Interview with Lynn Margulis, Part I
October 1, 2006
Twenty years have passed since the publication of Microcosmos: Four Billion Years of Microbial Evolution, co-authored by Lynn Margulis and her son Dorion Sagan. To mark this anniversary, Astrobiology Magazine interviewed Margulis, distinguished university professor of geosciences at the University of Massachusetts in Amherst. 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 scarce 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.
We Are All Microbes
Interview with Lynn Margulis, Part II
October 5, 2006
Microcosmos: Four Billion Years of Microbial Evolution, co-authored by Lynn Margulis and her son Dorion Sagan, was first published twenty years ago. Astrobiology Magazine recently interviewed Margulis, to find out how her and Sagan's ideas have stood the test of time. In this, the second part of a four-part interview, she talks about four specific microbial organisms that, through fusion, yielded modern plant and animal cells.
Astrobiology Magazine: In Microcosmos, you detailed four specific microorganisms that you thought were involved, through symbiogenesis, in the creation of various eukaryotic cells, the type of cells that animals and plants are made of. At the time, those ideas were not well accepted. Has that changed?
Lynn Margulis: Well, we've won three out of four.
Nobody today doubts that chloroplasts began as cyanobacteria. Chloroplasts are the little green dots in the cells of plants and algae, in which all photosynthesis occurs. Photosynthesis, the conversion of sunlight as energy to food and cell material, is fundamentally a bacterial virtuosity. It began in a specific group of oxygen-producing photosynthetic bacteria that, by definition, are cyanobacteria. If they're green, they're photosynthetic. They make food only in the sunlight, because they require sunlight for their source of energy. They take carbon dioxide out of the atmosphere, and fix it, that is, chemically change it to food and body, and they produce oxygen as waste. That series of changes is done by cyanobacteria exclusively. They're the only organisms that can make the oxygen and make the food that everything else needs.
Well, you say, can't plants do that? And the answer is yes, but plants are something that hold up cyanobacteria. That's all plants are. It's the cyanobacteria in the plants that do that transformation. You say, well, can't algae in the water, green water scum, can't they do it? And the answer is, yes, but the algae are something that brings the little green things inside the scum to the light. So the answer is: nothing but cyanobacteria can make our food and produce our oxygen.
We like to call them the greater bacteria, or the greatest bacteria, because they are. And they're in only three forms: they're in cyanobacteria (what used to be called blue-green algae) all by themselves; or they're in algae; or they're in plants. But fundamentally, if you cut them out of the plant cell, and throw away the rest of the plant cell, the little green dot is the only thing that can do that oxygen production. That is the greatest achievement of life on Earth, and it occurred extremely early in the history of life. Who knows whether it's 3 billion years ago, or 2.7 billion, or 3.5 billion, but it's that kind of time. And the idea that those little organelles, those little bodies inside of cells, started as free-living cyanobacteria is completely accepted by everybody who even thinks about these problems.
So that's one out of four.
AM: Number two is mitochondria, right?
LM: Yes. Mitochondria are little dots inside the cells of animals and plants and fungi, and all sorts of other organisms with hard names--those mitochondria are where the oxygen is actually respired. Mammals, including people, take oxygen out of the air into the bloodstream, and carry the oxygen all over the body, to all the cells. Inside each cell, the oxygen reacts with hydrogen atoms that are stripped off food as the food is converted into body parts and used for energy. This oxidation of the foodstuffs is carried out by little particles, the mitochondria, that are one micron, the size of bacteria, inside the animal cell, inside the plant cell, inside the amoeba cell, inside the mushroom cell, and so on. That's what respiration is, and that respiration comes from bacteria that used to be free-living. We know a lot about those bacteria. They used to be able to swim, they used to be able to break down glucose all by themselves, etc. The idea is that mitochondria are from bacteria was harder to accept, but it's now acceptable.
So that's two out of four.
AM: Okay, and number three?
LM: Well, then the question is, What type of cell incorporated the mitochondria, and eventually the chloroplasts, some of them, into itself? What was the original eukaryotic cell? The original cell was an archaebacterium. It was sulfanogenic; it made hydrogen sulfide. We have just reviewed the evidence for that. People are not against that idea at all, because there's a lot of molecular biological evidence for that.
