Earth mother, microbe lover

Worldly wise: 7. Biologist Lynn Margulis hates being seen as a 'woman scientist', rejects the current model of evolution and worships microbes. Andrew Robinson tries to find out what makes a controversialist

I'd rather share a platform with Attila the Hun," snapped Richard Dawkins, Oxford zoologist and best-selling science writer, on being asked by Cambridge students to speak alongside the American microbiologist Lynn Margulis. Sharp, even by Dawkins's standards; and this antipathy towards Margulis, a professor at the University of Massachusetts, is shared by others. Yet many academics speak very highly of the woman the journal Science dubbed "science's unruly earth mother"; American biologist Edward O. Wilson, for instance, calls her "one of the most successful synthetic thinkers in modern biology". What is it that makes this 60-year-old mother of four so controversial - a sort of Noam Chomsky of the life sciences?

I met her in a cluttered curator's office at New York's Museum of Natural History. Her forthrightness was immediately apparent - there is nothing PC about Margulis. She particularly resists attempts to pigeonhole her as a role model for young female scientists. "People constantly ask me to talk about 'the feminist view of evolution," she sighs.

"I hate the words role model. I spend most of my time trying to get back to doing science. It's extremely hard, and being a woman role model makes it much harder." Even outside science, Margulis has no use for women's studies as a separate discipline. "I think it's a bunch of phoniness. It's an excuse for people who can't make it in real study. There's no women's history, there's only history. My daughter calls me a 'closet feminist', but I am not a feminist at all."

Strong views - but it is not these that get under the skin of neo-Darwinists like Dawkins. It is, rather, her radically different theory of evolution and her effervescent championing of the controversial Gaia hypothesis of James Lovelock. The Gaia theory (named after the ancient Greek goddess of the earth) suggests that Earth can be considered as a single, self-regulating, "living" system. It irritates the majority of scientists who regard it as both unnecessary and "mystical".

In their view, it is best to regard living creatures (plants and animals) and the non-living environment (rocks, the oceans, etc) as independent, though interacting systems that will ultimately be explained at the level of atoms, molecules and genes by the laws of physics and chemistry. "Natural selection", Darwin's famous idea, thus consists of living creatures competing with each other to adapt to the conditions of a dead environment - those that are fittest surviving and reproducing, the rest dying off.

Margulis explains: "To me Gaia has no goddess implications at all. Gaia is the system at the surface of the earth that gives the planet properties of life." These "properties of life" include the earth's ability to regulate atmospheric gases like oxygen and to control surface temperature and the acidity and alkalinity of the oceans so that life can flourish. "The Gaian view is useful because it leads one to ask questions which one would not otherwise ask, such as why the oxygen in the earth's atmosphere is at 20 per cent?" - unlike the atmospheres of lifeless Mars and Venus and unlike that of the early earth before life (when there was very little oxygen).

Why on earth would "adaptation" to a low-oxygen environment have produced oxygen-loving animals and plants? "It makes no sense on the old-fashioned adaptationist paradigm but it is totally understandable from a Gaian point of view," says Margulis.

None of this would have been enough to provoke scientists to attack Margulis, had it not been for the fact that, in the past decade, Gaian science has scored notable successes and attracted talented scientists (whether they use the goddess's name or prefer the more fundable "earth system science"). Even more important is that growing evidence for Margulis's key scientific idea, Serial Endosymbiosis Theory (SET), has steadily pushed it to centre stage in the biological sciences.

Put at its simplest, Margulis maintains that the principal source of evolutionary innovation, the origin of new species, is not through the random mutation of genes edited by natural selection - the neo-Darwinist view - but through the amalgamating of different strains of bacterial cells, descended from our common bacterial ancestor: symbiogenesis.

Symbiosis may be defined as the living together of two or more organisms in mutually beneficial association. The sea anemone attaches itself to the shell of the hermit crab. The anemone provides the crab with camouflage, while stray bits of the crab's food nourish the anemone. At the level of an individual cell, symbiosis can occur when a cell swallows a bacterium belonging to another species - endosymbiosis. Successive swallowings - serial endosymbiosis - can lead to the creation of new species.

"My claim," writes Margulis in Symbiotic Planet, her forthcoming book, "is that, like all other apes, humans are not the work of God but of thousands of millions of years of interaction among highly responsive microbes. This view is unsettling to some ... I find it fascinating." Using endless evidence from her beloved microbial world, Margulis is out to show that living organisms not only compete and struggle, as the neo-Darwinians proclaim, they also associate and work together.

