Visiting this hidden kingdom requires a little preparation. A bright orange jumpsuit, a self-breather in the unlikely event of fire, a hard hat, a flashlight, and, of course, a backpack full of tubes, sterile shovels, and poles—not mining equipment, but the carefully selected tools of a microbiologist seeking life deep below the surface of the Earth.
An orderly procession of miners, and their small collection of scientists behind, heads single file through the thud of large metal doors to the top of the shaft, where the cage awaits them. Messages such as “Don’t be daft in the shaft” and “Act your age in the cage” scream out from the beams above the shaft. Those health and safety officials really know their stuff, and soon we are carried along by their enthusiasm (“Safety and science, it’s an alliance” was the best I ever came up with).
The miners and scientists huddle into the cage, a double-decker affair, and the wire door slams shut. With a jolt, the cage begins downward. A breeze of the air ventilation system that keeps the mine full of fresh air and at relatively cool temperatures blows into our faces as the ten-minute ride to the bottom passes in darkness, the only sight the dark, salty walls hurtling past through small holes in the side of the cage.
At the bottom, a kilometer underground, we are welcomed by the familiar sight of artificial lights flooding giant cavernous rectangular holes in the salt. The salt is the remnants of a briny sea that existed 260 million years ago in the Permian period. The miners are here to drill and dig the salt, using giant automated mining machines that crunch and eat away at the rock, some of it to end up on the roads to protect you and your cars from ice and snow, some of it to end up in fertilizers to make better crops. Down here, hidden from the gaze of the public, is the raw reality of humanity up against the crust of the Earth, gathering the minerals and rocks that make our civilization work.
Spanning out, like an ant nest, are over a thousand kilometers of tunnels that Cleveland Potash Limited, the company that runs the mine, has dug since the 1970s. The tunnels, big enough to drive a van down, sprawl out under the North Sea into the rich seams of salt. Once covering an area equivalent to Europe, the ancient Zechstein Sea would have been a marvel to gaze upon. No mere brine pool, this was an enormous inland water body, its white shimmering surface disappearing to the horizon on a primeval Earth when trilobites dominated the oceans and early four-legged animals on land included the sauropsids, which would in time rise to dinosaur dominance.
As the miners peel off to the mine face, we scientists divert through some tunnels to a door in the side of the salt, like the entrance to an arch villain’s lair. But behind this entrance is a laboratory that since the early part of the millennium has been at the center of the search for dark matter. Here, deep underground, where the kilometer of rock above blocks out the radiation from space, the scientists can look for the telltale signs of dark matter, that elusive component of the universe, while minimizing the interfering noise of unwanted particles streaming in from the Sun and the rest of the cosmos.
There is another reason to be here. Deep underground live microbes, denizens of the subsurface, biology’s dark matter. For decades now, biologists have realized that although most of us are familiar with the trees, reptiles, birds, and all manner of other life on our surface world, a vast quantity of the mass of living things on the Earth is underground. Few animals can make a living in these depths, but many forms of energy are here, waiting to be snapped up by microbes that can flourish and multiply in the cracks and fissures of this Hades-like underworld.
In Boulby, pockets and seeps of water provide natural habitats for microbes that can eat organic carbon or munch on some rare iron compounds here and there. Small pools of water that collect in the mine provide a permanent habitat. These microbes, unlike you and me, are in no hurry to go anywhere. They have no deadlines to meet. Like life anywhere underground, they may divide slowly, and, in some underground habitats around the world, microbes may multiply once every few thousand years or perhaps longer. This is a world in the biological slow lane. From the science-fiction cleanliness of the Boulby Underground Science Facility, we head into the dark, dusty tunnels to find these seeps, collecting the water in sterile sampling tubes and returning them to our labs to extract the DNA and find out what is living in these murky depths. A diversity of salt-tolerant microbes makes a living in these austere settings: these are the extremophiles, literally, extreme-loving microbes.