So that's three out of four.
AM: And what's the fourth one? What's left?
LM: The problem I'm still wrestling with is the origin of cilia, which are exactly the same in cross-section as sperm tails. That's the piece that's not been proven, the origin of the wiggly things. They all have strikingly identical 9-fold symmetry in cross-section, so it makes them easily identifiable. We believe the origin of that cell structure is from a free-living organism called a spirochete. That's the part that has been rejected, based on the usual nothing - based on prejudice.
If you look at Microcosmos, you'll see what we call spirochetal secret agents. But it's harder to put your mind around. You don't often hear of this connection between free-living bacteria and the movement inside cells, because there are so many different names associated with these motile structures. Historically they were approached by such different people in so many different studies in so many different fields and so many different countries.
Spirochetes are infamous because they are known to be the infectious agents of both syphilis and Lyme disease, and periodontal diseases are associated with oral spirochetes. Four of the spirochetes have been sequenced, because they're of medical interest.
But a colleague (through the literature only - we don't know her) named Galena Dubinina, a senior-level microbiologist at Moscow University, has sequenced the relevant spirochetes, the ones that can be directly compared with what we're claiming grew into being the cilia. And so what we are working on is either confirming or negating our predictions about the free-living version. We have these organelles, the cilia, on the cells. We now have, because of her work, the right spirochetes to study the sequences in, and we have very explicit predictions. We're trying to do that comparison, which is exactly what was done to prove the mitochondrial ancestry from the alpha-Proteobacteria, and the chloroplast ancestry from the Cyanobacteria.
Those same types of arguments are now, for the first time, usable to prove the spirochete origin of cilia. So that's what we want to do, confirm that last, fourth prediction. We want to win four out of four.
Bacteria Don't Have Species
Interview with Lynn Margulis, Part III
Lynn Margulis and Dorion Sagan first published the controversial book Microcosmos: Four Billion Years of Microbial Evolution, in 1986. Although many of the ideas in Microcosmos are now widely accepted, Margulis is still a controversial figure in the biological sciences. In this, the third in a four-part interview with Astrobiology Magazine, she explains why she believes that the notion of species doesn't apply to bacteria, and why she rejects the separation of Archaea into a different domain of life from Bacteria.
Astrobiology Magazine: You have argued that bacteria don't have species. I wonder if you could explain that idea.
Lynn Margulis: Bacteria are much more of a continuum. They drop their genes all the time. Like we say in What is Life?, it's like going swimming in a swimming pool, going in blue-eyed and coming out brown-eyed, just because you've gulped the water. Obviously, animals don't do that. But that's what bacteria do, all the time. They just pick up genes, they throw away genes, and they are very flexible about that.
Say you have a bacterium like Azotobacter. This is a nitrogen-fixing bacterium. It takes nitrogen out of the air and puts it into useable food. Nitrogen fixing is a big deal. It takes a lot of genes. If you put a little something like arsenium bromide in a test tube with these organisms, and put it in a refrigerator overnight, lo and behold, the next day the cells can't do this anymore, they can't fix nitrogen. So by definition you have to change them from one genus to another.
I'll give you another example: E. coli. It's a normal inhabitant of the human gut. If you put a particular plasmid into E. coli, all of a sudden you have Klebsiella and not E. coli. You've changed not only the species, but the genus. It's like changing a person to a chimpanzee. Can you imagine doing that, putting a chimpanzee in the refrigerator, and getting him out the next morning, and now he's a person?
Sorin Sonea, who was the chair of the microbiology department at the Université de Montreal, in Canada, has been saying for 25 or 30 years that you either have to consider all the bacteria on Earth as one species, or you have to consider them as no species at all. The criteria we use for species, which are good ones for animals and plants and fungi, do not apply, because bacteria can change overnight. You have all sorts of gradations, where adding or removing a few genes will change an organism's name, because those genes are what define the organism.
