Unit Five: Lynn Margulis
The History of Life

Interview: Lynn Margulis

Lynn Margulis is a professor of biology at Boston University. She has provocative ideas about many of the important episodes in the history of life, including the origin of eukaryotes. In several articles and books, Dr. Margulis has built a strong case for the theory that eukaryotic cells arose as communities of prokaryotes rather than by gradual modification of individual cells. According to this concept, known as the "endosymbiotic theory," chloroplasts and mitochondria are the descendants of prokaryotes that took up residence within larger bacterial cells. Dr. Margulis also has an active interest in the diversity of contemporary organisms, and she is coauthor of Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth. This interview and the following chapters develop an important theme of biology: To understand the diversity of life we must trace its evolutionary history.

Dr. Margulis, what motivated you to choose a career in biology?

As an undergraduate at the University of Chicago, I took an introductory biology course based on one question: What is inherited from generation to generation? James Watson had taken the same course several years earlier, and I remember the Watson-Crick model being discussed when I was a student. I found that whole problem fascinating, and by the end of the course I knew I wanted to study genetics. It was that simple.

Although you were trained as a geneticist, you have a broad interest in the evolution of biological diversity, which is showcased in your book Five Kingdoms. Nearly all biologists now accept the classification of organisms into Five Kingdoms, as proposed by Robert Whittaker in a paper published in 1969. Considering the problems with the two-kingdom classification's attempt to call everything either a plant or an animal, why did it take biologists so long to adopt a new view of biological diversity?

Historical inertia. Whittaker wrote a version of his broad classification of organisms in 1959, but the concepts in the paper were continually rejected. Whittaker was a perfectionist in every sense of the word. He wouldn't send in a paper until every sentence was perfect. He wouldn't even speak a sentence until every word was perfect. And he said that papers on the Five Kingdoms were the only ones in his whole career that were repeatedly rejected. He finally got it into The American Naturalist, which had the reputation for tolerance.

What happened between '59 and '69 that made biologists more receptive to Whittaker's five-kingdom concept?

Molecular biology ... and cytology ... and electron microscopy. That is, the evidence for his concept became much clearer. Whittaker's classification arguments were ecological. For example, it always disturbed him that the fungi were considered plants because their role as decomposers has nothing whatsoever to do with the primary production of food. As an ecologist studying organisms in the field, Whittaker saw primary producers, consumers, and decomposers: plants, animals, and fungi. But he didn't know the microorganisms well. Whittaker and I spent a couple of days going over groups of microorganisms together, and he welcomed my analysis. He agreed to write the foreword to Five Kingdoms, but by that time he was dying of cancer. All his life he wanted to do a book like that himself, but it just wasn't possible; he didn't have the time and he didn't know the microorganisms.

One of your contributions to the five-kingdom classification has been a clarification of the boundaries between the kingdoms. What are the characteristics that define each kingdom?

It's like a logic tree. The first division is between prokaryotes and eukaryotes: no nucleus and nucleus. The eukaryotes consist of four branches: animals, the branch of beings that develop from sperm and egg (both are haploid), which fertilize to form a blastula (diploid); fungi, the branch that develops from haploid spores; plants, the branch that develops from a diploid embryo supported by maternal tissue. (You can't classify plants and animals by their method of nutrition. I've got movies of photosynthetic animals, and there are many nonphotosynthetic flowering plants.) And then you're stuck: The other 200,000 or so species of eukaryotes are the protoctists.

So the protoctists are defined by exclusion from the other three eukaryotic kingdoms. Would it be accurate to define the protoctists as unicellular eukaryotes and their direct multicellular descendants?

Sure ... descendants that are exclusive of plants, animals, and fungi. That's what I've had to do. In morphology and life cycles, the protoctist kingdom is by far the most diverse. When you finish evolving that group, you have practically nothing left in evolution.

The first dichotomy you described in the logic tree of the Five Kingdoms was the separation between prokaryotes and eukaryotes. In your papers, you have described the eukaryotic cell as a microbial community. Could you explain that?

When I was studying genetics, I realized that chloroplasts and mitochondria have their own genes. They are like bacteria living as symbionts within a larger host cell. When you recognize that by studying eukaryotic cells you're studying microbial community ecology, you are forced to look at real microbial communities such as the microbial mats that live in salty pools. In my field research, we're looking at a spectrum of microbial communities, from loosely organized ones to communities with tighter and tighter organization. The tightest of all is the eukaryotic cell: a microbial community that has undergone a great deal of evolution.

This brings us to the endosymbiotic theory of eukaryotic origins: the idea that chloroplasts and mitochondria descended from prokaryotes living as endosymbionts within larger cells. Many biologists believe that the transition from prokaryotes to eukaryotes is the most important chapter in the history of life. Could you expand on this?

If we ask ourselves what kind of cell is most simple, the answer is the bacterial cell. And what is the most simple bacterial cell? We would have to say a membrane-bounded cell, not a walled cell: something that is spherical and very tiny, about one-half micron in diameter. Now, how does this relate to the eukaryotic cell? You can say that mitochondria in today's cells are more similar to free-living bacteria of a certain kind that can be found in nature than they are to anything else in the eukaryotic cell.

