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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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Selected prokaryotic actin homologs aligned with eukaryotic actins and actin-related proteins 2 and 3. Green boxes 1 and 2 highlight the major inserts in Arp 2, 3 distinguishing them from actins [118]: a loop in subdomain 4 of Arp3 (green box 1) and elongated loops in subdomain 3 in both Arp 2 and Arp 3 (green box 2). ALP, actin-like protein. Red boxes indicate homologous inserts shared between crenarchaeal and eukaryotic proteins. For the complete legend, see Additional File 5.
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Figure 2: Selected prokaryotic actin homologs aligned with eukaryotic actins and actin-related proteins 2 and 3. Green boxes 1 and 2 highlight the major inserts in Arp 2, 3 distinguishing them from actins [118]: a loop in subdomain 4 of Arp3 (green box 1) and elongated loops in subdomain 3 in both Arp 2 and Arp 3 (green box 2). ALP, actin-like protein. Red boxes indicate homologous inserts shared between crenarchaeal and eukaryotic proteins. For the complete legend, see Additional File 5.

Mentions: We then examined in detail the multiple alignment of selected representatives of the main groups of actin-superfamily proteins in search of possible derived shared characters (synapomorphies) Notably, despite the relatively low overall sequence conservation, we identified two homologous (as indicated by the amino acid residue conservation in several alignment positions) inserts that are shared between the archaeal and eukaryotic actin-like proteins; an additional conserved region that is missing in the MreB-like proteins is located near the C-termini of these proteins (Figure 2). These inserts appear to qualify as derived shared characters strongly supporting the monophyly of the archaeal and eukaryotic actins and actin-like proteins that is suggested by the topology of the phylogenetic tree (Figure 1). In addition, both archaeal actins and Arp3 possess unique inserts that are missing in eukaryotic actins (Figure 2).


The origins of phagocytosis and eukaryogenesis.

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

Selected prokaryotic actin homologs aligned with eukaryotic actins and actin-related proteins 2 and 3. Green boxes 1 and 2 highlight the major inserts in Arp 2, 3 distinguishing them from actins [118]: a loop in subdomain 4 of Arp3 (green box 1) and elongated loops in subdomain 3 in both Arp 2 and Arp 3 (green box 2). ALP, actin-like protein. Red boxes indicate homologous inserts shared between crenarchaeal and eukaryotic proteins. 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 2: Selected prokaryotic actin homologs aligned with eukaryotic actins and actin-related proteins 2 and 3. Green boxes 1 and 2 highlight the major inserts in Arp 2, 3 distinguishing them from actins [118]: a loop in subdomain 4 of Arp3 (green box 1) and elongated loops in subdomain 3 in both Arp 2 and Arp 3 (green box 2). ALP, actin-like protein. Red boxes indicate homologous inserts shared between crenarchaeal and eukaryotic proteins. For the complete legend, see Additional File 5.
Mentions: We then examined in detail the multiple alignment of selected representatives of the main groups of actin-superfamily proteins in search of possible derived shared characters (synapomorphies) Notably, despite the relatively low overall sequence conservation, we identified two homologous (as indicated by the amino acid residue conservation in several alignment positions) inserts that are shared between the archaeal and eukaryotic actin-like proteins; an additional conserved region that is missing in the MreB-like proteins is located near the C-termini of these proteins (Figure 2). These inserts appear to qualify as derived shared characters strongly supporting the monophyly of the archaeal and eukaryotic actins and actin-like proteins that is suggested by the topology of the phylogenetic tree (Figure 1). In addition, both archaeal actins and Arp3 possess unique inserts that are missing in eukaryotic actins (Figure 2).

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