Lynn Margulis: Symbiogenesis and the origin of the nucleus and undulipodia

At Leiden University, in the Institute I work at, there are several research groups devoted to symbiotic or parasitic relationships. On September the 6 a symposium was held: "Acquired Genomes: Evolutionary consequences of endosymbionts", taking advantage of the presence of Lynn Margulis in the city as a guest speaker for the Faculty of Science official opening of the academic year. The talks of that meeting were mainly about Wolbachia. Although the topic is most interesting, today I would like to focus on the talk given by the main speaker:

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Evolutionary Consequences of Endosymbiosis: Origin of the nucleus
Lynn Margulis
University of Massachusetts/Amherst, USA

No substitute exists for direct study of microbes in nature. Some serve as modern analogues of the origins of cells as integrated communities of bacteria and protoctists in anoxic environments. We base our model of the origin of the nucleus on current observations of relevant live organisms. We arrange our observations into a plausible evolutionary sequence that led from prokaryotes to the origin of the first nucleated cell. The nucleus is postulated to evolve after the archaebacterium and eubacterium merged to form the symbiotic ancestor of amitochondriates (archaeprotists) protists. Descendants of these swimming archaeprotists today thrive in organic-rich anoxic habitats where they are amenable to study. Eukaryosis, the origin of nucleated cells, occurred by the middle Proterozoic Eon prior to the deposition in sediments of certain well-preserved microfossils i.e., Vandalsphaeridium (Vidal, 1998) and spiny spheres in the Doushantou cherts of China (Knoll, 2003).

Our evolutionary scenario for nucleus origin in archaeprotist ancestors is based on observations by L.R. Cleveland (1892-1971) and Harold Kirby, Jr. (1900-1952). Intrinsic to our model is Cleveland's detailed work on cell motility, i.e., movements of undulipodia, the mitotic spindle and‚ “attraction spheres” (centriole-like organelles) in mitosis as well as on Kirby's concept of "mastigont multiplicity" (Kirby, 1994). Prokaryotic symbionts (Thermoplasm-like archaebacteria + motile eubacteria) began as components of the karyomastigont from which the nucleus was released. We posit that the acquisition and genomic integration of microbial symbionts extends far beyond the origin of the nucleus. Indeed it seems to be the major mode of evolutionary innovations and speciation in eukaryotes. Accumulation of random mutations plays a modulating rather than creative role in the origins of species. Two short videos illustrating these points will be shown.

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To tell the truth, the talk was quite amusing, especially the videos shown about "dancing" spirochetes. However, few news were presented to those who were already familiar with her work, in particular her last book "Acquiring Genomes". Among the new things, I must mention that she openly admits that there is no evidence of nucleic acids associated with centrioles or any other MTOC (microtubule organizing centre). Alas, this doesn't stop her insisting on her idea about a spirochete-archaean symbiosis as the source of the very first proto-eukaryotic cell.

Why does she push still this idea forward, then? Besides her well-known stubbornness, because an electron-micrograph of a spirochete (she didn't mention which species, as far as I remember) shows a quite clear resemblance with an undulipodium (eukaryotic cilia and flagella) since two pairs of "microtubules" could be observed (I shan't call them microtubules until I see the anti-tubulin staining); let's remember that undulipodia (almost) always have a 9+2 symmetry formula (nine pairs surrounding a central pair).

Another reason favouring the endosymbiotic scenario for the origin of the motile elements is of biochemical character. The metabolism of the archaea supported by Margulis as closest relative to the one that gave rise to eukaryotic cytoplasm, Thermoplasma, is sulphur-reducing: it can convert the sulphur abundant in its habitat into sulphide. Spirochetes can in turn oxidise the sulphide into sulphur again. This is a good reason to establish a symbiotic relationship (a similar hypothesis has been proposed for explaining the symbiotic origin of mitochondria; it's called the hydrogen theory), and more importantly, it appears that there is evidence for a sulphur metabolic cycle. Unfortunately, Margulis didn't give any reference for that besides a personal communication of someone (I don't remember the name) that has developed a "sulphurometer" in order to measure sulphur metabolites inside erythrocytes, having found proof of such a "futile" metabolic cycle.