Mitochondria not only have genes, they also have a protein synthetic system, including ribosomes, and the more you start adding to the list, the more you realize that mitochondria are like little bacterial cells. So it seems to me the case is settled about the origin of mitochondria.

And chloroplasts?

As with mitochondria, chloroplasts have much in common with certain free-living bacteria. Biologists back in the 1880s observed that chloroplasts looked like blue-green algae, which we now call cyanobacteria.

Another eukaryotic feature that must be accounted for is the microtubule. In undulipodia, which are the eukaryotic versions of flagella, microtubules are arranged in the 9 + 2 pattern [see chapter 7]. You have suggested that the undulipodium is another eukaryotic organelle descended from an endosymbiont — in this case, motile bacteria like spirochetes. Do you still believe this?

Yes. And we're finding microtubules in spirochetes that are symbionts with other microorganisms in the guts of termites. We have seen doublets, tubules arranged in twos. We have not found a 9 + 2 spirochete yet, but we've studied the structure of fewer than a dozen of the hundreds of spirochetes seen in nature. Furthermore, although microtubules apparently originated in spirochetes, I think the 9 + 2 arrangement probably evolved as a consequence of the motility symbiosis.

Microtubules, as components of spindle fibers, also function in mitosis, a process unique to eukaryotes. And meiosis, which is fundamental to eukaryotic sex, was probably derived from mitosis. How do you define sex?

Sex is any process that produces offspring that have more than one genetic parent. There are two basic kinds of sex. One is the bacterial-style sex, involving DNA-level recombination. The other is meiotic sex, involving meiosis and fertilization regularly and routinely in a life cycle. We're very careful to distinguish sex from reproduction; people are terribly confused about this. Reproduction is obligate — no organisms in the world get away without reproduction — but sex is facultative under many circumstances. Reproduction starts with at least one individual and ends up with more than one, whereas sex starts with two and ends up with one or two or many ... but it always starts with at least two.

How do you think bacterial sex began?

Sex in bacteria is a modification of their repair system. Bacteria on the early Earth were constantly threatened with ultraviolet radiation and chemicals that broke the DNA. And as long as they made new copies from a single parent, they were engaging in a straight repair process. But the minute a second parent — either a virus or pure DNA or another conjugant bacterium — became involved, then that process was, by our definition, sex.

What about meiotic sex?

The usual argument goes like this: Since asexually reproducing organisms can produce more offspring per unit of time than organisms requiring two parents, asexual reproduction is "cheaper." Why, then, has sex not been selected against entirely? What is the selective advantage of sex? Most people say sex generates more variation for natural selection to act on. I think biologists have this ass-backwards. They try to think of a mathematical reason meiotic sex occurs even if it's more "expensive."

I think most biologists don't understand either sexuality or reproduction. Two-parent sex, like chins, has no selective advantage. Let's go back to the obvious things. Bacterial sex is not directly ancestral to meiotic sex. Meiotic sex involving fertilization to form diploid nuclei evolved in protoctists before animals, plants, or fungi evolved. Some protoctists, plants, and animals seem to be bound to meiotic sexuality and fertilization in ways they can't help.

Asexuality does leave more offspring per unit time and would have won out, in the strictly Darwinian sense, if it could. When eukaryotic organisms can get rid of sex they often do. So the question is, How did meiotic sex evolve in the first place, and why are most eukaryotic organisms still bound to sex?

Can you speculate on how meiosis evolved?

Most people agree that meiosis evolved from mitosis. So, what were the selection pressures involved? Sometimes the only way to stop from dying is cannibalism. Sometimes single-celled protoctists, when threatened, they eat each other. In some cases they don't digest their prey's chromosomes and they end up with twice as many: a diploid condition. Another thing you often see is that something will block cytokinesis [the division of the cytoplasm] after mitosis doubles the chromosome number. Then the two nuclei may fuse, coming together again to produce the diploid nucleus. So there are various ways of getting these doublings of chromosome number.

Furthermore, the doubling is often pushed by unfavorable environmental conditions: desiccation, low nitrogen, change in light conditions, change in temperature. If you make a list of the things that make protoctists go sexy in the laboratory, they're almost always associated with unfavorable environmental conditions. And they're very often correlated with the formation of a resistant cyst stage.

Now, the chromosome doublings, if they keep happening, lead to uncontrollably large chromosome numbers and are lethal. The double number must be "relieved." So I suspect meiosis first evolved to relieve incomplete cannibals of their diploidy. They got into this doubled state, and meiosis had to get them out of it. Although it's in all the textbooks, there is no evidence at all that sex is required for variation. It's just something we've been taught because it makes intuitive sense, but it happens not to be true. I can't stand it when biologists claim the advantage of sex is that it leads to variation. The fungi, for example, are an enormously variable group, and one of the biggest groups of fungi (the "imperfecti") has no sex at all and they presumably derive from sexual forms.

