By Jeanne McDermott
Freelancer Jeanne McDermott lives in Cambridge, Massachusetts. She authored The Killing Winds: The Menace of Biological Warfare (Arbor House, 1987).
As the director of a S100,000- a- year research lab, she taught two or three courses at Boston University every semester for 22 years, and is continuing this work at the University of Massachusetts. She has authored more than 130 scientific articles and 7 books. She rarely sits still. Her speech is nonstop and, in the jargon of her profession, filled with references to DNA homologies, microtubules and antitubulin probes. She interrupts and digresses constantly because one idea triggers an avalanche of others. She likes to make daring statements such as, "The nervous system is explicable in terms of microbiology." "That's propaganda" is her way of dismissing dogma, which she hates. She is restless, passionately curious, irreverent, sassy and very sharp.
One colleague calls her the most gifted theoretical biologist of her generation. Another, of the century. Her mind keeps shooting off sparks," says Peter Raven, director of the Missouri Botanical Garden and a MacArthur Fellow. "Some critics say she's off in left field. To me, she's one of the most exciting, original thinkers in the whole field of biology."Margulis is an authority on the microcosmos. She likely knows more than anyone else about the role of microorganisms in the past 3.5 billion years of evolution. While most American biologists emphasize the role of competition in evolution, Margulis stresses symbiosis. For example, she views each human cell as a "sophisticated aggregate of evolving microbial life." We are made, if you will, of conglomerated bacteria.
As children, we gradually learn how the world works--china cups break when they fall. hot coffee burns, the sun sets at night. As any summer visitor to northern Alaska can attest, it can be very upsetting when the world does not work as expected. Scientists. Iikewise, build their own notions of the way the world works, which MIT philosopher Thomas Kuhn calls scientific paradigms. Periodically, but not very often, a scientist will make a discovery so outlandish that it does not fit into any paradigm, leading to a sort of intellectual earthquake or, in Kuhn's language a paradigm shift. Margulis is one of the few living scientists who has shifted a paradigm.
"When I was an undergraduate, two theories were held up for ridicule, to show how farfetched scientific theories can get," says William Culberson, professor of botany at Duke University. "One was the theory of continental drift and the other was the symbiotic theory of the origin of the cell. Neither is laughed at today. The reason that the symbiotic theory is taken seriously is Margulis. She's changed the way we look at the cell;"
Yet, Margulis has spent much of her career on the margins of respectability, battling the scientific community's lack of familiarity with the more than 200,000 known species of microbes on Earth, most of which do nothing that directly harms or helps the human race. "Microbiology was, historically, a practical art, not a science," she says. "You know, kill the germs and save the food." Only in the past ten years have science textbooks begun to reflect her views. Ironically, she herself has become the new authority. "It's worrisome," she says. "Depressing. Authorities change. The experience doesn't. When science is taught by reading a textbook, you open the door to dogma." Her students get their feet wet.
Despite her success, Margulis' work remains controversial. Hers is not the kind of work with which the scientific community can simply agree to disagree. "It's a question of changing your religion," she says. Academia rewards its brightest stars with a specially funded teaching position called a named chair. A few years ago, Margulis was on the verge of being appointed to a named chair at a major university but was not offered the position, though the possibility still remains. The antagonism stems, in part. from Margulis' collaboration with British chemist James Lovelock on Gaia. the hypothesis that the Earth acts as a self-regulating, self-maintaining system (Phenomena, May 1988). Gaia's most vocal supporters are ecoactivists, church groups and science fiction writers. To some establishment scientists, these countercultural associations make the ideas behind Gaia suspect. Ironically, Margulis is hard on Gaia's popular supporters. "Lynn is ferocious about going after mysticism," says Stewart Brand, founder of the Whole Earth Catalog. " New Age types are drawn to her and then she busts them high, low and center for being softheaded."
In a sense, Margulis challenges the American myth of the rugged individual--alone, self- contained and able to survive. "Our concept of the individual is totally warped," she says. "All of us are walking communities of microbes. Plants are sedentary communities. Every plant and animal on Earth today is a symbiont. Iiving in close contact with others."
Consider one species of desert termite. Living in its hindgut are millions of single-celled, lemon-shaped organisms called Trichonympha ampla. Attached to the surface of one T. ampla live thousands of whiplike bacteria known as spirochetes. Inside live still other kinds of bacteria. If not for these microbial symbionts (in some wood-eating insects, the symbionts are too numerous to count), the termite, unable to digest wood, would starve.