For example, Agrobacterium causes tumors on the crown of a plant, where the soil meets the base of the plant. If you get rid of just one plasmid, Agrobacterium can't make the tumor anymore. So it's now got a new name, by definition. So you've got this terrifically arbitrary situation.
But microbiology's mostly not science, it's practical art. That comes from its beginnings with Pasteur. Microbiologists are pragmatic, pious businessmen. There's no intellectual tradition in microbiology.
Bacteria do not have species. The rules for species naming do not apply to bacteria. But they need to have identity labels because of the practical importance in agriculture and health.
AM: So what would you call them, these different microbial organisms?
LM: You'd call them bacterial strains, or something like that. They definitely have some kind of identity. The genus name is more important than the species name. The genus name does correlate with a lot of common traits. But the reason the species were imposed is because they're socially so important, they're economically so important, that you can't have total chaos. You have to have a name, just like you have to have a name for diseases. How can you treat them if you don't have a name?
When you get to any eukaryotic organism, a species is a meaningful term. It represents the entire group. Species are discontinuous and distinct in the eukaryotes. But they're just not in bacteria. It's a continuum.
AM: Carl Woese in the late 1970s discovered a group of microorganisms that he named Archaea, and he drew a new tree of life, in which the major subdivisions were three domains - Archaea, Bacteria and Eukarya - rather than five kingdoms. But you like the five-kingdoms approach better. That was a surprise to me, because it was in part Woese's redrawing of the tree that helped bring the importance of microbes to more general awareness.
LM: Okay. I think that's a really crucial thing.
The first thing to say is that Woese made an unprecedented contribution, because he's got a single gene, namely the one for 16S RNA, which is present in all cells - because they don't work otherwise. And that gene can be compared in all organisms, whether they have feathers or teeth, or leaves, or spores, or whatever it is. That gives you what the 19th century people called a "partial phylogeny." It gives you a trait that can be traced through every cellular organism.
By tracing that gene he found that there are these two major groups of bacteria, and then most of the eukaryotes are relatively uniform with respect to this one trait. That's so far, so good. But he's worse than wrong about taking that trait as representing the live organism and the organism's history. That's where there's a horrible problem.
And the problem is that you've only got one gene. But an organism has 30,000 genes (if it's a eukaryote), and he's ignoring 29,999. (If it's a prokaryote, it typically has 5 or 6 thousand genes.) So you're not studying the lineage of live organisms when you study this gene. You're studying this gene.
Now this gene does give you an insight, and I would not deny that.
If Woese had not seen the differences between Archaebacteria and Eubacteria, I wouldn't have been able to see that all eukaryotes have both types in their ancestry, and therefore are products of symbiogenesis. It's a very valid point.
And being able to quickly assess what kind of bacteria an organism is with respect to this 16S RNA, all of that's very useful and very practical. And very informative. But what he's done is extrapolated it way beyond what it's really telling you. What amazes me is how fast people accepted this. Archaebacteria can exchange genes with Eubacteria. They are bacteria in every way.
Interview with Lynn Margulis, Part IV
October 12, 2006
Lynn Margulis and Dorion Sagan are the authors of Microcosmos: Four Billion Years of Microbial Evolution, which was first published twenty years ago. To mark the occasion, Astrobiology Magazine spoke with Margulis, whose ideas have long been considered controversial. In this, the fourth and final part of a four-part interview, she lays out the evidence for bacterial intelligence, and shares her thoughts on the likelihood of life on Mars.
Astrobiology Magazine: In Microcosmos, you talk about bacterial intelligence. A lot of people have trouble with that concept because -
Lynn Margulis: - Well, they haven't been to parties with adolescents -
AM: - they tend to think intelligence comes from brains.
LM: I know they do. They're wrong.
AM: Can you explain how you view bacteria as being intelligent?
LM: If you look up consciousness in the dictionary, it says, "awareness of the world around you," and that's because you lose it somehow when you become unconscious, right? Well, you can show that microorganisms, or bacteria, are certainly conscious. They will orient themselves, they will work together to make structures. They'll do a lot of things. This ability to respond specifically to the environment and to act creatively, in the sense that that precise action has never been taken before, is a property of life. Of course, it has to be moving life, or you can't tell. You can't tell if a plant is thinking, but in organisms that move, you can tell their intelligence.
