Lynn Margulis - an appreciation

Lynn Margulis passed away recently at the age of 73 (NY Times obituary). She was responsible for one of the great ideas of modern biology -- the endosymbiotic theory for the origin of organelles. This is the idea that chloroplasts and mitochondria of eukaryotic cells originated as independent prokaryotes that became associated symbiotically with host cells, and eventually became indispensable organelles. The whole process she called "symbiogenesis". Siva blogged about this here two days ago, and suggested that I share something to.

The story of the theory itself is also quite well known. Margulis put forward the hypothesis in a paper titled "On the origin of mitosing cells" (Journal of Theoretical Biology 14: 225, under her married name L. Sagan - PubMed, ScienceDirect) in 1967, but before it was accepted for publication there, it had been rejected 15 times by other journals. It was initially controversial--to think that an essential part of our own cells are actually bacteria in disguise!--but today it is textbook knowledge. Much like the theory of plate tectonics, this is one of the great Cinderella stories of modern science.

I was fortunate enough to hear Margulis speak a few years ago when I was in college. I don't remember the details now, but I do remember a few things she said. She recalled that the last time she was at Harvard, it was at a seminar where Ernst Mayr (one of the pioneers of the Neo-Darwinian Synthesis) was in the audience, sitting right there; she pointed at the seat in front of my friend Noor and me and we got a little thrill from it. "Although he was almost a hundred years old, he was still the sharpest mind in the room!"

(She wrote a reminiscence of Mayr when he passed away in 2005, which gives some flavor of their personalities. Mayr: "You don't have to tell me what 'symbiosis' is! I studied symbiosis with Paul Buchner in Griefswald [in the 1920s]." Buchner later wrote one of the classic books on symbiosis, Endosymbiose der Tier mit pflanzlichen Mikroorganismen.)

She also showed a video of protists from termite guts, some of which have symbiotic bacteria living on their surface, which act more or less as surrogate flagella. One could tell that she was really captivated by the beauty of these organisms, and I heard later from someone that she often showed this video at her talks.

Margulis's 1967 paper is best known for its hypotheses about chloroplasts and mitochondria, which have been validated by lines of evidence, such as DNA sequencing, that were not available to her at the time. Her remaining hypothesis was that eukaryotic flagella evolved from symbiotic spirochaetes, which are corkscrew-shaped bacteria that swim helically. This idea hasn't done so well, and hasn't been supported by evidence in the way which the chloroplast and mitochondrial hypotheses have, but as her fascination with the video shows, she was still thinking about it. One of her last papers, published in 2010, was on the microscopical structure of one kind of these bacteria on a termite-gut protozoan.

On rereading her 1967 paper, a few things stood out to me. She managed to synthesize a tremendous amount of information (the paper is 49 pages long) from very different fields, including microbiology, palaeontology, geology, cytology, and evolution.

This was where she first put forward many of the concepts and themes which she would continue to think about and work on for long afterwards. For example, the scenario for eukaryote evolution that appears as a figure is re-presented in modified form in her popular book, Five Kingdoms.

The book, which she coauthored with Karlene Schwartz, was one of my favorite books as a student. The latest edition is from 1998, but it's still a good read, giving a brief overview of all the major phyla of living organisms in the classical five kingdoms: Prokaryotes, Protoctists (i.e. protists), Plants, Fungi, and Animals. It was my first introduction to the weird and wonderful world of protist and microbe diversity, which otherwise get such short shrift in introductory biology. It also shows how effective she was as an encyclopedic collator and system-builder.

In her thoroughness she also delved into the older literature. She had an interest in the history of biology, and what might be called her intellectual predecessors. She was involved in a recent project to translate a 1924 Russian book titled Symbiogenesis: A New Principle of Evolution by Boris Kozo-Polyansky. She did not shy from acknowledging these "forbears" and other early insights and ideas that were "before their time".

I think that she represented a very "classical" sort of biology, informed by visual thinking and reasoning by analogy. Looking at older books of zoology, botany, or cytology, one finds a similar frame of mind and emphasis on pattern-recognition. Modern biology is definitely still about pattern-recognition, but much of it is now impossible to "eyeball", such as searching for gene homology.

Unfortunately, reasoning by analogy can sometimes lead us down the wrong track, and an over-enthusiasm for it seems to have been responsible for a controversy that involved her in 2009. As a member of the National Academy of Science in the USA, she sponsored a paper for publication in its Proceedings, which hypothesized that "caterpillars evolved from onychophorans [velvet worms] by hybridogenesis" with insects. The paper never made it into print, but attracted a storm of protest and the imputation that she misused the submission process to push through a paper which would never have been published elsewhere.

That episode didn't help her reputation for "eccentricity", which is a word which seems to crop up in describing her, alongside "maverick" or "rebel". Nonetheless, her place in biology is secured, and I think it's important to acknowledge why. She gave us a whole new way of thinking about evolution, spurred scientific interest in endosymbiosis and early evolution, brought protists and other formerly obscure organisms to the attention of scientists and public, and defended the importance of symbiosis to the evolutionary process.

In doing so, Lynn Margulis gave us a glimpse into the biological world as it could have been at its origin, and also into the present, where we still make regular use of the concepts that she pioneered. RIP.