SOME LIKE IT VERY HOT

For years it was thought that life couldn’t exist below a certain depth or above a certain heat. Now those limits turn out not to be limits after all. Bryan Appleyard looks into extremophiles

From INTELLIGENT LIFE magazine, May/June 2012

Russian scientists have now poured 60 tonnes of freon and kerosene down the four-kilometre bore hole that plunges through the ice above Lake Vostok in Antarctica. This will stop the hole freezing up during the long Antarctic winter. When summer comes, the Russian team will return to drill the last 100 metres and expose the surface of a lake that has been buried beneath the ice for at least 15m years. Eventually they intend to explore this lost world, a place unseen by human eyes, with a robot submarine.

The temperature of the lake is about -3°C, but the water remains liquid because of the pressure exerted by the ice sheet. The pressure should also have kept the water super-saturated with oxygen and nitrogen. Once we would have assumed that this cold, lost lake would be no more than a geological curiosity, a dead relic of the time when Antarctica separated from Africa and drifted south. Now we can be almost certain that it is full of life. Most of these creatures will be tiny single-celled organisms, microbes, visible only under a microscope. But they will have novel genetic structures, they will use previously undiscovered enzymes and they will have evolved unique survival strategies. They will be a class of creature now known as extremophiles, lovers of extreme conditions.

This is a biological category that was only discovered 40 years ago. Now we know that the Earth is teeming with these hyper-resilient microbes, organisms that can survive levels of heat, cold, pressure, radiation and salt or acid concentrations that previously would have been thought fatal to all living things. The study of these creatures is still in its infancy, but they have already broadened our conception of life on Earth and raised hopes of detecting life in space. The surface of Jupiter’s moon Europa, for example, is an ocean of ice, beneath which there could be inhabited lakes like Vostok. Extremophiles also offer a cornucopia of new medical compounds, primarily antibiotics, as well as almost indestructible enzymes that could transform chemistry at both the domestic and industrial scales.

Almost daily now, new extremophile species are discovered. Also in Antarctica, outside the prefabricated hut erected by Robert Falcon Scott at the start of his doomed expedition in 1911, there are drums containing diesel oil. The site has been preserved as an historic monument so the drums remained intact until, in the last few years, they started leaking. Professor Michael Danson, director of the Centre for Extremophile Research at the University of Bath, seized the opportunity to dig into the soil beneath these leakages.“Behold! We isolated organisms that were living off the diesel oil.” Such organisms could be used to consume oil spills like BP’s disastrous gusher in the Gulf of Mexico in 2010.

In the 1980s, Karl Stetter couldn’t get funding from his university, Regensburg in Bavaria, to pursue his obsessive search for organisms that lived in temperatures higher than 60°C. The authorities just didn’t believe such creatures existed. So he took a holiday on the island of Vulcano off Sicily. First, he used his hotel shower to accustom his hands to very hot water. Then he dived off a rubber boat manned by his wife and daughter and took samples from the hot vents on the seabed. He took the samples back to his lab and discovered an organism that reproduced happily at 100°C. The world record for thermophiles—heat lovers—is now just above 120°C.

In the early 1990s, the prevailing microbiological wisdom said that the biosphere ended 7.5 metres beneath the seabed. Undeterred, John Parkes, now head of the School of Earth and Ocean Sciences at Cardiff, began to look for life in deep ocean cores, obtained by specialised drilling ships. Of the cores he acquired from around the world, two stood out. They were to make him one of the leading extremophile researchers in the world. The first came from just off the Peruvian coast, the other from near Newfoundland, the point where the continents first tore apart to form the Atlantic Ocean. Off Peru he immediately found life at 80 metres, overthrowing the orthodoxy. Later, off Newfoundland, he found life at 1.6km beneath the seabed. “That’s the record so far,” he says, “but we think we might be able to get down to 4km.”

Picture: The black smoker—the Saracen’s Head hydrothermal vent, 3,100 metres below sea level in mid-Atlantic. The picture was taken from Alvin the submersible (Science Photo Library)

Deep in Mexican caves, where the air is poisonously saturated with hydrogen sulphide, Diana Northup, a biology professor at the University of New Mexico, found the walls covered with slime which she calls “snot”. There are even “snottites” hanging from the cave ceiling and “snot” balls—cities of bacteria. These creatures excrete concentrated sulphuric acid that eats away at the cave walls. In fact, it now looks as though the caves were largely built by the corrosive effect of bacterial excretions.

