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Rooting the tree of life by transition analyses.

Cavalier-Smith T - Biol. Direct (2006)

Bottom Line: RNA polymerase and other insertions strongly favour the monophyly of Gracilicutes (Proteobacteria, Planctobacteria, Sphingobacteria, Spirochaetes).Evolution of the negibacterial outer membrane places the root within Eobacteria (Hadobacteria and Chlorobacteria, both primitively without lipopolysaccharide): as all phyla possessing the outer membrane beta-barrel protein Omp85 are highly probably derived, the root lies between them and Chlorobacteria, the only negibacteria without Omp85, or possibly within Chlorobacteria.The last ancestor of all life was a eubacterium with acyl-ester membrane lipids, large genome, murein peptidoglycan walls, and fully developed eubacterial molecular biology and cell division.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK. tom.cavalier-smith@zoo.ox.ac.uk

ABSTRACT

Background: Despite great advances in clarifying the family tree of life, it is still not agreed where its root is or what properties the most ancient cells possessed--the most difficult problems in phylogeny. Protein paralogue trees can theoretically place the root, but are contradictory because of tree-reconstruction artefacts or poor resolution; ribosome-related and DNA-handling enzymes suggested one between neomura (eukaryotes plus archaebacteria) and eubacteria, whereas metabolic enzymes often place it within eubacteria but in contradictory places. Palaeontology shows that eubacteria are much more ancient than eukaryotes, and, together with phylogenetic evidence that archaebacteria are sisters not ancestral to eukaryotes, implies that the root is not within the neomura. Transition analysis, involving comparative/developmental and selective arguments, can polarize major transitions and thereby systematically exclude the root from major clades possessing derived characters and thus locate it; previously the 20 shared neomuran characters were thus argued to be derived, but whether the root was within eubacteria or between them and archaebacteria remained controversial.

Results: I analyze 13 major transitions within eubacteria, showing how they can all be congruently polarized. I infer the first fully resolved prokaryote tree, with a basal stem comprising the new infrakingdom Glidobacteria (Chlorobacteria, Hadobacteria, Cyanobacteria), which is entirely non-flagellate and probably ancestrally had gliding motility, and two derived branches (Gracilicutes and Unibacteria/Eurybacteria) that diverged immediately following the origin of flagella. Proteasome evolution shows that the universal root is outside a clade comprising neomura and Actinomycetales (proteates), and thus lies within other eubacteria, contrary to a widespread assumption that it is between eubacteria and neomura. Cell wall and flagellar evolution independently locate the root outside Posibacteria (Actinobacteria and Endobacteria), and thus among negibacteria with two membranes. Posibacteria are derived from Eurybacteria and ancestral to neomura. RNA polymerase and other insertions strongly favour the monophyly of Gracilicutes (Proteobacteria, Planctobacteria, Sphingobacteria, Spirochaetes). Evolution of the negibacterial outer membrane places the root within Eobacteria (Hadobacteria and Chlorobacteria, both primitively without lipopolysaccharide): as all phyla possessing the outer membrane beta-barrel protein Omp85 are highly probably derived, the root lies between them and Chlorobacteria, the only negibacteria without Omp85, or possibly within Chlorobacteria.

Conclusion: Chlorobacteria are probably the oldest and Archaebacteria the youngest bacteria, with Posibacteria of intermediate age, requiring radical reassessment of dominant views of bacterial evolution. The last ancestor of all life was a eubacterium with acyl-ester membrane lipids, large genome, murein peptidoglycan walls, and fully developed eubacterial molecular biology and cell division. It was a non-flagellate negibacterium with two membranes, probably a photosynthetic green non-sulphur bacterium with relatively primitive secretory machinery, not a heterotrophic posibacterium with one membrane.

No MeSH data available.


