by David Toomey
For Woods Hole scientists, the heat presented some challenges. They had to design and build water samplers that would work at high temperatures, and they had to be careful to keep Alvin a safe distance from the chimneys, as the heat might soften its Plexiglas portholes enough to implode them. But the work was exciting and welcome. In the months and years that followed, scientists from many different institutes and universities found more vents and more chimneys (they would come to be called “black smokers”) along other midocean ridges, and near all of them, a great many living organisms.*
The theory of plate tectonics had predicted hot springs in the seams between tectonic plates. In the most dramatic fashion, Corliss and Edmond’s discovery of the hydrothermal vents went a long way to support that theory, and thus closed a chapter in geology. At the same time, their discovery of life that was fed and energized by hydrothermal vents opened a new chapter in biology. Like all good chapters, it provoked questions. Exactly what sorts of organisms live in these places, and in what numbers? How did they adapt to the pressure, the dark, the heat? And how exactly did they get there to begin with?
THERMOPHILES AND HYPERTHERMOPHILES
Some of these questions had been answered several years earlier by a microbiologist named Thomas Dale Brock. Brock was an assistant professor at Indiana University, developing an interest in microbial ecology—the study of the relationship of microorganisms with one another and with their environment. In the summer of 1964, on a brief sabbatical, he was among the thousands of tourists visiting Yellowstone National Park. Brock was captivated not by the bison and grizzly bears so much as by somewhat smaller organisms. He noticed distinct colors in the outflow channels of the hot springs, and when he took a closer look he was astonished to see what he later described as “pink gelatinous masses of material, obviously biological.”9
The water was decidedly hot. In, fact it was nearly boiling. People had seen the pink stuff before, of course, but they did not know what Brock knew: that no microbiologist expected any microbe could live in water this hot. Microbes that live in water at temperatures between 60°C and 80°C are called “thermophiles,” and microbes that live in water with a temperature of 80°C or higher are called “hyperthermophiles.” But that is now. In 1964, few would have believed hyperthermophiles possible, and a standard textbook recommended that researchers incubate thermophilic bacteria at a temperature of 55°C or 60°C.10 The temperature Brock measured in the outflow channels was 90°C. For years, Brock had suspected that research limited to lab-grown bacteria would lead to a blinkered view, and here was his vindication. Because no one had thought bacteria could survive at temperatures much higher than 60°C, no one had bothered to look for them.
Exactly how something in plain sight might pass unnoticed by researchers was a very good question. One answer, offered by historian of science Thomas Kuhn, is that people (scientists included) see what they expect to see, and may not see what they don’t expect to see. By way of example, Kuhn described an experiment in which subjects were asked to identify the color and suit of playing cards presented to them quickly and in sequence. The experiment used a trick deck. Most of its cards would be found in any deck, but a few were special, with combinations of color and suit, like a red six of spades, that do not appear in a normal deck. The test subjects, shown the cards quickly and in sequence, did not register the special cards as special, and mistakenly assigned them normal combinations of suit and color. When shown the red six of spades, for instance, many saw a red six of hearts. On the second or third run-through, some subjects began to hesitate before answering. On still more run-throughs, several became hopelessly confused, with one nearly unraveling altogether. “It didn’t even look like a card that time,” he said. “I don’t know what color it is or whether it’s a spade or a heart. I’m not even sure now what a spade looks like.”11 Only a few recognized the red six of spades as a red six of spades. But as soon as they did, they began to look for other special cards. Kuhn made the point that something similar happens in science. When a scientist recognizes something no one else has recognized, Kuhn wrote, there follows “a period in which conceptual categories are adjusted until the initially anomalous becomes the anticipated.”12
In the fall of 1964, with his own conceptual categories properly adjusted, Brock anticipated the anomalous—and sought it out. He set up a laboratory in West Yellowstone and began to spend his summers exploring the boiling and superheated pools, doing a sort of microbial fishing. At particularly interesting places he would attach one end of a long string to a tree branch and the other end to a glass microscope slide, and drop the slide into the water. A few days later he would retrieve the slide and examine it. On almost every slide he found heavy bacterial growth.