But, the termite itself is only one element in a planetary set of interlocking, mutual interactions which Lovelock's neighbor, novelist William Golding, dubbed Gaia, for the Greek goddess of the Earth. After digesting wood, the termite expels the gas methane into the air. (In fact, the world's species of termites. cows, elephants and other animals harboring methane-producing bacteria account for a significant portion of Earth's atmospheric methane.) Methane performs the vital task of regulating the amount of oxygen in Earth's atmosphere. If there were too much oxygen, fires would burn continuously; too little and animals plants and many other live beings would suffocate. Earth s atmospheric oxygen is maintained, altered and regulated by the breathing activities of living creatures. such as those of the methane-makers in the microcosmos. Life does not passively "adapt." Rather, it actively. though "unknowingly," modifies its own environment
When NASA sponsored a search for life on Mars in the early 1970s, Lovelock looked for ways that life might have modified the Martian atmosphere. Finding no particular modification attributable to microbes or any other form of life, he and Margulis predicted that the Viking probe would find a dead Mars. They turned out to be right. "Gaia is more a point of view than a theory." says Margulis. "It is a manifestation of the organization of the planet.'
That organization resembles those hollow Russian dolls that nest one inside another. "For example, some bacteria in the hindgut of a termite cannot survive outside that microbial community," explains Gail Fleischaker, Boston University philosopher of science and a former graduate student of Margulis'. "The community of termites, in turn, requires a larger ecological nest. And so it expands. You will never find life in isolation. Life, if it exists at all, is globe covering."
Although Margulis provided the "biological ammunition" for Gaia and remains its staunch advocate, she does little work on it directly. "I've concentrated all my life on the cell," she says. The ideas that she has championed were once "too fantastic for mention in polite biological society," as one scientific observer described them in the l920s. As recently as 20 years ago, these ideas were so much at odds with the established point of view that, according to another observer, they "could not be discussed at respectable scientific meetings." Although aspects of the symbiotic theory of cell evolution still provoke hostility, the theory is now taught to high school students. "This quiet revolution in microbiological thought is primarily due to the insight and enthusiasm of Lynn Margulis," states Yale ecologist G. Evelyn Hutchinson. "Hers is one of the most constructively speculative minds, immensely learned, highly imaginative and occasionally a little naughty."
Kith and kin in lab and home
There is little separation between Margulis' professional and personal lives. You're just as likely to find her children in the lab as at her home. She drops her grandson Tonio at preschool on the way to hear a student defend his thesis. There are times when you wonder if she runs a family business. Dorion Sagan, her eldest son from her first marriage, coauthored the popular book Microcosmos along with five other scientific books. Her daughter-in-law Christie Lyons has illustrated most of them. Students say that they are treated like extended family; she shares the benefits of her prestige, insisting, as other scientists of her stature rarely do, that they are invited as well when she speaks at exclusive scientific meetings. "That's the way it should be," says Lovelock. "That's something consonant with the theories we've worked on. We're ecumenical people."
Unlike most authorities on microbes, Margulis has never taken a microbiology course. She was born in 1938 and grew up in Chicago, the eldest of four sisters. Intellectually precocious, she started the University of Chicago's undergraduate program at 14. It was the Great Books era at Chicago. Chancellor Robert Hutchins had instituted a curriculum in which students read original works, following the development of ideas rather than academic disciplines, an intellectual approach that Margulis embraces to this day. In her second year, she took a natural science course that examined the question: What is heredity? Watson and Crick had just discovered DNA, and she became fascinated. She also met a fellow student whom she later married, astronomer Carl Sagan.
Dorion Sagan laughingly refers to his parents as his Earth mother and Space father. Indeed, while Carl Sagan emphasizes the cosmos of the stars. Margulis stresses the microcosmos on Earth. Where Sagan speculates about extraterrestrial life. Margulis insists that life be seen as a planetary phenomenon whose Earthbound limits remain unexplored.
After graduation, Margulis and Sagan moved to Madison where she pursued a master's degree in zoology and genetics at the University of Wisconsin. There she studied with cell biologist Hans Ris. They discussed puzzling patterns of heredity that could not be explained by the conventional assumption that the genes in the cell's nucleus solely determined the genetic makeup of its offspring. In 1960, Margulis followed Sagan to Berkeley. For her dissertation she wanted to look for genes in the cell's cytoplasm, the area outside the nucleus; her professors tried to talk her out of it.