It is sometimes said that calling these hardy little creatures extremophiles is anthropocentric. If they could observe us living in the oxygen-rich atmosphere with all those damaging oxidants so created, they would think we were the extremophiles; their nice, cozy underground home, often oxygen-free, is not extreme to them. Fun though this contrarian view is, it is actually nonsense. If these deep dwellers could express an opinion about humans walking through a rain forest surrounded by monkeys swinging in the branches, parrots squawking in the canopy, and the vast diversity of microbes inhabiting just a spoonful of rain-forest soil, they would express dismay at the decadence of the good life. There really are extremes on Earth, where physical and chemical conditions push life to its limits and where the biosphere teeters between the living and the dead. Here, animal life is excluded, and even among the microbes, habitats are occupied by just a few with the evolutionary heritage and the biochemical wherewithal to grow.
Down in Boulby, only the microbes that can take the harsh briny fluids and the sparse amounts of carbon and nutrients found here can hang on. Here, no more than a thirty-minute drive from the chatter and excitement of children licking ice creams and playing on the beach and dogs barking in the summer sun, life is at its limits. A small reduction in water availability here, an increase in brininess there, threatens instantly to extinguish it. Here, we witness the experiment in biological evolution on planet Earth as a fickle thing. Not an endless, unbounded possibility of life, powering ceaselessly through Earth, a universal phenomenon unrestricted by physics. Although tenacious, life is a phenomenon circumscribed very much in its empire, constrained like the animals in a zoo by a fence of extremes that bounds it into a pocket of existence that occupies a trifling fraction of all the physical conditions, in their extremities, to be found across the known universe.
But what are these boundaries, and are they just an unlucky and unfortunate perimeter in Earth’s particular experiment in life? Would other experiments in evolution carve out new and unimaginable dominions, driving headfast into physical and chemical spaces in which our own extremophiles would wither?
With these questions, we advance to think about how cellular life is constrained not only in its construction—in the shapes of its cells and the molecules from which it is assembled—but also in the habitats it can master. Physics circumscribes the limits of life.
Boulby mine is an impressive depth, but even a kilometer is hardly a pinprick in the surface of the Earth. Go deeper, and one of the first problems for life is getting enough food. Probably only about a millionth of the space underground, all those pores and fractures in the rocks, is actually made into a home by life. The problem for microbes is not housing—it is getting energy. Life deep down is impoverished compared with the lush vegetation and relatively life-covered surface of the planet, but it is not impossible.
Dig deeper still, several kilometers deep, and now a new problem confronts life: the rising temperature. Within our planet is the primordial heat from its formation, heat trapped from the incandescent, swirling clouds of gas from which our Solar System was formed and produced from the decay of radioactive elements that form part of the recipe for making planets. At the center of the Earth, the heat is so intense that the solid iron core glows a withering 6000°C, surrounded by a liquid iron core whose churning motions, a giant dynamo, produce the magnetic field that protects us and our atmosphere from the bombardment of much of the radiation streaming in from space. Between this searing core and the relatively balmy surface, there is a gradient of heat, the geothermal gradient, and as lif
e buries itself deeper and deeper in the Earth, it must confront this gradient.
It takes little for that temperature to rise. Even in Boulby, in the caverns and tunnels just a few meters away from the ventilated tunnels, you are hit by a stifling heat, over 30°C. Generally less than ten kilometers underground, depending on where you are on Earth and how that heat finds its way upward, temperatures exceed 100°C, the boiling point of water at sea level.
Heat up molecules in a living cell, and the bonds that hold the atoms together get so much energy that they break apart. The higher the temperature, the more damaging the energy. Increase the temperature by 10°C, and the rate of chemical reactions about doubles, so as life gets deeper underground, the rising temperature becomes ever more dangerous. It must expend its own energy to repair proteins and membranes and make new ones.