Related in: MedlinePlus

Hypothetical phylogeny for photosynthetic reaction centres. Prior to the last common ancestor of all extant life the primitive reaction centre, a homodimer with two bound quinones, each donating electrons to a primitive cytochrome cc complex, evolved into the heterodimeric type found in green non-sulphur bacteria (Chlorobacteria). This was duplicated prior to divergence of cyanobacteria and gracilicutes to generate a modified homodimeric type of cytochrome bc1 complex with iron-sulphur clusters (FF); for a mechanistic explanation of this duplication see [126]. Cyanobacteria converted the two versions into photosystems I and II. Proteobacteria replaced chlorosomes in the original heterodimeric type by an H subunit with purple carotenoid, but did not retain the new duplicate with FeS clusters. By contrast, this was the only version retained by green sulphur bacteria (Sphingobacteria) and Heliobacteria, both losing the earlier heterodimeric type. This scenario is simplified from ref. 1 and congruent with the cladistic tree in Fig. 7 and the concatenated rRNA tree [80] and is compatible with photosynthetic protein trees, if properly rooted (see text).
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Figure 9: Hypothetical phylogeny for photosynthetic reaction centres. Prior to the last common ancestor of all extant life the primitive reaction centre, a homodimer with two bound quinones, each donating electrons to a primitive cytochrome cc complex, evolved into the heterodimeric type found in green non-sulphur bacteria (Chlorobacteria). This was duplicated prior to divergence of cyanobacteria and gracilicutes to generate a modified homodimeric type of cytochrome bc1 complex with iron-sulphur clusters (FF); for a mechanistic explanation of this duplication see [126]. Cyanobacteria converted the two versions into photosystems I and II. Proteobacteria replaced chlorosomes in the original heterodimeric type by an H subunit with purple carotenoid, but did not retain the new duplicate with FeS clusters. By contrast, this was the only version retained by green sulphur bacteria (Sphingobacteria) and Heliobacteria, both losing the earlier heterodimeric type. This scenario is simplified from ref. 1 and congruent with the cladistic tree in Fig. 7 and the concatenated rRNA tree [80] and is compatible with photosynthetic protein trees, if properly rooted (see text).

Mentions: It is generally accepted that photosystem I and photosystem II, which carries the oxygenic reaction centre, arose by duplication and divergence from a common ancestor that had only a single photosystem. Just when in the tree did this duplication occur? Clues come from the fact that the two partly photosynthetic gracilicute phyla (Proteobacteria, Sphingobacteria) have very different photosystems. As Fig. 9 indicates, that of green sulphur bacteria such as Chlorobium resembles photosystem I of cyanobacteria, whereas that of purple bacteria is more like photosystem II of cyanobacteria. Given the root of the tree in or beside Chlorobacteria, it is entirely unnecessary to postulate lateral gene transfer of complete photosystems as is sometimes unparsimoniously done. Vertical inheritance alone can very simply explain the known diversity of photosystems and their distribution among phyla given the root and topology of the eubacterial tree as now deduced by cladistic and transition analysis (Figs 3 and 7).


Rooting the tree of life by transition analyses.

Cavalier-Smith T - Biol. Direct (2006)

Hypothetical phylogeny for photosynthetic reaction centres. Prior to the last common ancestor of all extant life the primitive reaction centre, a homodimer with two bound quinones, each donating electrons to a primitive cytochrome cc complex, evolved into the heterodimeric type found in green non-sulphur bacteria (Chlorobacteria). This was duplicated prior to divergence of cyanobacteria and gracilicutes to generate a modified homodimeric type of cytochrome bc1 complex with iron-sulphur clusters (FF); for a mechanistic explanation of this duplication see [126]. Cyanobacteria converted the two versions into photosystems I and II. Proteobacteria replaced chlorosomes in the original heterodimeric type by an H subunit with purple carotenoid, but did not retain the new duplicate with FeS clusters. By contrast, this was the only version retained by green sulphur bacteria (Sphingobacteria) and Heliobacteria, both losing the earlier heterodimeric type. This scenario is simplified from ref. 1 and congruent with the cladistic tree in Fig. 7 and the concatenated rRNA tree [80] and is compatible with photosynthetic protein trees, if properly rooted (see text).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1586193&req=5

Figure 9: Hypothetical phylogeny for photosynthetic reaction centres. Prior to the last common ancestor of all extant life the primitive reaction centre, a homodimer with two bound quinones, each donating electrons to a primitive cytochrome cc complex, evolved into the heterodimeric type found in green non-sulphur bacteria (Chlorobacteria). This was duplicated prior to divergence of cyanobacteria and gracilicutes to generate a modified homodimeric type of cytochrome bc1 complex with iron-sulphur clusters (FF); for a mechanistic explanation of this duplication see [126]. Cyanobacteria converted the two versions into photosystems I and II. Proteobacteria replaced chlorosomes in the original heterodimeric type by an H subunit with purple carotenoid, but did not retain the new duplicate with FeS clusters. By contrast, this was the only version retained by green sulphur bacteria (Sphingobacteria) and Heliobacteria, both losing the earlier heterodimeric type. This scenario is simplified from ref. 1 and congruent with the cladistic tree in Fig. 7 and the concatenated rRNA tree [80] and is compatible with photosynthetic protein trees, if properly rooted (see text).
Mentions: It is generally accepted that photosystem I and photosystem II, which carries the oxygenic reaction centre, arose by duplication and divergence from a common ancestor that had only a single photosystem. Just when in the tree did this duplication occur? Clues come from the fact that the two partly photosynthetic gracilicute phyla (Proteobacteria, Sphingobacteria) have very different photosystems. As Fig. 9 indicates, that of green sulphur bacteria such as Chlorobium resembles photosystem I of cyanobacteria, whereas that of purple bacteria is more like photosystem II of cyanobacteria. Given the root of the tree in or beside Chlorobacteria, it is entirely unnecessary to postulate lateral gene transfer of complete photosystems as is sometimes unparsimoniously done. Vertical inheritance alone can very simply explain the known diversity of photosystems and their distribution among phyla given the root and topology of the eubacterial tree as now deduced by cladistic and transition analysis (Figs 3 and 7).

