Margulis is a controversial figure in the world of biological science. Many of the ideas she and Sagan put forth in Microcosmos, which met stiff resistance at the time, are now widely accepted. In this, the first part of a four-part interview, Margulis talks about how scientific understanding of early life on Earth has changed, and explains one of the central ideas of her life's work: symbiogenesis.

Astrobiology Magazine: This year marks the twentieth anniversary of the publication of Microcosmos, which you co-authored with your son Dorion Sagan. You expressed some ideas that at the time were considered pretty maverick. How much controversy did the book generate?

Lynn Margulis: Well it depends on which aspects. The idea that the Precambrian, that is from 4600 million years ago to 541 million years ago, 7/8ths of the entire fossil record, was empty, that nothing happened for all that time, that the fossils were so scare that you couldn't trace lineages - that idea prevailed such that Stephen Jay Gould said it relatively recently before he died. It was overturned almost exclusively by the science supported by this guy Dick Young. He started as an embryologist, and he started funding non-human NASA biology

Young had a great deal of insight. He funded people like Elso Barghorn, the professor at Harvard who in 1954 published a paper describing two billion year old plants from the Gunflint chert. They weren't plants, of course, they were bacteria, but at the time the world was divided into plants and animals and there wasn't any choice. Young funded the whole activity that started as exobiology - today it's more astrobiology than exobiology - that completely turned around that idea. And I was privileged to be involved with those people as these data were coming in on the evidence for early life.

Our book is very microbe-centric. The world is very anthropocentric. What we did was sort of turn it around, put the people on the bottom and the microbes on the top as far as their importance in running the ecological system of the Earth. We said people are totally late, typical animals, and are really very unimportant in the workings of the system, whereas the microbes are much earlier, they do all the major gas transformations, they created all the major things we think are important, like sex.

Today we might say that this turnaround - people down and microbes up in a world that has always had people up and microbes down -is a strategic perceptual shift. As humans, you can't escape your human perspective. We have a more nuanced view than we had in Microcosmos. On the other hand, at the time it was absolutely necessary to make that shift toward microbial perception because of the skewed anthropocentrism that was driving everything.

AM: So the idea that there was a microbial fossil record going back billions of years was not well-accepted 20 years ago?

LM: It was not even known at all. It's still not well known. Among sophisticated scientists, it's very much more known now than it was then, but then it was not known at all. There were a lot of explanations, and none of them were really valid. Because the answer for the emptiness of the Precambrian, with respect to fossils and life, has to do with detection. You don't see dinosaur footprints. And you don't see fossil jaws. Because the action is going on on a microbial scale and you're not prepared to see it. But when you start becoming prepared to see the microbial contribution, then you see that the fossil record is loaded, at all times, from the origin of life to the present.

AM: One of the central ideas you develop in Microcosmos is the concept of symbiogenesis. Can you explain what that is?

LM: Sure. When organisms of different species or with different kinds of current histories live in physical contact, that is symbiosis. And they have to be in physical contact for more than half of the life history of at least one of them. So you have a symbiosis not with your father, if he's still paying your rent, but with your underarm bacteria, and the ones between your toes. Someone recently calculated that there are more bacterial cells per human body than there are human cells.

And that's partly because bacterial cells are small - you can fit a thousand of them into one animal cell. At any rate, you have a hugely important symbiotic relationship with intestinal microbiota, because various vitamins are made by them, and so on. So symbiosis is simply the living together in physical contact of organisms from different species.

Symbiosis is an ecological relationship. Pollen ecology is also a relationship between organisms of different species. You've got flower and bees, for example. But that's not symbiosis, because there's no long-term physical association. So symbiosis is an ecological relationship, and it is a precursor to symbiogenesis.

Symbiogenesis is an evolutionary relationship. It's symbiosis over time, such that a new feature can be recognized as a product of that symbiosis.

For example, I have film of photosynthetic animals. These animals have closed mouths and they lie in the sun and they derive their nutrients from photosynthesis. But you can tell where they come from because they have a lot of relatives that are not green. The photosynthetic animals are green. They can be mollusks, they can be worms - it happened many times. But their direct ancestors aren't green, they're still eating, they have intestines and so on.

So the symbiogenesis part is when, after long association of these animals with what was begun as an algal food, the food was retained, the animal became more and more translucent, and we ended up with a symbiotic permanent relationship that is present in every animal in the population. So you would say the appearance of a green animal is the product of symbiogenesis. A long-term symbiosis can lead to new organs, new tissues, new behaviors - and that is symbiogenesis.

AM: In Microcosmos, you argued that eukaryotic cells, the cells that animals, plants and mushrooms are made of, came about through symbiogenesis. Was that idea well accepted at first?

LM: Absolutely it was not. I was invited to Yale University to give a little talk to George Evelyn Hutchinson's seminar. He was a founder of American ecology. He said the symbiogenesis idea skipped an academic generation. He called himself with respect to me the grandparent generation. In his generation, these ideas were at least discussed, and many times favorably. In the parent generation, he said, they were totally suppressed. The grandparental generation was in the early 1900s, up through the 1920s. After the 1920s, and before the 1960s, that kind of information was suppressed by the neo-Darwinists.

Neo-Darwinism comes from the combination of two ideas. The acceptance that Darwin is right about all organisms on Earth having common ancestry and that evolution of life has occurred. But that Gregor Mendel is also right when he shows that inheritance factors are simply recombined, they don't change through time.

For example, you cross a red flower and a white flower - a rose, say - and you get a pink rose; and then you cross the pink rose back to the parents, you get ratios of red, pink and white that are absolutely identical to the parents. You don't lose the red or lose the white - ever. That's what Mendel showed. In other words, the genetic factors are simply recombined; there's no evolution.

Now Mendel is often touted to be this backwater monk who played with his garden peas. But Mendel was in touch with the pope. He knew damn well what was going on with the concept of evolution and did not like it.

The supporters of neo-Darwinism, which is also called the modern synthesis, wanted to reconcile - they had to reconcile - Darwinian change through time with this brilliant, experimentally proven concept of Gregor Mendel.

This field they invented is called evolutionary biology by a lot of people, or sometimes population genetics. I think the whole thing's corrupt. I think it's repulsively corrupt. Because it has no reference in the real world.

It was made from the beginning as a very clever generalization to combine the fact of Darwinian change through time, which seems to be based on fossils and lots of other evidence, with the evident fact that Mendel was right about genetic factors recombining. And so it developed a superstructure, a theory of which only a very small part could be verified by science. And it was called population genetics, because the word evolution, at least in this country, is a dirty word amongst a lot of people.

And as Hutchinson pointed out, symbiosis was considered communist and Russian. The great work had been done in Russia.

AM: How did you get interested in these ideas?

LM: I started to study cytoplasmic genetics. In nuclear genetics, the standard genetics, offspring have half the genes of each of the parents: half of the female parent, half of the male parent. That's true of animals and plants. But mitochondria don't follow those rules at all. They have all the genes from the mitochondria of the mother only. That's single-parent genetics. So cytoplasmic genetics is the field of the ones that don't follow the rules of the nucleus of the cell, and that's the field of genetics I started with.

I didn't know anything about bacteria. But I was interested in these anomalous exceptions to the rules of nuclear genetics. And starting that way, I realized that there was a literature and there was an understanding that had been suppressed. And that is that the chloroplasts and the mitochondria have their own genes, they have their own rules of transmission, and the best explanation is the Russian one: that they started as independent organisms.

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