Abstract
BackgroundPhagocytosis, that is, engulfment of large particles by eukaryotic cells, is found in diverse organisms and is often thought to be central to the very origin of the eukaryotic cell, in particular, for the acquisition of bacterial endosymbionts including the ancestor of the mitochondrion.ResultsComparisons of the sets of proteins implicated in phagocytosis in different eukaryotes reveal extreme diversity, with very few highly conserved components that typically do not possess readily identifiable prokaryotic homologs. Nevertheless, phylogenetic analysis of those proteins for which such homologs do exist yields clues to the possible origin of phagocytosis. The central finding is that a subset of archaea encode actins that are not only monophyletic with eukaryotic actins but also share unique structural features with actin-related proteins (Arp) 2 and 3. All phagocytic processes are strictly dependent on remodeling of the actin cytoskeleton and the formation of branched filaments for which Arp2/3 are responsible. The presence of common structural features in Arp2/3 and the archaeal actins suggests that the common ancestors of the archaeal and eukaryotic actins were capable of forming branched filaments, like modern Arp2/3. The Rho family GTPases that are ubiquitous regulators of phagocytosis in eukaryotes appear to be of bacterial origin, so assuming that the host of the mitochondrial endosymbiont was an archaeon, the genes for these GTPases come via horizontal gene transfer from the endosymbiont or in an earlier event.ConclusionThe present findings suggest a hypothetical scenario of eukaryogenesis under which the archaeal ancestor of eukaryotes had no cell wall (like modern Thermoplasma) but had an actin-based cytoskeleton including branched actin filaments that allowed this organism to produce actin-supported membrane protrusions. These protrusions would facilitate accidental, occasional engulfment of bacteria, one of which eventually became the mitochondrion. The acquisition of the endosymbiont triggered eukaryogenesis, in particular, the emergence of the endomembrane system that eventually led to the evolution of modern-type phagocytosis, independently in several eukaryotic lineages.ReviewersThis article was reviewed by Simonetta Gribaldo, Gaspar Jekely, and Pierre Pontarotti. For the full reviews, please go to the Reviewers' Reports section.
Highlights
Phagocytosis, that is, engulfment of large particles by eukaryotic cells, is found in diverse organisms and is often thought to be central to the very origin of the eukaryotic cell, in particular, for the acquisition of bacterial endosymbionts including the ancestor of the mitochondrion
The core set of proteins involved in phagocytosis identified by comparison of the proteomics results To delineate the complement of the evolutionarily conserved protein components of the phagosome, we compared the sets of proteins identified in proteomic studies of phagosomes isolated from mouse macrophages [53,54], Drosophila S2 cells [55], Dictyostelium discoideum [56], Entamoeba histolytica [57,58], and Tetrahymena thermophila [59]
Actin-related protein 3 (Arp3) was identified only in 3 of the 5 species, and actin-related protein 2 (Arp2) was detected in only one species
Summary
Phagocytosis, that is, engulfment of large particles by eukaryotic cells, is found in diverse organisms and is often thought to be central to the very origin of the eukaryotic cell, in particular, for the acquisition of bacterial endosymbionts including the ancestor of the mitochondrion. It is universally accepted that mitochondria and related organelles, that so far have been discovered in all eukaryotes studied in sufficient detail, have evolved via endosymbiosis, most likely, a single endosymbiotic event that involved an alpha-proteobacterium, the apparent ancestor of the mitochondria [1,2,3,4]. The major difficulty faced by the archezoan hypothesis is that so far all candidate archezoa, such as Diplomonada, Parabasalia, and Microsporidia, have been shown to possess organelles derived from or, at least, related to mitochondria (hydrogenosomes, mitosomes, and others) as well as some nuclear genes of apparent mitochondrial (alpha-proteobacterial) origin [1,6]. The proponents of the archezoan hypothesis are forced to postulate that the archezoa represent an extinct lineage of primitive eukaryotes [8]
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