Initially, other microbiologists thought Brock’s discoveries too specialized and esoteric to be of wider interest. There were, after all, only so many hot springs in the world, and so there could be only so many species of thermophilic (or hyperthermophilic) bacteria living in them. Then Corliss and Edmond and their many successors found ecosystems whose basis was organisms that thrived in hot water. And the environments that they preferred, while difficult for species like Homo sapiens to reach, were not rare. Far from it. Midocean ridges snake along the oceanic crust for tens of thousands of kilometers. By the late 1970s, microbiologists were poring over Brock’s published works for ideas on how thermophilic bacteria adapted and how thermophilic ecosystems might work. And since it was easier and a lot cheaper than mounting an expedition to a midocean ridge, quite a few began to visit his old haunts at Yellowstone.
Meanwhile, word of life on midocean ridges was reaching all corners of academia. The life sciences department at most universities and colleges has a large bulletin board mounted outside the department’s main office. On that bulletin board one is likely to find a notice of a forthcoming department meeting, announcements of conferences and calls for papers, as well as more personal ephemera, like a scribbled note about lost car keys. Occasionally there is a page torn from a journal on a subject that someone thought might be of general interest. Such was the case in the fall of 1979, when it seemed that every bulletin board outside every main office of every life sciences department at every university and college—and high school too—had an article about the deep-water sulfide chimneys and the life around them.
Soon enough, biologists began to wonder whether there were other “special” cards in the deck, and many began looking. Through the 1980s and 1990s, to anyone reading the science section of a newspaper, it seemed that every other week someone had found life where (one would have thought) it had no reason to be. There were heat lovers, cold lovers, pressure lovers, acid lovers, alkaline lovers, salt lovers, and even radiation lovers.* As a group they became known as extremophiles, a term that had been coined by R. D. MacElroy in 1974.13
Through much of the twentieth century, biologists classified organisms within a taxonomic system whose largest and most fundamental categories were Animalia and Plantae. Single-celled organisms like bacteria were included among the Plantae, it seemed to some, as an afterthought. In the 1960s, biologists began to regard the system as inadequate, especially with respect to microorganisms, and they developed a new taxonomy in which the most fundamental divisions were five “kingdoms”: Animalia, Plantae, Fungi, Bacteria, and Protista. The kingdom of Protista, its boundaries particularly ill defined, included many organisms simply because they fit nowhere else. Certain microbiologists (among them evolutionary biologist Ernst Mayr) proposed a more fundamental division into two “empires.” Bacteria, whose cells were relatively small and lacked a nucleus, were classified as prokaryotes (pro meaning “before” and karyote meaning “kernel” or “nucleus”); and the other four kingdoms, whose organisms were composed of larger, nucleated cells, were classified as eukaryotes (eu meaning “true”).
In the 1960s, microbiologist Carl Woese and his colleagues began to sequence ribosomal RNA and realized that many microorganisms that had been clas
sified as bacteria (under a light microscope they looked like bacteria) were in fact fundamentally different. The categories were redrawn yet again, this time as three “domains.” The eukaryotes were called Eukarya, and the prokaryotes were split into the domain Bacteria and the newly discovered domain Archaea. Woese’s taxonomy is especially pertinent to our interests here. While extremophiles include members of all three domains, most are archaea.
