Full Speed Ahead
By James di Properzio
Photography by Dan Dry

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As she continued her research at Boston University Margulis realized that life’s most important division was not plants versus animals. Instead, the great divide came between bacteria and all other organisms—protoctists, fungi, plants, and animals. Members of the last four groups, whether microscopic or enormous, are composed of cells with nuclei. For her, the implication was clear: bacterial cells (without nuclei) are the basic units of life, and all other organisms (with nuclei) are composite multiples. Once she came to this conclusion, traditional science seemed outdated. “Having to teach stuff that was half-true or untrue, based on a false dichotomy between animals and plants,” she says, “led me to want to document the problem.”

So with Karlene Schwartz (now a Boston University biology professor), she collected information from myriad colleagues to write Five Kingdoms. In the book—named by American Scientist magazine in 1999 as “One of the 100 (Or So) Books that Shaped a Century of Science”—they show that five categories of organisms are relevant as rational kingdom divisions: plants, animals, bacteria, protoctists (single-celled organisms with nuclei, such as amoebae, protozoa, and slime molds, and their multicellular descendants), and fungi. This system also provided an evolutionary perspective on the taxonomic groups, needed since Lamarck originated the theory of evolution.

Quick to place her work on a continuum, Margulis points out that Five Kingdoms had two notable predecessors: Robert H. Whittaker, a Cornell University ecologist who, she says, “removed all fungi from the plant kingdom,” and H. F. Copeland, a botanist at Sacramento State College, on whom Whittaker’s own work was based. Copeland had previously divided life into four kingdoms, placing all fungi in the protoctists. “I sent [Copeland] some of my work and he wrote back to me from the hospital after suffering a heart attack,” Margulis recalls. He praised her work but warned that “none of it would ever be accepted in professional biological journals.”

While Margulis and Schwartz were writing Five Kingdoms, an atmospheric chemist named James Lovelock contacted Margulis, whom he’d met through Sagan, with a question: was it possible that atmospheric methane comes from any life process? Lovelock was puzzled by the fact that methane gas is dramatically more abundant in Earth’s atmosphere—30 orders of magnitude higher—than predicted by physical and chemical forces alone. Speculating that methane and many other atmospheric gases could not have reached their current abundance in an oxygen-rich world, Lovelock theorized that such levels could not be maintained without the enormous influence of biology.

Margulis believed that an important source of methane, one of the greenhouse gases that raises the planet’s atmospheric temperature, is bacteria—found, for example, in cow rumen. When bacteria break down grass during the cow’s digestive process, the methane produced as ruminant burps joins the methane from other bacterial sources (swamps, sewage sludge, animal intestines) to influence atmospheric temperature and gas.

Together Lovelock and Margulis wrote an essay, “The Atmosphere as Circulatory System of the Biosphere—The Gaia Hypothesis,” which appeared in the Summer 1975 CoEvolution Quarterly. In Greek mythology Gaia was the Earth goddess, and in the Gaia hypothesis, Lovelock and Margulis argue, certain aspects of the atmosphere (temperature, composition of gases, oxidation-reduction state, and acidity) form a homeostatic system, and these properties are products of evolution. The atmosphere is a nonliving, actively regulated part of the biosphere, the total system of atmosphere, water, geology, and life on Earth.

“Homo sapiens sapiens are filled with arrogance—we think we are at the center of the universe and the center of life on Earth,” Margulis grumbles. “But Gaia teaches us that humans are not at the center—in fact, they aren’t even central to life on Earth. Bacteria have survived devastating impacts. Bacteria thrive on what we see as pollution, they will survive a nuclear winter. We think we have the power to wipe out life, but we only have the power to wipe out ourselves, our pets, our corn, and other visible totems of our lifestyle. All the life you see with the naked eye is just the tip of the iceberg.”

After 22 years at BU, in 1989 Margulis joined the biology department at UMass Amherst. She now lives next door to the 19th-century home of Amherst’s famous belle, the poet Emily Dickinson, and was inspired to name her 1997 book of essays Slanted Truths, which she and cowriter Dorion Sagan dedicated to Carl Sagan, after a Dickinson poem:

Tell all the Truth, but tell it slant—
Success in Circuit lies
Too bright for our infirm Delight
The Truth’s superb surprise
As Lightning to the Children eased
With explanation kind
The Truth must dazzle gradually
Or every man be blind—

The dazzling truth that Margulis presents in Acquiring Genomes, as in her teaching video Green Animals, explains how symbiogenesis acts as a major mechanism of evolution. Subtitled “A Theory of the Origins of Species,” the book is in part a dialogue with Lamarck—who proposed that new characteristics might arise during an organism’s lifetime in response to a challenge and that, if successful, they would be passed on to offspring—and Darwin—who refined Lamarck’s theory by adding natural selection. Darwin, although doubting that any characteristics arising during a single lifetime could be passed on, was nonetheless at a loss to explain the source of innovation, the new characteristics by which emergent species vary from related species.

Margulis’s theoretical work, meanwhile, argues that most life evolves by trading whole genomes, as happens routinely in the microbial world; and the mergers of whole bacteria into other cells, forming a thriving symbiosis, is the source of all larger life. Her latest paper describes a species of protoctist, Staurojoenina assimilis, with striations across its surfaces. Those distinguishing tiny zebra stripes, Margulis and her colleagues have discovered, although always found on the protist, were not originally part of its body. Rather they are rod-shaped bacteria attached to the surface in “obligate” symbiosis: you don’t find one without the other.

For Margulis such careful examination of a tiny organism recalls her days of washing amoebae—and continues to give her food for thought. “I care about the science—I always go back to the science,” she says. “I try to reconstruct the history of the cell from modern clues including the fossil record—that is the central idea.”

She takes pride in the fact that her ideas are now becoming a part of the larger body of scientific thought. “Two of my four original postulates are now accepted as correct by all knowledgeable scientists,” she says, lapsing into science-speak, “that mitochondria come from oxygen-respiring alpha proteobacteria—we even know the details—and that plastids evolved from cyanobacteria.

“The third part of the idea,” she continues, “is that the basic cytoplasm that did the trapping evolved from acid- and heat-resistant archaebacteria, like Thermoplasma acidophilum. This is now supported by lots of evidence, mainly put together by my UMass colleagues, Dennis Searcy and Michael Dolan.”

Her fourth postulate from graduate-school days is the idea that cilia and sperm tails have spirochete ancestors—corkscrew-shaped, wriggly bacteria that attached to other organisms and developed a symbiosis that functions in movement and sensation. According to this argument, the rods and cones of our eyes are descendants of light-sensitive swimming bacteria, which once had the structure of independent cells and their own complement of DNA. Once again, most scientists think that she has gone too far, and peer reviewers have refused to approve her federal research grants, cut to zero over the last two years.

But Margulis, characteristically shrugging off the criticism, remains optimistic. “I think we are finally in a position to prove” the spirochete postulate. “I do think we can now, with the use of the new molecular-biology techniques, show the bacterial origins of the cilia, sperm tails, and other motile and sensory microtubular structures of cells. In fact,” she adds with the relentless drive that propels her early-morning bike rides, “we have big plans for next year.”

James di Properzio, a graduate of St John’s College, is a freelance writer and editor of scientific and literary texts. He lives in Greenfield, Massachusetts.

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