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Infection and the first eukaryotes

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Science  27 May 2016:
Vol. 352, Issue 6289, pp. 1065
DOI: 10.1126/science.aaf6478

In their Perspective “Pathogen to powerhouse” (12 February, p. 659), S. G. Ball et al. argue that the endosymbiotic events that led to the evolution of eukaryotes involved infection of an already complex host. They write that “the first challenges for an endosymbiont are to avoid being digested.…” There are, however, issues associated with such a concept.

In the case of plastid endosymbiosis, Ball et al. advocate involvement of chlamydial pathogens (the MAT hypothesis), but independent analyses have rejected this idea (1). In the case of mitochondrial endosymbiosis, Ball et al. suggest that a relative of the Rickettsia pathogen infected an archaeon, with one caveat being that all Rickettsia are obligate intracellular pathogens that depend on eukaryotic cells and their mitochondria for survival. Furthermore, Ball et al. assume that the interplay of the endosymbiotic partners was not symbiotic. Yet, such symbioses are common, Paulinella chromatophora and all secondary endosymbioses being two examples.

For mitochondrial endosymbiosis, the authors envision an archaeal host that could endocytose (i.e., incorporate large particles including bacteria). Lokiarchaea currently represent the closest relatives of such a host. However, pangenome data (2) show that Lokiarchaea lack critical endocytosis components, including those that mediate membrane curvature toward the cytosol and dynamins responsible for membrane scission; the latter are likely of mitochondrial origin (3). Endocytosis is selective and requires vesicle formation, an acidified lysosome, and a multivesicular body, which also matures through vesicles that mitochondria secrete (4). It is thus misleading to say “It is likely that endocytosis in Archaea originally evolved…,” particularly in the absence of endocytosing prokaryotes.

Ball et al. also suggest that autophagy evolved earlier than mitochondria to remove incidentally captured prokaryotes. Yet, the initiation of the phagophore depends on mitochondria-associated endoplasmic reticulum membranes (5). The endomembrane system appears to depend a lot on mitochondria, not vice versa. Most important, advocating a complex host that was infected by a Rickettsia relative fails to explain the universal presence of mitochondria in eukaryotes and offers no rationale for why mitochondria came about in the first place.

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