Of course, since they are as unlike each other as they are unlike other life, extremophiles are a group only in the sense that “all composers not Beethoven” or “all painters not Monet” are a group. Any given extremophile can be represented by a different outlying point on a bell curve, and there are bell curves for temperature, pressure, and pH. Many, like a certain species of Acidianus that thrives at high temperatures and low pH levels, can be represented by outlying points on two bell curves.14 What counts as extreme, of course, depends on who is ringing the bell. R. D. MacElroy, presumably, had a body temperature of 98.6°F and most probably a distaste for strong acids. If the Acidianus species were to categorize him, it would call him a “psychrophile” and an “alkaliphile”—a cold lover and an alkaline lover.15
In any case, by the 1990s the search for extremophiles had accelerated. NASA, interested in learning how organisms might adapt to harsh environments like the subsurface of Mars, funded numerous research programs—some independently, some with the National Science Foundation. In 1996 a group of biologists convened the first International Conference on Extremophiles. Within a few years, researchers in the new field had established a journal and a professional society, and had published thousands of papers.
One point of agreement in all this research was that if there is a limit, an outer boundary beyond which the most extreme of extremophiles cannot pass, it was probably set by the swish, gurgle, and drip of liquid water. It so happens that every place scientists have found life, they have also found liquid water or evidence of its presence. And almost every place they have found liquid water, they have found life.16
WATER
In a list of chemicals arranged by their molecular weight, you would expect water, with a lower weight than oxygen or carbon dioxide, to be a gas at room temperature. In fact, the only reason water is a liquid hereabouts is that its molecule is polarized—the two hydrogen atoms on one side of the oxygen atom holding a slight positive charge, the oxygen atom itself holding a modest negative charge. It is an arrangement that allows water molecules to form bonds that are gentle, yet strong enough to make water bead on glass, to let it be pulled upward through a plant stem, and to endow it with surface tension—that intriguing quality by which molecules on the liquid’s surface are attracted to each other more powerfully than they are to the air molecules above them or the water molecules below them.
The charged poles that pull water molecules together are the very feature that enables them to pull other molecules apart. Chemists speak of water as an unusually versatile solvent. Like the perfect dinner party host, water gently breaks apart couples (like sodium chloride) and large groups (like sugars and amino acids). Chemists also speak of water as a very good medium for diffusion. Again like that perfect host, water provides its guests an environment in which their parts can move and mingle freely. This environment, it should be said, happens to be particularly congenial to life. Water offers protection from DNA-damaging ultraviolet radiation, and it holds heat so well that temperatures near the ocean floor are unchanging year-round. And because, by comparison with other chemicals, water stays liquid at a very wide range of temperatures (in fact, a range of 100 degrees on the scale that is based on that very liquidity), life can operate at that same wide range.
One of water’s properties is at once so peculiar and so conducive to life’s presumed beginnings and long-term well-being that some nineteenth-century naturalists pointed to it as evidence of intelligent design.17 If water were like most liquids, it would become denser and heavier when it froze. Ice would sink, and bodies of water in colder climes would radiate away heat and freeze solid from the bottom up. Life in those places—especially aquatic life—would have a very hard go of it. In fact, though, ice expands when it’s frozen, becoming more voluminous by about 10 percent and forming a surface layer on lakes and oceans that insulates the water and organisms beneath.
As if all this congeniality weren’t enough, water also uses dissolved compounds to make “microenvironments” within itself. The charged poles of water molecules lead other molecules to orient themselves side by side and facing in the same direction, some forming whole choreographed chorus lines, row after row of them, until they are best regarded as membranes. Some of these membranes develop into the microscopic bubbles that molecular chemists call vesicles, and whose interiors, some 4.6 billion years ago, may have sheltered the first self-replicating molecules and over time developed into cells.
Given all the virtues of water, we should not be surprised if organisms no one would call extreme go to astonishing lengths and employ ingenious strategies to get it. And they do. Spanish moss (Tillandsia usneoides) pulls water directly from the air; a species of kangaroo rat (Dipodomys merriami) draws it from metabolized food; and California redwood trees (Sequoiadendron giganteum and Sequoia sempervirens), by a means only imperfectly understood, pump it to their highest branches 100 meters above the forest floor. And once they have water, organisms no one would call extreme go to great lengths to hold it, to keep it from freezing or evaporating, to distribute it within themselves, and, where possible, to recycle it.