By l963, Ris and W. S. Plaut--another of Margulis' professors at Wisconsin--published a photograph showing that DNA resided in the cytoplasm. specifically in the chloroplasts, tiny organelles found in plant cells. (Organelles are the visible bodies and structures inside a cell.) The presence of DNA outside the nucleus baffled the biological communitv. (Boris Ephrussi. a Russian geneticist working in France. made the joke that there were two kinds of genetics--nuclear and unclear.) But not Margulis. "In Ris' classes. I had read the cell biology and genetics literature of the late 19th and early 2Oth centuries." She remembered the "crackpot" idea that the genes in the cytoplasm and the genes in the nucleus had different origins in evolution.
The first creatures to evolve happened to be the last creatures that scientists discovered. It wasn't until the advent of good microscopes in the 19th century that the scientific community began to appreciate the diversity of the microbial world. No one knew how to classify microbes. Zoologists called the moving little things animals. Botanists called the green little things plants. But neither classification made sense. It turns out that the most profound difference between living creatures lies not in their color or their locomotion but in the cells of which they are made.
There are only two types of cells on Earth. One type has a nucleus. The other type does not. Animals and plants are made of nucleated cells. Most microbes are made of nonnucleated cells. At the turn of the century, Russian biologist K. S. Mereschkovsky proposed the idea that plant and animal cells evolved from symbioses between bacterial cells. He based his theory on the similar appearances and behaviors of free-living bacteria and the organelles of plant and animal cells - their chloroplasts and nuclei. Margulis saw that the advances in electron microscopy and molecular biology vastly expanded the quality and quantity of evidence.
The years from 1963 to 196? were not easy. Margulis got her PhD at 26 and moved to Boston; she and Sagan ended their marriage. Without a formal academic position, she continued to build a case for the symbiotic theory. A big break came when she saw a list drawn up by British crystallographer J. D. Bernal of the most important unresolved biological questions of the times. One was the origin of the nucleated or eukaryotic cell. She immediately sent Bernal a three-page reply and having mimeographed it, mailed copies to scientists interested in cell evolution. Her solution was the theory that cells with nuclei evolved from the merger of two or more different bacterial cells lacking nuclei. The responses to her letter resembled a Rorschach test. One scientist corrected her grammar. Another ordered her out of his field. "Bernal said I'd solved the problem.' she says.
By 1970. she was an associate professor at Boston University and was married to Thomas N. Margulis; she was the mother of two more children and author of the first comprehensive account of her ideas, The Origin of Eukaryotic Cells. One reviewer wrote, "Readers will find this book sprawling, stimulating, irritating and challenging but they will have difficulty ignoring it." Another wrote that "it had to be a young scientist and a woman who dared to challenge the scientific establishment."
As one former student puts it, the scientific community tried to shut her up by attempting to prove her wrong and by denying her grant support. Ironically, she turned out to be right, no doubt a factor in some of the controversy she generates. "She's made people think more than any other figure in contemporary biology, and for many men it is particularly galling that this has been done by a woman," says Culberson.
By 1981, when Margulis published Symbiosis in Cell Evolution, a new version of the thesis of her first book, the scientific establishment had finally accepted the notion that mitochondria and chloroplasts evolved symbiotically. "I always thought that everyone would catch up," Margulis says wryly. With acceptance came "semi- fame," according to Betsey Dyer, a former graduate student of Margulis' and now professor of biology at Wheaton College in Norton, Massachusetts. Grant money that had been impossible to obtain came in with more ease. Margulis could no longer answer her own phone. The lab tripled in size. Then, in 1983, she received the honor that is second only to the Nobel for an American scientist: she was elected to the National Academy of Sciences. "They called out of the blue. I was totally shocked. Amazed," she says. The certificate hangs on her office wall, along with pictures of the children and one taken of her scavenging mudflats in Baja, California for spirochetes.
The case of the fast-evolving amoebas
The symbiotic scenario that Margulis has constructed for the evolution of the first nucleated cell is finallv being discussed in polite biological society. It is, and always will be, a rough scenario because no fossils and no witnesses remain. But Margulis constructs it from an impressive understanding not only of geology, genetics, molecular biology and natural history but of the microbes that flourish today. She tells the story of Prof. Kwang Jeon at the University of Tennessee at Knoxville, who noticed that the amoebas used in his research looked sick. Under the microscope he saw that perhaps 100,000 rod-shaped bacteria infected each amoeba. Only a few infected amoebas survived; of these, Jeon selected the strongest and nurtured them. Five years later, not only had the amoebas recovered, but they required the bacterial infection in order to grow at all. If such a symbiosis evolved in five years. it is easy to imagine how nucleated cells evolved in more than a billion. Margulis' scenario has clarified a new taxonomy of living things, expanding the traditional division of plants and animals into five kingdoms, each based on fundamental cell structure.