Bottom Line: RNA polymerase and other insertions strongly favour the monophyly of Gracilicutes (Proteobacteria, Planctobacteria, Sphingobacteria, Spirochaetes).Evolution of the negibacterial outer membrane places the root within Eobacteria (Hadobacteria and Chlorobacteria, both primitively without lipopolysaccharide): as all phyla possessing the outer membrane beta-barrel protein Omp85 are highly probably derived, the root lies between them and Chlorobacteria, the only negibacteria without Omp85, or possibly within Chlorobacteria.The last ancestor of all life was a eubacterium with acyl-ester membrane lipids, large genome, murein peptidoglycan walls, and fully developed eubacterial molecular biology and cell division.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK. tom.cavalier-smith@zoo.ox.ac.uk

ABSTRACT

Background: Despite great advances in clarifying the family tree of life, it is still not agreed where its root is or what properties the most ancient cells possessed--the most difficult problems in phylogeny. Protein paralogue trees can theoretically place the root, but are contradictory because of tree-reconstruction artefacts or poor resolution; ribosome-related and DNA-handling enzymes suggested one between neomura (eukaryotes plus archaebacteria) and eubacteria, whereas metabolic enzymes often place it within eubacteria but in contradictory places. Palaeontology shows that eubacteria are much more ancient than eukaryotes, and, together with phylogenetic evidence that archaebacteria are sisters not ancestral to eukaryotes, implies that the root is not within the neomura. Transition analysis, involving comparative/developmental and selective arguments, can polarize major transitions and thereby systematically exclude the root from major clades possessing derived characters and thus locate it; previously the 20 shared neomuran characters were thus argued to be derived, but whether the root was within eubacteria or between them and archaebacteria remained controversial.

Results: I analyze 13 major transitions within eubacteria, showing how they can all be congruently polarized. I infer the first fully resolved prokaryote tree, with a basal stem comprising the new infrakingdom Glidobacteria (Chlorobacteria, Hadobacteria, Cyanobacteria), which is entirely non-flagellate and probably ancestrally had gliding motility, and two derived branches (Gracilicutes and Unibacteria/Eurybacteria) that diverged immediately following the origin of flagella. Proteasome evolution shows that the universal root is outside a clade comprising neomura and Actinomycetales (proteates), and thus lies within other eubacteria, contrary to a widespread assumption that it is between eubacteria and neomura. Cell wall and flagellar evolution independently locate the root outside Posibacteria (Actinobacteria and Endobacteria), and thus among negibacteria with two membranes. Posibacteria are derived from Eurybacteria and ancestral to neomura. RNA polymerase and other insertions strongly favour the monophyly of Gracilicutes (Proteobacteria, Planctobacteria, Sphingobacteria, Spirochaetes). Evolution of the negibacterial outer membrane places the root within Eobacteria (Hadobacteria and Chlorobacteria, both primitively without lipopolysaccharide): as all phyla possessing the outer membrane beta-barrel protein Omp85 are highly probably derived, the root lies between them and Chlorobacteria, the only negibacteria without Omp85, or possibly within Chlorobacteria.

Conclusion: Chlorobacteria are probably the oldest and Archaebacteria the youngest bacteria, with Posibacteria of intermediate age, requiring radical reassessment of dominant views of bacterial evolution. The last ancestor of all life was a eubacterium with acyl-ester membrane lipids, large genome, murein peptidoglycan walls, and fully developed eubacterial molecular biology and cell division. It was a non-flagellate negibacterium with two membranes, probably a photosynthetic green non-sulphur bacterium with relatively primitive secretory machinery, not a heterotrophic posibacterium with one membrane.

No MeSH data available.


Related in: MedlinePlus