For example, take Foraminifera - they're single-celled sea creatures, protoctists. The Egyptian pyramids are built of their shells. A colleague of mine put one of these forams in a dish with a small crustacean animal, like a water flea. He was going to watch the crustacean eat the foram. The foram's a single cell, and smaller, right? And he saw the foram kill, trap, and completely destroy and eat the animal. He's got beautiful movies of it. So that group of organisms not only can eat animals, but they can make hunting towers, and they can hunt from the top of the towers.
There's a group of them, called agglutinating forams, these have offspring that look exactly like the parent, with multi colors. But every generation they construct their coloration from pebbles. This single-celled blob - it would look to you like a blob of snot, probably - can pick up pebbles of the different colors. You have to have some red ones and some white ones and some black ones in order to get an offspring that looks like a parent. They will make appropriate choices such that when you see the offspring next to the parent, it looks like they just came about by dividing in half. You can't believe that the newer one, the offspring one, was naked, and then it spent a lot of time plastering and remolding and rearranging pebbles on the surface of itself, so that it now looks indistinguishable from its parent. Those kinds of activities are rampant.
People think that if you can't talk, you can't be intelligent. But you know that's not true if you have a dog. You can communicate with them without talking. If you define intelligence as speaking American English, well maybe they're not. But if you define it in the much more broad sense of behaviors that are modified on the individual level, that involve choice and change and response to the environment, there's every bit of evidence that intelligence is a property of life from the very beginning. It's been modified, of course, and changed and amplified, even, but it's an intrinsic property of cells.
AM: You support the Gaia theory, the view that Earth's biosphere is a living superorganism that's capable of self-regulation.
LM: That's what James Lovelock, who developed the Gaia theory, might say, and I disagree with him about the word "organism" in there, super or not. Why? Because no single organism is known that breathes in its spent gasses and eat its own waste, drinks its own liquid waste, and survives. An organism is too small, in principle, the way one person is not a family, and one family is not a city, to be the self-regulating system that Gaia refers to. So I would replace the word "organism," or "superorganism" with, say, "ecosystem," or "set of communities that make an ecosystem." The original Gaia hypothesis was that Earth was a physiological, self-regulating system with respect to temperature, reactive gas composition and acidity-alkalinity. Because if that system were destroyed on the surface of the Earth, then the Earth would become completely reflective of its cosmic background. It would just be an interpolation between Mars and Venus, like it probably started.
AM: That's a good lead-in to the next question I wanted to ask you. What does the Gaia theory predict about the likelihood of finding evidence for life on Mars?
LM: Gaia from a distance sees no life on Mars. Jim Lovelock and I wrote a paper in 1974 that said that from a Gaian point of view there is no life on Mars, you're wasting your time to go. We said the atmosphere was what you would expect of a sort of a steady-state composition at this distance from the sun, that there was no evidence from space that the living phenomenon was occurring on Mars, the way there is from space that it is occurring on the Earth.
I would say that that would still be true, unless there was some form of deep-freeze dormant life. If there's life on Mars, it's got to be such that it does not influence the measurable aspects of the environment. I would still bet there isn't any, but I certainly can't preclude the idea that there's dormant, deep life, cave life, quiet life, that just doesn't have a planetary-level effect because it's so sparse. I can't preclude that, but I think it's very doubtful.
At any rate, the Gaia hypothesis I think is totally useful. It was invented as an explanation of the differences between Mars, Venus and Earth, and it does give us fantastic criteria. If you go to Jupiter and see hydrogen, methane, ammonia, water, hydrogen sulfide, those are all chemically reduced gasses compatible with each other. But if you see, in the presence of overwhelming chemically reduced gasses, even a trace of oxygen or carbon dioxide, you don't have a test for life, but you have a putative indication of life. It tells you, Get over there and do something about it, because that's what you'd expect of a living system. It leads to environmental inconsistencies. That's one of the beautiful things about the Gaia hypothesis: you don't have to know anything else, but you can detect a chemical anomaly, and then use it as a criterion for further exploration.