“Yes, we were pretty narrow in our thinking,” she says. “That’s what extremophiles have done for biology. They’ve opened our eyes…if you only think about life in terms of your condition, you can miss a lot of what’s going on in the planet.”

To get some idea of how revolutionary these findings are, we need to go back to the biological preconceptions of the 1950s and 1960s. Then it was thought that life was the supreme cosmic rarity, only possible within the narrowest of conditions. The microbiologist Claude ZoBell laid down the doctrine that life ended at a depth of 7.5 metres below the seabed, the immoveable line at which the biosphere was thought to encounter the geosphere. Beyond that point there was simply insufficient energy to sustain living processes.

And then, in 1968, some sandwiches, an apple and a submarine named Alvin seemed to prove beyond doubt that life at extreme cold and high pressure was impossible. Alvin was (and still is) a deep-sea submersible belonging to the Woods Hole Oceanographic Institute in Massachusetts. While being transported, it was accidentally dropped, with its hatches open and three crewmembers on board, into 1,500 metres of water. The crew escaped but their lunch went down with its ship. Ten months later Alvin was retrieved and the lunch was found to be damp but edible, proving to the satisfaction of many that there was no microbial action on the sea floor.

John Parkes now laughs about this: “It was just that at that depth the bugs had never seen a bologna sandwich before, or an apple.” More prosaically, Michael Danson points out that we can be sure that, on Earth, where there is water there is life, however extreme the conditions.

Danson likes to point out that, strictly speaking, extremophiles were first recorded in the Old Testament when the Moabites noticed a red bloom on the Dead Sea. They wrongly concluded that it was blood and that the Israelites were fighting among themselves. In fact, the bloom was a mass of halophiles—salt-loving bacteria—and the deluded Moabites descended, only to be slaughtered by the Israelites.

In our time, those who drew the initial conclusions from the Alvin sandwiches were, like the Moabites, mistaken because they accepted the conventional view of survivable environments. And yet, only the year before, 1967, an article had appeared that formally established the existence of extremophiles. It was by an American microbiologist, Thomas Brock, and was published in the journal Science. In the hot springs of Yellowstone National Park, Brock (then 40, now 85) had discovered a microbe which he christened Thermus aquaticus, a creature that could survive at temperatures as high as 80°C. At once, our sense of the life-sustaining zone on Earth expanded. “It was Brock who set the ball rolling,” says Michael Danson. “What has happened since is that the temperature has been set higher and higher. The highest temperature record at which growth has been observed is 121°C.”

Thermus aquaticus was also, serendipitously, the organism that established the enormous potential practical importance of these newly discovered life forms. The point about a thermophilic bacterium is that it needs some very tough enzymes, the catalysts of living processes. Our own enzymes break down very quickly at high temperatures, which is another reason that life outside what we consider a normal temperature range was thought impossible. An enzyme in Thermus aquaticus is now known as Taq DNA polymerase and it has become one of the most important enzymes in microbiology. It made possible the polymerase chain-reaction (PCR) technique for amplifying DNA samples. This led to the uses of DNA in forensic science and, in fact, to much of what we now know about DNA. PCR is a molecular photocopier, making it possible to take very small samples of DNA and repeatedly reproduce them. So now murderers have to be obsessively clean if they are to escape the attentions of the forensic scientist.

Picture: Thomas Brock, the microbiologist who set this ball rolling in 1967 (Science Photo Library)

In the decades after Brock’s discovery, an entire menagerie of extremophiles emerged. We now have acidophiles (acid lovers), halophiles (salt lovers), piezophiles (pressure lovers), xerophiles (dryness lovers) and many others. One category, the radioresistants, contains Deinococcus radiodurans, which the environmentalist James Lovelock says is his favourite creature and which has been listed as the toughest bacterium in the world in “Guinness World Records”. It can survive 1,000 times the level of radiation that would kill a human and has been found to exist in the cores of nuclear-power stations. As such levels are not found on the Earth’s surface, why it should have such a system is unknown. Deinococcus has a system for constantly repairing its own DNA which, if we understood it, could have extraordinary medical implications. Cancer, for example, starts as a DNA mutation in a single cell. If we could use this bug’s repair system, then perhaps we could stop cancer before it takes hold.