The first cells with mitochondria, the organelles that produce energy for the cell, probably appeared by 1.4 billion years ago when large quantities of oxygen first entered Earth's atmosphere. Oxygen- breathing bacteria (perhaps akin to the modern- day Bdellovibrio or Daptobacter) invaded bacteria that did not breathe oxygen. Most killed their prey, but in a handful of cases the prey resisted and worked out an uneasy truce. The prey gave the invader a continuous source of food while the invader gave the prey the means to survive in an oxygen- rich environment. What began as a hostile takeover ended as a merger--and the emergence of nucleated cells, eukaryotes.
The first cells with chloroplasts, the organelles that convert sunlight into energy, probably evolved later. This symbiosis began not as an invasion but as a meal. The host eukaryotes swallowed photosynthesizing, free- oxygenproducing bacteria (probably akin to Prochloron), but in a handful of cases the ingested bacteria resisted digestion. The new chimera managed to survive where neither could have on its own.
As might be expected from someone who thrives on combating the status quo, Margulis has not been content to rest on her laurels. She is avidly gathering evidence to prove the last and by far the most controversial, most heretical chapter of the symbiotic theory.
"We believe that the nucleated cell's internal transporation system, its ability to move within, is the contribution of another symbiotic merger with bacteria, this time with rapid whiplashing spirochetes," she writes. Spirochetes are tiny, spiral- shaped, highly mobile bacteria, of which the most notorious is the one that causes syphilis.
In mudflats along the coast of Baja, California where conditions bear a resemblance to those found on Earth three billion years ago, Margulis discovered a spirochete that, she believes, is like the ancestors of the "tail"- bearing cells in the human body, such as the sperm cells and those that line the lungs or oviduct. She also believes that related spirochetes were the ancestors of an entire intracellular transportation network, constructed of microtubules, which includes the tails and the mitotic apparatus responsible for chromosome movement in cell division.
This chapter in the symbiotic theory is considerably harder to prove. Unlike the ancestors of the mitochondria and the chloroplasts, early spirochetes left almost no tangible clues behind. Only in the past year has some tantalizing new evidence emerged. "The most important discovery of the century in cell biology is the finding made by David Luck and his colleague John Hall, at Rockefeller University, of kinetosomal DNA," says Margulis. She believes that DNA in the kinetosome, the structure from which sperm and all other cell tails grow, had at one time belonged to the free- living spirochetes.
"Most people in microbiology know this hypothesis but can't take it seriously. There's no reasonable body of evidence. My attitude is wait and see, and I'm more sympathetic than many," says Peter Greenberg, microbiologist at the University of Iowa. Supporters say it misses the point to argue that Margulis may be wrong. They cite this work as an example of her excellence as a theoretician who pushes the frontiers of current thinking with provocative, testable hypotheses. Other scientists scoff. At a conference several years ago, a former Margulis student, University of North Texas biologist Stephen Fracek, caught "a lot of flak" when he presented some preliminary data. At a postconference party, one of the staunchest critics said that he could never support the theory, even if Margulis demonstrated amino acid homologies. "There is enormous hostility to the ideas behind the data," Margulis readily acknowledges. "Some people resist the concept that the tails of their own sperm evolved from free- living spirochetes."
Margulis, who believes "absolutely" that the case for spirochete ancestry will be proved, says that it will "change everything. Neurobiology, for example, then she speculates, "You can reduce the study of the nervous system to physics and chemistry, but you're missing the microbiological step. It's as if you documented the changing surface of Earth at urban sites using Landsat images, without knowing anything about people. In the nerve cell, the axons and the dendrites that make the physical connections that allow us to communicate are latter-day spirochetes. Nerve cells, having long ago discarded the rest of the spirochete body, use the fundamental motility system of spirochetes. Think of the nerve as coming from what had formerly been a bacterium, trying but unable to rotate and swim. Thought involves motility and communication, the connection between remnant spirochetes. All I ask is that we compare human consciousness with spirochete ecology."
"History may prove she isn't always right.'- says G. Evelyn Hutchinson. "She often puts things in a dramatic way." But Margulis cares little for always being right. She cares about stripping the rungs off the evolutionary ladder, puncturing the anthropocentric view of life and encouraging her students to ask embarrassing questions. Her latest projects (coauthored with Dorion). aimed at the next generation of scientists, expose young minds to the biological riches of unseen worlds. Thev are called The Garden of Microbial Delights and The Microcosmos Coloring Book.