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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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The proposed endosymbiotic scenario of eukaryogenesis and subsequent origin of phagocytosis. The evolutionary tree of archaea is shown as a multifurcation of 5 major branches: Crenarchaeota, Euryarchaeota, Korarchaeota, Thaumarchaeota, and the hypothetical Archaeal Ancestor of Eukaryotes which is depicted as an irregular shape to emphasize the likely absence of a rigid cell wall. LECA, Last Universal Eukaryotic Ancestor. HGT, Horizontal Gene Transfer. The primary radiation of eukaryotes is shown as a multifurcation of 5 supergroups: Unikonts, Chromalveolata, Excavates, Rhizaria, and Planta. At least, three of the supergroups evolved full-fledged phagocytosis (Ph).
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Figure 4: The proposed endosymbiotic scenario of eukaryogenesis and subsequent origin of phagocytosis. The evolutionary tree of archaea is shown as a multifurcation of 5 major branches: Crenarchaeota, Euryarchaeota, Korarchaeota, Thaumarchaeota, and the hypothetical Archaeal Ancestor of Eukaryotes which is depicted as an irregular shape to emphasize the likely absence of a rigid cell wall. LECA, Last Universal Eukaryotic Ancestor. HGT, Horizontal Gene Transfer. The primary radiation of eukaryotes is shown as a multifurcation of 5 supergroups: Unikonts, Chromalveolata, Excavates, Rhizaria, and Planta. At least, three of the supergroups evolved full-fledged phagocytosis (Ph).

Mentions: Together, these findings lead to an admittedly speculative scenario for the origin and role of the phagocytic capacity in the general context of eukaryogenesis (Figure 4). Under this model, the organism that acquired the mitochondrial endosymbiont was an archaeon without a cell wall that morphologically might resemble the extant Thermoplasma and possessed an actin-like-protein based cytoskeleton in the form of filament networks. The branched-filament cytoskeleton allowed the hypothetical archaeal ancestor of eukaryotes to produce actin-supported membrane protrusions, resembling eukaryotic lamellipodia/filopodia, thus facilitating occasional engulfment of bacteria. One of such occasions would eventually lead to the mitochondrial endosymbiosis. Conceptually, this process can be regarded as the simplest, primordial form of phagocytosis. Indeed, it has been shown that some bacteria enter the host eukaryotic cell by inducing protrusions of the host plasma membrane [128]. This model, essentially, takes the middle ground between the "primitive phagocyte" and "fateful encounter" scenarios of endosymbiosis: it is proposed that the archaeal host had no full-fledged phagocytosis but did possess a primitive mechanism for the engulfment of other prokaryotic cells. Such an ability would substantially increase the frequency of engulfment and the likelihood that a stable enosymbiosis would be established. Thus, this model is generally compatible with the hypotheses which portray the protoeukaryote as a predator or scavenger that fed on other prokaryotes [18,104,129]; however, compared, say, to modern amoebas, this would be a rather ineffective predator. Clearly, this scenario is also compatible with the earlier "you are what you eat" idea of Doolittle according to which the protoeukaryote continuously acquired diverse genes from bacteria engulfed as food or transient endosymbionts [19].


The origins of phagocytosis and eukaryogenesis.

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

The proposed endosymbiotic scenario of eukaryogenesis and subsequent origin of phagocytosis. The evolutionary tree of archaea is shown as a multifurcation of 5 major branches: Crenarchaeota, Euryarchaeota, Korarchaeota, Thaumarchaeota, and the hypothetical Archaeal Ancestor of Eukaryotes which is depicted as an irregular shape to emphasize the likely absence of a rigid cell wall. LECA, Last Universal Eukaryotic Ancestor. HGT, Horizontal Gene Transfer. The primary radiation of eukaryotes is shown as a multifurcation of 5 supergroups: Unikonts, Chromalveolata, Excavates, Rhizaria, and Planta. At least, three of the supergroups evolved full-fledged phagocytosis (Ph).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: The proposed endosymbiotic scenario of eukaryogenesis and subsequent origin of phagocytosis. The evolutionary tree of archaea is shown as a multifurcation of 5 major branches: Crenarchaeota, Euryarchaeota, Korarchaeota, Thaumarchaeota, and the hypothetical Archaeal Ancestor of Eukaryotes which is depicted as an irregular shape to emphasize the likely absence of a rigid cell wall. LECA, Last Universal Eukaryotic Ancestor. HGT, Horizontal Gene Transfer. The primary radiation of eukaryotes is shown as a multifurcation of 5 supergroups: Unikonts, Chromalveolata, Excavates, Rhizaria, and Planta. At least, three of the supergroups evolved full-fledged phagocytosis (Ph).
Mentions: Together, these findings lead to an admittedly speculative scenario for the origin and role of the phagocytic capacity in the general context of eukaryogenesis (Figure 4). Under this model, the organism that acquired the mitochondrial endosymbiont was an archaeon without a cell wall that morphologically might resemble the extant Thermoplasma and possessed an actin-like-protein based cytoskeleton in the form of filament networks. The branched-filament cytoskeleton allowed the hypothetical archaeal ancestor of eukaryotes to produce actin-supported membrane protrusions, resembling eukaryotic lamellipodia/filopodia, thus facilitating occasional engulfment of bacteria. One of such occasions would eventually lead to the mitochondrial endosymbiosis. Conceptually, this process can be regarded as the simplest, primordial form of phagocytosis. Indeed, it has been shown that some bacteria enter the host eukaryotic cell by inducing protrusions of the host plasma membrane [128]. This model, essentially, takes the middle ground between the "primitive phagocyte" and "fateful encounter" scenarios of endosymbiosis: it is proposed that the archaeal host had no full-fledged phagocytosis but did possess a primitive mechanism for the engulfment of other prokaryotic cells. Such an ability would substantially increase the frequency of engulfment and the likelihood that a stable enosymbiosis would be established. Thus, this model is generally compatible with the hypotheses which portray the protoeukaryote as a predator or scavenger that fed on other prokaryotes [18,104,129]; however, compared, say, to modern amoebas, this would be a rather ineffective predator. Clearly, this scenario is also compatible with the earlier "you are what you eat" idea of Doolittle according to which the protoeukaryote continuously acquired diverse genes from bacteria engulfed as food or transient endosymbionts [19].

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