Once biologists routinely said there were 10m distinct species on the planet; now nobody knows how many there are, but it is certainly a lot more than 10m. The rate of new discoveries suggests that we have barely scratched the surface of extremophile numbers. This proliferation has even led to an entirely new division of life on Earth. Before extremophiles there were thought to be two types of life—prokaryotes, mostly single-cell organisms that lack a cell nucleus—and eukaryotes, mostly multi-cell organisms, including us, that have complex structures inside the cell, including a nucleus. But it was soon found that many extremophiles, though they appeared to be prokaryotes, had such a different evolutionary history that they were an entirely new form of life. In 1977 Carl Woese, an American biologist and physicist, separated these out and christened them archaea, the third domain of life.

“That was one of the great landmarks,” says Karl Stetter, “this was a very, very important finding. At the time, of course, nobody believed Woese.”

Extremophile researchers have one thing in common: they are constantly being told that what they are seeking is impossible. This gives them a quixotic determination to seek anyway. What drives them, I think, is the realisation that, thanks to extremophiles, microbiology can once again be a science of discovery. In an age when people had begun to think there was nothing left to discover on Earth, they have become explorers in a new and exotic landscape.

It was Woese who inspired Stetter to study extremophiles. A theatrical, constantly excited and brilliant man, Stetter went on to become the godfather of the discipline. He’s not sure how many new creatures he has discovered, but it is in the region of 50 or 60. They include some of the smallest microbes ever found, which he called nano-archaea. They live by hot deep-sea vents, on larger host bacteria, and are thought to resemble the earliest forms of life on Earth. Stetter also solved a problem for BP. They were puzzled to find hydrogen sulphide in their oil and wanted to find out where it was coming from. Their own microbiologists could find no signs of life. On a drilling rig in Alaska, Stetter realised that this was because they had installed a “splitter” that separated oil, water and gas. When they turned off the splitter, the H2S-producing organisms, which were in the water, appeared on the surface.

Thanks to television, the best-known of the big extremophile breakthroughs is the black smoker. More formally known as hydrothermal vents, black smokers are deep-ocean chimney-like formations from which geothermally heated water pours. As the hot water meets the cold water of the sea, the dissolved minerals blacken the plume. These are, for extremophile scientists, sacred locations; some speculate that they may be where life on Earth began. By the old definitions of suitable environments, no more inhospitable location could be found, and yet the black smokers turn out to be crawling with life, from strange shrimps and crabs to the most bizarrely adapted extremophiles. One black-smoker bacterium is phototrophic—it depends on light—yet it lives 2,500 metres beneath the sea surface, where, to our eyes, there is no light at all. It survives, incredibly, on the glow from the smoker. There may well be black smokers deep beneath the ice on Europa, the Jovian moon.

Picture: The halophile effect—a salt lake near Dakar, Senegal, stained pink by salt-loving bacteria (Science Photo Library)

So dynamic and so new is this whole area of science that, mostly, it is still in the research rather than the application phase. It has, however, already inspired the growth of another discipline, astrobiology. Unique among the sciences, astrobiology has no object of study since we have not yet found any life beyond the Earth. But the discovery of extremophiles has proved that life can sustain itself in many more environments than was previously thought possible. So, for example, we now know that digging up regolith (surface soil) is no way to find life on Mars. Rather, we have to drill deep beneath the surface. And extremophiles have given new life to the theory of panspermia, the idea that life exists throughout the universe and is disseminated on meteorites or asteroids. The problem with this was always that it seemed impossible that life could survive the journey. Now we know it could; indeed, bacteria have been shown to be able to survive. In 2010 bacteria from cliffs in the village of Beer in Devon were found to have lasted 553 days on the exterior of the International Space Station. Extremophiles have convinced astrobiologists that alien life is now much more likely.

But two big applications here on Earth are, first, the polymerase chain reaction, developed in 1983, and, secondly, the preservation of the colour of your favourite jumper. With the development of more powerful and fully automatic washing machines in the 1970s and 1980s, ever-more demanding consumers grew restless because they noticed colours had begun to fade in the wash. Manufacturers worked out that invisible and colourless hairs were being raised from the fabric by the washing process. If they could cut these hairs, colour would be restored. A Japanese extremophile researcher, Koki Horikoshi, worked out that the best way to cut them was to use enzymes from extremophiles that could survive both the highly alkaline conditions found in washing machines and either very hot or quite cold water. Their first attempts failed because they overdosed the wash with an enzyme which ate all the clothes. Finally, they got it right, and developed the washing powders we call “biological”.