Okay. So let's say eukaryotic cells and meiotic sex have evolved and we've got protoctists, which later give rise to plants, fungi, and animals. How do you account for the explosion of animal diversity, which seems to have been rather sudden relative to the vast scale of geologic time?

I think the suddenness aspect is not what it might seem. If you looked at southern California by satellite in 1850 and then looked at it again in 1950, you'd see an enormous and "sudden" evolution — the "sudden appearance" of a city. Yet Los Angeles didn't appear in the fossil record out of nowhere. Before there was Los Angeles, there was toolmaking, and tool using, and talking apes; there was development of architecture, metal working, automobiles, electricity. All of this and more is a prerequisite to the origin of Los Angeles. The city we see from the satellite is a physical manifestation of changes in Homo sapiens that were going on for at least 3 million years.

Like Los Angeles becoming visible from satellites, the explosion of animal diversity in the fossil record resulted from a jumping of thresholds into something visible on another level. In the late Precambrian, protoctists of hundreds of different kinds began evolving into soft-bodied animals, and then in the Cambrian, skeletonization began to occur. That's quite clear. Where animals were partially skeletonized before, they became completely skeletonized in the Cambrian, especially as animal predation evolved. So I think all these so-called explosions happen when all the prerequisites have been met.

What do you think were important prerequisites for the origin of plants, which became land organisms during the Silurian period at least 400 million years ago?

To me the big innovation in plants was lignification. [Lignin is a complex organic material that hardens the cell walls of plants.] The strengthening allows you to take the whole biosphere onto land, which requires physical support. And I think fungi were associated with that transition from the very beginning. There is certainly fossil evidence of fungi and their connections to plants from the beginning.

Which brings us to the fungi. Can you speculate on their history?

I think it's unlikely they were marine. From the very beginning they must have fed on things. Whether they started as decomposers of algae and then went into the roots of plants as symbionts or whether they started in plant roots, I don't know. But fungi and roots coevolved.

Before any of this happened, before plants and fungi and animals, before the origin of the eukaryotic cell and the protoctists, there was a long history of prokaryotic life. If a space probe like the one used in our Viking mission to Mars had landed on Earth — say 2.5 billion years ago — what would the signs of life have been?

Two and a half billion years ago you'd have bacterial mat communities similar to the contemporary versions we're working on. The fossils geologists call stromatolites are produced by microbial mat communities, just as coral reefs are produced by colonies of coral animals.

But the major sign of bacterial life would be an atmosphere in disequilibrium. The atmospheres of the inner planets have a tendency to become richer in CO2. This was being thwarted on the early Earth by the presence of life. Once life appeared, you would have been able to measure gases that are incompatible with each other. You could measure ammonia, hydrogen, and methane in the presence of oxygen, and you could measure an atmosphere that had nitrogen plus oxygen. Ammonia, methane, nitrogen, and hydrogen just shouldn't be in an atmosphere that has 20% oxygen.

Was this considered when the Viking mission attempted to identify life on Mars?

No. Measuring atmospheric gases would have been the best way to find life, but they didn't do it. If you found hydrogen-rich gases on Mars, that would have been much more impressive than any kind of visual image of something that looked like a bacterium. What was really needed was a probe that measured the indigenous gas production and uptake. These kinds of gas measurements on Earth show metabolism going on. You see that the Earth is alive, you see there's no ordinary chemical way of explaining this vast production of oxygen, especially in the presence of methane or hydrogen. This never happens in chemical systems alone.

Let's go back even further in time to the origin of life. What is your evaluation of the prevailing theory that spontaneous chemical evolution on the early Earth produced the forerunners of cells?

The monomers [amino acids and nucleotide base pairs] can be produced in laboratory simulation experiments of the early Earth without life itself. Researchers now have as many as 80 nucleotides spontaneously associating in the absence of enzymes. And when lipids are added to mixtures of organic compounds, they tend to surround and concentrate amino acids, peptides, nucleotides, and nucleotide polymers.

Astronomical cycles-tidal cycles, light cycles, hot and cold-may have been important for these chemical processes to occur early on in Earth history. One of the best techniques for concentrating organic matter is to freeze it. If you freeze it, you take the water out. And what's left are high concentrations of organics. Then you dissolve it and freeze it again. Just adding the water back allows chemistry to go on that couldn't go on otherwise. And taking the water away again concentrates the organics again. And you're not exactly where you were the first time.

We've covered about 4 billion years of Earth history. I'd like to finish with a question about the present. What qualities do you like to see in your students?

Well, certainly intellectual curiosity. One problem I'm observing is that students are scared and they want jobs, or they're here because their parents want them to be, which is very sad. I think science should be taught as a liberal art. I try to resist the pressures to make technicians out of everybody. If they don't get exposure to liberal arts thinking at the college level, they're not likely to get it for the rest of their lives. Students, like scientists, have to stop trusting authority and start looking at nature and people for themselves.

©2005 Pearson Education, Inc., publishing as Benjamin Cummings