Personally, I wouldn't mind recognizing an endosymbiotic origin for undulipodia. It's a reasonably well-argued hypothesis and some circumstantial evidences are on its side. Since all eukaryotes have microtubule cytoskeleton – what allows them to have an enormous versatility of form and movement – it is one of the most crucial acquisitions of protoeukaryotic history. The problem is that Margulis is convinced that this supposed symbiosis came prior to the mitochondrial one, and that as a result the most distinctive eukaryotic feature evolved. She is not the only one arguing that the nucleus is a secondary result of the first eukaryotic symbiogenesis. The authors behind the hydrogen theory also speculate about this in their model.

In a meeting held in France ("The Origin of the Nucleus", Les Treilles, 7-13 July 2004; editorial comment in Science) several models were debated, but the one that convinces me most is the syntrophic model: metabolic symbiosisàsymbiogenesisànucleated protoeukaryote. This scenario stands both for the hydrogen theory (mitochondria first) and Margulis' theory (spirochete-undulipodia first).

What arose first (assuming that the spirochete story is true), the flagellum or the mitochondrion? That's a good question. All eukaryotes have microtubule cytoskeleton, but not all eukaryotes have mitochondria. Eureka! Lynn would say. But not. Because the fact is that the absence of mitochondria is a derived character, no matter how much she resists to it – she continues to say that the most primitive extant eukaryotes are mitochondria-less anaerobic protist. If there was once an amitochondriate protoeukaryote, it has not left amitochondriate descendants. Facts rule, so for the time being, I support mitochondrion as first endosymbiont and nucleus origin as a result of that symbiogenesis. If the hypothesis of the undulipodia is ever proved, I'll begin to ask myself about what happened first.

I've used several times the word 'symbiogenesis'. In her book "Acquiring Genomes", Lynn and her son Dorion Sagan, basically propose that symbiogenesis – evolutionary consequence of symbiosis – is the main cause for the origin of new species, insisting on the old argument about "simple accumulation of random mutations can't generate new species". Furthermore, it is proposed a new definition of 'species' that takes that into account: different species have different genome compositions. Unfortunately, they easily fall into circular argumentation because as soon as they postulate their new definition, they use it to demonstrate that new species can only originate by genome-wide changes, being the fusion of two (or more) genomes the main mechanism for new species origin.

It's a pity that her extremely relevant discoveries on early eukaryotic evolution be tarnished for her confusion over "orthodox science". During the talk she mentioned several times that her financial support had been removed because of her search of heterodox ideas, blaming the "neodarwinist establishment" for that. After her talk I had the opportunity to ask her how does symbiogenesis exactly take place. To me it was obvious that the answer is by Natural Selection, but she answered in a most Lamarckian way: the initial symbiosis is a behavioural one, it is then strengthened by metabolic bonds, then a physical permanent interaction takes place and finally the genetic materials are fused. No matter how hard I tried, I couldn't make her to acknowledge that the only way that sequence can evolve is by the accumulation of selected random mutations.

In any case, she is a lovely person and she had the friendly detail of kindly dedicate me her book (another more for my collection! :-)

A webpage about Margulis' theory for the origin of undulipodia (in Spanish).
Discussion about the issue at Evolucionarios (also in Spanish).

Article about hydrogen hypothesis for the origin of mitochondria: W. Martin and M. Müller, Nature 392, 37 - 41 (05 March 1998);
editorial comment in Nature: W. Ford Doolittle, Nature 392, 15 - 16 (05 March 1998);
editorial comment in Science: G. Vogel, Science, 279, 1633-1634 (13 March 1998).

Article about another syntrophic hypothesis: D. Moreira and P. López-García, J Mol Evol 47, 517-530 (November 1998).

I hope to have time to look for more references on eukaryotic nucleus origin.