The emphasis on symbiosis is not original to Margulis. It was a familiar notion among biologists earlier this century. But the association of germs with disease, the rise of neo-Darwinism and the triumph of molecular biology (the discovery of DNA's double-helix structure in 1953) killed symbiotic theory off. When the young Lynn Sagan (Margulis's first husband was the astrophysicist Carl Sagan) tried to publish on endosymbiosis in the mid-1960s, she met a brick wall - her paper was rejected 15 times and lost altogether by Science.

In it, Margulis proposed that the energy-producing organelles inside cells, known as mitochondria, were originally bacteria that had been swallowed by the cells; but she had no proof for this unorthodox idea. Then, in the 1970s, came clinching evidence. When mitochondrial DNA was analysed, it turned out to be different from the DNA in the nucleus of the cell and to be similar to that of purple photosynthesising bacteria. In other words, mitochondria proved to be naturalised immigrants, rather than native cellular citizens.

Today, the Margulis explanation of the origin of mitochondria is a staple of biology textbooks. But not in a form that satisfies its author. "The exposition is dogmatic, misleading, not logically argued and often frankly incorrect. They say, this is 'female' evolution. The 'male' evolution is competitive Darwinism, and Serial Endosymbiosis Theory is cooperative, gentler and kinder evolution."

She feels that microbes have had a bad press, both among scientists and the general public. Most biologists, she says, are dismissive of microbes as primitive organisms: "When Dawkins says 'lower organism', he means rat or bee. People generally don't know anything about microbes except they've been told microbes are going to kill 'em. The terminology is military: microbes are labelled enemy agents, we have to conquer disease, etc." She calls herself a "microbial chauvinist" and is delighted by the fact that sociobiologist E. O. Wilson, who is a world expert on ants, concluded his recent autobiography with a paean to microbes: "If I could ... relive my vision in the 21st century, I would be a microbial ecologist. Ten billion bacteria live in a gram of ordinary soil, a mere pinch held between thumb and forefinger. They represent thousands of species, almost none of which are known to science."

As Margulis likes to point out, when Neil Armstrong stepped on to the moon and said "One small step for a man, one giant leap for mankind", "he overlooked vast numbers of bacteria on his skin and in his intestine that stepped with him."

Her bug's-eye perspective has led to a passion to establish a different ruling taxonomy of species in biology, set out in Five Kingdoms, written with Karlene Schwartz. Most biologists, she says, are satisfied with a three-kingdom classification: plants, animals and microbes. But this misrepresents evolution, because the ancestors of plants and animals were neither plants nor animals; and it leads to serious confusion in the classification of early organisms, with the introduction of the term protozoa (meaning 'first animals') to cover organisms such as certain algae - which might just as well be regarded as plants. Margulis avoids "protozoa" and prefers to speak of "protoctists", which means simply "first beings". Her five kingdoms in order of their evolution are therefore: bacteria (cells without nuclei), protoctists (cells with nuclei), animals, plants and fungi.

The five kingdoms have important support, for instance from the veteran evolutionary biologist Ernst Mayr and from the palaeontologist Stephen Jay Gould. But there is a rival scheme, that of Carl Woese, proposing three kingdoms based not on an organism's structure or function but on the composition of its DNA. It is a case of biologists versus chemists, non-reductionists versus reductionists, says Margulis, who cannot resist a dig:"Chemists often can't tell the difference between a live system and a dead one."

For almost her entire career, Margulis has battled on two fronts: for the symbiotic theory of cell evolution and for the Gaia hypothesis. She is still unclear how her two scientific passions are connected. "'Mom, what does the Gaia idea have to do with your symbiotic theory?' asked my son Zach, aged 17, after work one day," she begins her Symbiotic Planet. "'Nothing,' I immediately responded. 'Or at least nothing as far as I'm aware.'" But she likes to quote a former student, Gregory Hinkle, who quipped: "Gaia is just symbiosis as seen from space." She explains: "If you get off the surface of the planet you see that organisms are in physical contact, through the surface waters or through the atmosphere, that is, organisms are always producing gases to the atmosphere or removing gases from the atmosphere. So from a distance, Gaia is simply symbiosis as seen from space."

Even Margulis's strongest detractors grant that she is a fecund figure in today's biology. It may be that, to quote another former student Tom Wakeford, now lecturing at the University of East London: "As so often in the history of science, Margulis herself has become so notorious that we have to wait for another generation to reap the full rewards of her insights."