Prokaryotic symbiotic consortia and the origin of nucleated cells: A critical review of Lynn Margulis hypothesis

Abstract

The publication in the late 1960s of Lynn Margulis endosymbiotic proposal is a scientific milestone that brought to the fore of evolutionary discussions the issue of the origin of nucleated cells. Although it is true that the times were ripe, the timely publication of Lynn Margulis' original paper was the product of an intellectually bold 29-years old scientist, who based on the critical analysis of the available scientific information produced an all-encompassing, sophisticated narrative scheme on the origin of eukaryotic cells as a result of the evolution of prokaryotic consortia and, in bold intellectual stroke, put it all in the context of planetary evolution. A critical historical reassessment of her original proposal demonstrates that her hypothesis was not a simple archival outline of past schemes, but a renewed historical narrative of prokaryotic evolution and the role of endosymbiosis in the origin of eukaryotes. Although it is now accepted that the closest bacterial relatives of mitochondria and plastids are α-proteobacteria and cyanobacteria, respectively, comparative genomics demonstrates the mosaic character of the organelle genomes. The available evidence has completely refuted Margulis’ proposal of an exogenous origin for eukaryotic flagella, the (9 + 2) basal bodies, and centromeres, but we discuss in detail the reasons that led her to devote considerable efforts to argue for a symbiotic origin of the eukaryotic motility. An analysis of the arguments successfully employed by Margulis in her persuasive advocacy of endosymbiosis, combined with the discussions of her flaws and the scientific atmosphere during the period in which she formulated her proposals, are critical for a proper appraisal of the historical conditions that shaped her theory and its acceptance.