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The origins of phagocytosis and eukaryogenesis.

Yutin N, Wolf MY, Wolf YI, Koonin EV - Biol. Direct (2009)

Bottom Line: 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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA. yutin@ncbi.nlm.nih.gov

ABSTRACT

Background: 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.

Results: Comparisons 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.

Conclusion: The 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.

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A maximum likelihood tree of actin-related proteins. The root position was forced between the HSP70 superfamily and the actin superfamily. The tree was constructed by analysis of 295 aligned amino acid residues (Additional File 8). Support values are indicated only for major internal branches (not within smaller monophyletic groups). The protein sequences whose structure alignment was used to correct the multiple protein alignment of actin-related proteins are denoted in red. For the complete legend, see Additional File 5.
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Figure 1: A maximum likelihood tree of actin-related proteins. The root position was forced between the HSP70 superfamily and the actin superfamily. The tree was constructed by analysis of 295 aligned amino acid residues (Additional File 8). Support values are indicated only for major internal branches (not within smaller monophyletic groups). The protein sequences whose structure alignment was used to correct the multiple protein alignment of actin-related proteins are denoted in red. For the complete legend, see Additional File 5.

Mentions: In order to gain further insight into the relationships between eukaryotic actin protein family and their prokaryotic homologs, we reexamined the phylogeny of actins and actin-like proteins, with HSP70 family used as the outgroup. The HSP70 family is the group of proteins with the closest similarity to the actin family and thus an obvious choice for an outgroup to infer the root position in this tree although it remains uncertain whether HSP70 was present in the Last Universal Common Ancestor (LUCA) of modern cellular life or has a bacterial origin [116,117]. The resulting tree has bacterial proteins of the MreB family as the basal branch, followed by the MamK and ParM-StbA branches that also consist primarily of bacterial but also some archaeal (like the experimentally characterized Ta0583) proteins. The actin family proper that includes archaeal and eukaryotic actin-like proteins (and actins) is the sister group of the ParM-StbA group (Fig. 1). This topology seems to be best compatible with an ancient acquisition of the progenitor of the actin family by an archaeon via HGT from bacteria, perhaps, via a plasmid that encoded a ParM-StbA family protein. Regardless of exact evolutionary scenario and of which (if any) of these proteins were present in LUCA, the tree strongly supports the hypothesis that the crenarchaeal and korarchaeal actin-like proteins are the closest prokaryotic homologs of the eukaryotic actin family (Figure 1 and Additional file 5). By contrast, euryarchaeal actin-like proteins including the experimentally characterized Ta0583 clustered within the MreB and ParM branches, suggesting multiple horizontal gene transfers between bacteria and archaea. Within the eukaryotic branch of the tree, the Arp3 clade is the first to branch off the trunk, followed by the divergence of the actins and Arp2 (Figure 1).


The origins of phagocytosis and eukaryogenesis.

Yutin N, Wolf MY, Wolf YI, Koonin EV - Biol. Direct (2009)

A maximum likelihood tree of actin-related proteins. The root position was forced between the HSP70 superfamily and the actin superfamily. The tree was constructed by analysis of 295 aligned amino acid residues (Additional File 8). Support values are indicated only for major internal branches (not within smaller monophyletic groups). The protein sequences whose structure alignment was used to correct the multiple protein alignment of actin-related proteins are denoted in red. For the complete legend, see Additional File 5.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2651865&req=5

Figure 1: A maximum likelihood tree of actin-related proteins. The root position was forced between the HSP70 superfamily and the actin superfamily. The tree was constructed by analysis of 295 aligned amino acid residues (Additional File 8). Support values are indicated only for major internal branches (not within smaller monophyletic groups). The protein sequences whose structure alignment was used to correct the multiple protein alignment of actin-related proteins are denoted in red. For the complete legend, see Additional File 5.
Mentions: In order to gain further insight into the relationships between eukaryotic actin protein family and their prokaryotic homologs, we reexamined the phylogeny of actins and actin-like proteins, with HSP70 family used as the outgroup. The HSP70 family is the group of proteins with the closest similarity to the actin family and thus an obvious choice for an outgroup to infer the root position in this tree although it remains uncertain whether HSP70 was present in the Last Universal Common Ancestor (LUCA) of modern cellular life or has a bacterial origin [116,117]. The resulting tree has bacterial proteins of the MreB family as the basal branch, followed by the MamK and ParM-StbA branches that also consist primarily of bacterial but also some archaeal (like the experimentally characterized Ta0583) proteins. The actin family proper that includes archaeal and eukaryotic actin-like proteins (and actins) is the sister group of the ParM-StbA group (Fig. 1). This topology seems to be best compatible with an ancient acquisition of the progenitor of the actin family by an archaeon via HGT from bacteria, perhaps, via a plasmid that encoded a ParM-StbA family protein. Regardless of exact evolutionary scenario and of which (if any) of these proteins were present in LUCA, the tree strongly supports the hypothesis that the crenarchaeal and korarchaeal actin-like proteins are the closest prokaryotic homologs of the eukaryotic actin family (Figure 1 and Additional file 5). By contrast, euryarchaeal actin-like proteins including the experimentally characterized Ta0583 clustered within the MreB and ParM branches, suggesting multiple horizontal gene transfers between bacteria and archaea. Within the eukaryotic branch of the tree, the Arp3 clade is the first to branch off the trunk, followed by the divergence of the actins and Arp2 (Figure 1).

Bottom Line: 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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA. yutin@ncbi.nlm.nih.gov

ABSTRACT

Background: 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.

Results: Comparisons 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.

Conclusion: The 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.

Show MeSH
Related in: MedlinePlus