As for extremophiles? To acquire and retain water, they go to lengths that are, well, extreme.
FIRE AND ICE
The Celsius temperature scale uses the range at which water is liquid as its central scaffolding, but that range may be extended upward into hotter temperatures if, as we’ve seen, the water is kept under pressure. It may be extended downward into colder temperatures if the water is mixed with something else. Extremophiles are quite willing to exploit this wider range of temperature, and biologists are interested in the strategies they use to do it.
To appreciate the ingenuity of those strategies requires a brief refresher in biology. The cell is the smallest structural unit of an organism that can function independently. The cells in you and me, and in any other multicellular being, have a nucleus that contains their DNA. In the rather simpler cells of bacteria and archaea (groups to which all microbial extremophiles belong), the DNA floats freely in the semiliquid cytoplasm. In the cytoplasm are large molecules called proteins that initiate and accelerate chemical reactions in the cell and (in some cases) act as a supporting structure. The DNA, cytoplasm, and proteins are held inside a plasma membrane covered by a cell wall. The membrane protects what is inside the cell from the harsh environment outside it, and the wall prevents the cell, in certain situations, from expanding and bursting. The membrane and the proteins in the cytoplasm inside happen to be especially vulnerable to high temperatures. In water approaching boiling, the cell membrane grows more and more watery, eventually becoming too porous to do its job, while the proteins inside it are twisted, bent, or just plain broken (or as microbiologists put it, “denatured”), and so made useless.
To stay healthy in hot water, some thermophiles substitute the weaker parts of proteins with parts that are more durable and heat resistant. This is probably the method used by the hot-water record holder at present, a bacterium retrieved from a hydrothermal vent off Puget Sound. In 2003, University of Massachusetts microbiologists Derek Lovley and Kazem Kashefi had cultured the bacterium successfully and were curious about how much heat it could tolerate. They increased the temperature to 100°C, and the bacterium kept growing. The only means to still-higher temperatures that they had on hand was an autoclave, the pressurized steam–heated vessel commonly used to sterilize medical equipment—an instrument, one can’t help but note, designed not to culture microorganisms, but to kill them. They left the bacterium cooking in the autoclave for ten hours. The bacterium repr
oduced at 121°C and survived for two hours at 130°C. “We were,” Lovley said, “truly amazed.”18
There are reports of microbes, also living near hydrothermal vents, that survive at still-higher temperatures, but collecting samples in the vicinity of hydrothermal vents is difficult, and the samples in question may have been contaminated. Still, since scientists can imagine substituting parts that would allow a cell to hold up under even higher temperatures, a confirmed finding would not be particularly surprising. As the NRC’s Limits of Organic Life report observes, “the upper temperature limit for life is yet to be determined.”19
As to the lower temperature limit? Ice threatens an organism by an act of omission, denying the organism the solvent it needs to work its chemistry. It also threatens with an act of commission: ice crystals can easily tear a cell membrane. When water inside a cell freezes, the result is, in the ominous language of one paper, “almost invariably lethal.”20
If water didn’t mix well and life insisted on taking its drinks straight up, the coldest temperature at which an unprotected cell could survive would be 0°C, and we could learn all there was to learn about the chemistry of water in an afternoon. But as it happens, water will mix readily with any number of solutes. Stir in the right salts and you can keep water liquid at –30°C. Add some organic solvents and the temperature can go lower still. Where organisms can supply these salts and organic solvents, they will.* Some keep the juices flowing by increasing the concentration of solutes between cells; others, by modifying lipids and proteins in cell membranes. Mix in an amino acid like methionine and an organic compound like ethylene glycol and you can expect that enzymes, the proteins that act as biochemical catalysts, speeding up reaction rates, will still do their catalyzing at a chilly –100°C.