In the 1960s and 1970s, an American microbiologist, Thomas Brock, who was investigating microbes that inhabit Yellowstone National Park, wondered whether anything could possibly be growing in its boiling volcanic pools. He prodded and probed the bubbling, venting cauldrons, collecting mud to take back to his lab. Within the unremarkable sludge, he found many microbes capable of growing at temperatures of 70°C or more. This was a new and surprising discovery, and these microbes, thermophiles, did not merely tolerate these temperatures, but needed them. Cool the mud down, and they refused to grow. These new discoveries spurred others to look at higher temperatures. Like a Guinness World Records contest, pushing the upper temperature horizon of life had become something of a challenge. From the pools of scalding water at Yellowstone, scientists turned their attention to the hydrothermal vents gushing water from the Earth’s crust deep in the oceans, the pressures sufficient to push the temperature of the water well above 100°C.
The hyperthermophiles, real extreme-loving microbes that prefer to grow above 80°C, cover a rich tapestry of species. Among their ranks is the record holder, Methanopyrus kandleri, a microbe from a black smoker hydrothermal vent, a strain of which can reproduce at 122°C.
The adaptations that all these microbes use to grow at such high temperatures bear witness to the challenge of taking on these scalding habitats. Many proteins in the cell have extra bonds or bridges of sulfur atoms, essentially bolts to hold the molecules’ three-dimensional structure together against the energy at high temperatures, which has a tendency to unravel them. Proteins can be made into more-compact structures, which make them less liable to unfold. Alongside these cunning adaptations, the microbes produce heat-shock proteins, part of a network of responses designed to lock on to damaged proteins and remove or stabilize them. Chaperonins are a class of small proteins that help refold other proteins that have gone awry in the intense heat. This thermostability of the molecules of life comes at a cost. The cell must synthesize all these helper proteins, and it must make entirely new copies of proteins. This ongoing battle between damage and the energy to prevent it must set the upper temperature limit of life.
We do not know what this upper reach is. It might go above 122°C. One group of researchers suggested that a temperature of about 150°C might be the limit. With all the competing energy needs of a cell, the multifarious ways in which proteins and membranes may be made more resistant to heat, and the different sources of energy in the environment, there is not an easy theoretical way to just work out an upper limit. However, one general principle is clear. Life as we know it is based on complex carbon molecules. The various strengths of bonds between carbon and other elements are not mere serendipitous outcomes of terrestrial evolution, mere parochial numbers that exist on Earth. They are universal values. The average bond strength between a carbon atom and another, for instance, is 346 kilojoules per mole. It is this value on Earth or in a distant galaxy.
When we expose a living thing, made of chains of carbon atoms linked variously to atoms such as oxygen and nitrogen, to high temperatures, we are not confronting a chance fluke of terrestrial evolution. At the chemical level, we are challenging the integrity of the C-C bond and its universal bond energy, and other bonds besides.
At temperatures of around 450°C, most organic molecules from which life is made are destroyed. It takes special arrangements of carbon atoms to make something that is resistant to high temperature. Graphite, the material in your pencil, can tolerate much higher temperatures, but this mineral is a tedious arrangement of carbon atoms linked to one another in monotonous atomic sheets. This is not a material from which to make life forms. Place some complex organic matter into an oven at 450°C, and it will transform into carbon dioxide gas. Chemists routinely use this heating procedure to clean organic matter off their laboratory glassware. So somewhere between 122°C and 450°C, there is a hard limit to the upper extremes of life. The efforts cells expend to hold together at 122°C suggest that the limit is nearer this temperature than it is to 450°C.
I will not be so naive as to make a prediction on what that limit might be. For the point of our discussion, it is not too important. High temperature sets a border to life. Serendipitous events and chance evolutionary innovations might well modify the range of that upper limit. Maybe in the course of evolution, the development of certain heat-shock proteins shifted the upper temperature frontier upward by a few degrees. Maybe future evolutionary innovations will push life slightly higher. And perhaps synthetic biologists and genetic engineers will achieve the feat in the laboratory.