Stetter, meanwhile, has co-founded Verenium, a San Diego company which specialises in the use of extremophiles. Their primary products are enzymes that split cellulose to make sugar. On the whole, extremophile scientists admit they are pure researchers rather than applications experts. The potential, however, is enormous, especially for the pharmaceutical industry. Most of Diana Northup’s cave-slime bacteria contain hitherto unknown antibiotics. It is not yet certain how they use them, but a popular hypothesis is that they form signalling and sensing systems which the bacteria use to detect and communicate with each other or possibly even as weapons against competing bacteria and predators. There are many potential human uses. “New drugs”, says Northup, “are entirely possible. A few years ago people seemed to give up on the idea that it was worth looking for new compounds in nature. But I don’t believe in giving up when you have environments like these.”

Picture: Deinococcus radiodurans (Science Photo Library)

John Parkes is excited about the possibilities of immortality, in bacteria at least. We are used to the slightly sinister spectacle revealed by microscopy of bugs dividing —ie, reproducing—every few minutes. But the creatures Parkes has found deep in the ocean sediment divide very slowly indeed, perhaps only once in several thousand years or even, in some cases, once every hundred thousand years. Even more astounding are the bugs found in fluid inclusions. These are microscopic bubbles of liquid gas that are trapped within crystals. They form, for example, within salt crystals and, almost inevitably, extremophiles have been found in these bubbles. The point about fluid inclusions is that they are very long-lasting; some are known to be 50m years old. The creatures that inhabit them don’t appear to divide at all.

“Why should they?” says Parkes. “There are no predators. There may be viruses but, if so, division is a very bad strategy as it will help the viruses to reproduce.”

This means we may have discovered 50m-year-old life forms. Are they, therefore, immortal? “Aha!” says Parkes, an exclamation he often uses. It seems to mean “Maybe, but we don’t yet know,” with the further subtext “I hope so.”

“On the surface of the Earth”, Parkes goes on, “the best strategy is ‘live fast, die young’. Down there the best strategy seems to be ‘live slow, die old’.”

But, for the moment, the most spectacular effect of extremophiles has been not on the human body but on the human imagination. This effect is humbling. Ever since the geological and biological insights of the 18th and 19th centuries, life on Earth had usually been seen as a poignantly fragile membrane spread across the surface of an unremarkable planet orbiting an average-sized star.

“On this crust”, wrote the great and gloomy philosopher Arthur Schopenhauer in 1818, “a mouldy film had produced living and knowing beings; this is empirical truth, the real, the world.”

Extremophiles have revealed that the film is much thicker, more resilient and more ingenious than Schopenhauer could ever have imagined. Some estimates suggest that the biomass beneath the seabed is greater than that above. They have also encouraged a new confidence in the idea that we are not alone in the universe. The bandwidth of possible survivable environments—and, therefore, forms of life—has broadened enormously. There may only be bacteria out there but, after Deinococcus radiodurans and Thermus aquaticus, there would seem to be almost no limit to what these creatures can do.

Extremophiles have changed our view of ourselves. We are, ultimately, their offspring. Anaerobes, organisms that do not use oxygen, were the original forms of life on Earth before they were almost extinguished by the appearance of oxygen in the atmosphere. But they persist and flourish deep beneath the ocean floor. And it was the invasion of bacterial cells by other bacteria that created the more complex cells of the eukaryotes. Numerically, we remain only 10% human, the remaining 90% of our cells being the bacteria in our guts. We are born of infection.

Finally, we cannot observe these organisms without feeling a vertiginous shift of perspective. Anthropocentrically, we define the limits of our environment as “normal”, but we can now see that it is common to find much higher and lower temperatures, extreme pressures, intense acidity or alkalinity and what seem to us phenomenally long lifespans. The shift comes when we realise that the creatures living in such environments are extreme only by our standards, and there could be far greater extremes waiting to be discovered. In the depths of Lake Vostok, four kilometres beneath the ice, those Russian scientists will find more of the ordinary life of Earth and further evidence that, as John Parkes says, “we are the extremophiles.” 

Bryan Appleyard is a feature writer on the Sunday Times and author of "The Brain is Wider than the Sky"

Picture: John Parkes—when he started, the record depth of life was 7.5 metres below the seabed. Now it’s 1,600 metres (Science Photo Library)