It could quickly have migrated downwards into the subsurface.”
For the foreseeable future, this remains speculation. NASA’s next mission, Mars 2020, plans to drill into the surface to search for signs of life, but not deep enough to reach a subsurface biosphere. We will have to wait for another mission – probably a crewed one – to get answers, says Onstott.
But why stop at Mars? “Anywhere where there’s enough heat to generate a fluid environment at depth, you might find life,” says Onstott. “You could go to Mercury, to the southern polar regions of the moon or out to Pluto. There’s even talk of life on Ceres.”
Even if deep life is confined to Earth, many new discoveries await us. The Deep Carbon Observatory has only been running for a decade and has merely scratched the subsurface.
“I think it’s safe to say that the discoveries that have been made are mind-boggling and incredibly exciting,” says Hazen. “They open our eyes to a new kind of life.”
The greatest
The underground biosphere is pretty amazing. Here are some of its record-breaking inhabitants
Hottest
Until recently, the record holder was an archaeon or single-celled microorganism called Pyrolobus fumarii, discovered on the wall of a hydrothermal “black smoker” in the mid-Atlantic ridge in 1996. It grows optimally at 106°C and can survive at 113°C. It has since been bested by Geogemma barossii, a methane-producing archaeon discovered in a hydrothermal vent on the Juan de Fuca ridge in the Pacific Ocean. It can grow and replicate at 121°C.
Biggest
In 2011, a team reported finding a nematode worm 1.3 kilometres below ground in a South African gold mine. It was later confirmed that this was indeed its natural habitat, where it fed on microorganisms. Half a millimetre long, Halicephalobus mephisto is the monster of the subsurface world. “It exists at the upper temperature limit for multicellular organisms,” says Tullis Onstott, part of the team that made the find.
Oldest
In 2010, the scientific drilling ship JOIDES Resolution, used by the International Ocean Discovery Program, bored deep into sediments under the South Pacific gyre. In its samples were microbes trapped in sediment that was at least 100 million years old. Nobody is entirely sure how old the organisms are, but analysis suggests they are probably several million years old. Scraping by on increasingly scarce scraps of organic matter buried alongside them, they can do little more than hunker down. “They’re living lives of quiet desperation,” says Steven D’Hondt at the University of Rhode Island, who discovered them.
Deepest
The deepest signs of life seen so far come from about 7 kilometres underground, from the Kola Superdeep Borehole in Russia. But the project wasn’t explicitly about biology and the discovery isn’t considered watertight. The deepest organisms to be properly characterised are a mixture of bacteria and archaea from a 5-kilometre borehole in China. Microbes have also been discovered 2.5 kilometres under the sea floor. “Maybe that doesn’t sound that impressive as a distance because we’re used to thinking of lateral distances, but when you’re drilling down a deep core, that is an impressive feat,” says Karen Lloyd, a microbiologist at the University of Tennessee, Knoxville.
Most exclusive
Around 2.8 kilometres below the surface in South Africa’s Mponeng gold mine is one of the most peculiar ecosystems ever discovered. More than 99.9 per cent of the organisms in it are a single species, the bacterium Desulforudis audaxviator, making it the world’s only known one-species ecosystem.