What is important is that ultimately it is hard physics that sets the upper limit, and no amount of Darwinian mutation, chance innovations, or new discoveries by life will change that boundary. Pushing the upper perimeter of temperature can certainly buy life more habitat. The typical geothermal gradient into the Earth is about 25°C for every kilometer you go down. Push the upper temperature limit by 50°C, and you have just bought yourself 2 kilometers’ depth of rock where all other life has been forbidden. That is no minor amount of space from a microbe’s viewpoint. It is about 1.0 billion cubic kilometers of extra rock to explore.
At a planetary scale, though, the extra temperature tolerance probably does not modify the picture of life much. Even at our conservative 122°C, the thickness of the biosphere is about 5 to 10 kilometers—compare that with the radius of the Earth, 6,371 kilometers. The biosphere is a mere 0.1 percent. Life on Earth should probably be referred to as the biofilm, not the biosphere. Even with the unorthodox suggestion that life could get near to 450°C, we would about triple the thickness of the biosphere, but its depth of penetration into the Earth’s crust would still be only about 0.3 percent of the Earth’s radius. Life is a thin layer on the planet, a patina of organic material denied the depths of the Earth by the limits imposed by thermal energy.
From the searing depths of the Earth, we take another trip—to the freezing extremes of the universe—and here, too, physics places boundaries on the lower-temperature capacities of life. At absolute zero, there is no possibility of molecules shifting around, linking up with other molecules, making proteins, and reading genetic codes. Trivial though the observation may be, somewhere between the temperatures you and I find clement and absolute zero, physics sets a boundary. For life, that limit is much nearer the temperatures you and I are familiar with than the chilling extremes of zero kelvin. So far, there is no good, convincing evidence of life replicating below about −20°C, although metabolic activity, the production of gases or the activity of enzymes, seems likely to occur below this.
Organisms can live below 0°C, the temperature at which pure water freezes at sea level, because there are environments where liquid water can persist. Add some salt, and the freezing point depresses to about −21°C for the lowest freezing temperature of a solution of table salt, sodium chloride. Solutions of more exotic salts, such as perchlorates, can take the freezing point well below −50°C. Part of the problem with finding active life at these low temperatures is the glacial rate of chemical reactions. Measuring growth or metabolism at low temperatures is just technically difficult.
The challenge t
hat low-temperature life must confront is to repair molecules that are damaged when chemical reactions, and by extension many repair processes and biochemical pathways, run so slowly. Unlike life at high temperatures, damage to molecules does not primarily come from excess thermal energy, but comes from stray particles from radioactive decay; an errant zap of ionizing radiation through the cell will break DNA or destroy a protein.
All around us is radiation. Particles, including protons and heavy ions, stream in from the galaxy and the Sun. Although many of them are deflected by our planet’s magnetic field, some get through and intersect with DNA.
Radiation also comes from within the Earth. In the crust or core of any planetary body, natural minerals that contain certain isotopes of uranium, potassium, or thorium produce radiation from the decay of these elements. This radiation, made up of different types of emissions, including damaging gamma rays, affects us all, although it is of sufficiently low intensity that we rarely worry about it.
This background radiation causes damage to the major components of life, particularly DNA. Background radiation can break the double helix of DNA or cause the formation of reactive oxygen radicals, which themselves attack and damage the DNA molecule. It can disrupt any sort of complex, long-chained compound from which life might be formed. There is no easy way for life to screen this radiation. Most of it can effectively penetrate biological material, a problem that is exacerbated if you happen to be a microbe made only of a single cell. Your only option is to repair the damage once it has happened.
Added to these problems is the natural tendency of some molecules to alter their structure, or decay. Sit there and do nothing, and all this damage will slowly, steadily accumulate until, eventually, it is so great that the cell will never recover. At some low-temperature region of active life, there must be just enough energy and biochemical activity for the cell to repair this unavoidable destruction, but not so little activity in the cell that it cannot keep up with damage collected in molecules over long periods. Like life at high temperatures, there is no easy way to calculate unequivocally that temperature. We know, however, that cells can evolve stunning ways to deal with plummeting temperatures. The so-called psychrophiles, microbes that grow best at below 15°C, have developed ingenious methods to offset the effects of cold.
The Equations of Life Page 13