Limits...
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

Contrasting cell envelope structure in posibacteria and negibacteria. OM phospholipids, and when present possibly also lipopolysaccharides (LPS), may pass from their site of synthesis in the cytoplasmic membrane to the OM at the Bayer's patch contact sites, but this is not proven and only one protein (Imp) needed for LPS export is yet known. During its biosynthesis murein is secreted across the cytoplasmic membrane by isoprenol carriers. Lipoprotein (LP) is cotranslationally synthesised in both groups. Conversion of a negibacterial wall to a posibacterial wall as shown would be very much simpler than the reverse, requiring only a mutation causing sudden murein hypertrophy that could have broken the OM away from the Bayer's patches, preventing further lipid transfer and OM regrowth, plus the origin of sortases with a novel recognition system for covalently attaching murein lipoproteins (MLP) to the wall. As the negibacteria most closely related to Posibacteria (Eurybacteria) are glycobacteria with much more complex OM, secretion, and import mechanisms than Chlorobacteria (which lack lipopolysaccharide, most porins, Omp85, type I, II, and III secretion machinery, and probably the LolDE lipoprotein release mechanism, of more advanced bacteria), evolution in the reverse direction of such a complex OM in one step from a posibacteria would be practically impossible (see text) and immensely more difficult than the stepwise increase in its complexity possible with a chlorobacterial root of the tree. As the transitional stage between negibacteria and posibacteria had flagella, adding an outer membrane to a posibacterium and evolving a lipid export mechanism in one step would be even more complicated and improbable, as flagellar biogenesis would have had to be conserved and modified at the same time (see Fig. 8). No satisfactory mechanistic explanation has ever been given of how it could possibly have occurred.
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Figure 6: Contrasting cell envelope structure in posibacteria and negibacteria. OM phospholipids, and when present possibly also lipopolysaccharides (LPS), may pass from their site of synthesis in the cytoplasmic membrane to the OM at the Bayer's patch contact sites, but this is not proven and only one protein (Imp) needed for LPS export is yet known. During its biosynthesis murein is secreted across the cytoplasmic membrane by isoprenol carriers. Lipoprotein (LP) is cotranslationally synthesised in both groups. Conversion of a negibacterial wall to a posibacterial wall as shown would be very much simpler than the reverse, requiring only a mutation causing sudden murein hypertrophy that could have broken the OM away from the Bayer's patches, preventing further lipid transfer and OM regrowth, plus the origin of sortases with a novel recognition system for covalently attaching murein lipoproteins (MLP) to the wall. As the negibacteria most closely related to Posibacteria (Eurybacteria) are glycobacteria with much more complex OM, secretion, and import mechanisms than Chlorobacteria (which lack lipopolysaccharide, most porins, Omp85, type I, II, and III secretion machinery, and probably the LolDE lipoprotein release mechanism, of more advanced bacteria), evolution in the reverse direction of such a complex OM in one step from a posibacteria would be practically impossible (see text) and immensely more difficult than the stepwise increase in its complexity possible with a chlorobacterial root of the tree. As the transitional stage between negibacteria and posibacteria had flagella, adding an outer membrane to a posibacterium and evolving a lipid export mechanism in one step would be even more complicated and improbable, as flagellar biogenesis would have had to be conserved and modified at the same time (see Fig. 8). No satisfactory mechanistic explanation has ever been given of how it could possibly have occurred.

Mentions: Fig. 6 contrasts cell envelope structure in posibacteria and negibacteria. In Posibacteria, except for the almost entirely parasitic Mollicutes (mycoplasmas and spiroplasmas, which lost murein walls) the murein peptidoglycan layers are very thick and are attached to the cytoplasmic membrane by covalently attached lipoproteins with their lipid tails embedded in the outer leaflet of the phospholipid bilayer. In negibacteria the murein is usually much thinner and attached instead to the outer membrane (OM) by covalently attached murein lipoproteins with their lipid tails embedded in the inner phospholipid leaflet of the OM lipid bilayer; unlike in mycoplasmas, lipoproteins are retained in negibacteria even when murein is lost (most Planctobacteria). In Chlorobacteria and Hadobacteria the outer leaflet of the OM bilayer is also simple phospholipid, but in all six other phyla it is lipopolysaccharide (within Spirochaetes a greatly modified version is present in Leptospira [58], whereas the obligately parasitic spirochaetes have totally lost it; a few proteobacteria have simplified it to lipooligosaccharide). Unlike the cytoplasmic membrane, the OM is pierced by hollow cylindrical β-barrel porin proteins that allow small molecules to diffuse freely across it [59]. At intervals the OM is in direct and strong adhesive contact with the inner membrane at points known as Bayer's patches where there is a hole in the thin murein wall. As OM proteins and lipids are all synthesized by enzymes associated with the inner, cytoplasmic membrane, they have to be transported to the OM secondarily, through the periplasm for proteins [59] and probably via the Bayer's patches for lipids. Posibacteria entirely lack both the OM and this transport machinery. The OM and Bayer's patch structure can have evolved only once in prokaryote history as its structural and biogenetic complexity is so great. Transition analysis asks would it have been easier for a negibacterium to have lost the OM (evolution from bottom to top in Fig. 6) and make its wall thicker or for a posibacterium simultaneously to add an OM to a cell without them and simultaneously make the wall thinner and invent machinery for export of both lipids and proteins to it and to make the proteins that would make this complex system function (evolution from top to bottom in Fig. 6)?


Rooting the tree of life by transition analyses.

Cavalier-Smith T - Biol. Direct (2006)

Contrasting cell envelope structure in posibacteria and negibacteria. OM phospholipids, and when present possibly also lipopolysaccharides (LPS), may pass from their site of synthesis in the cytoplasmic membrane to the OM at the Bayer's patch contact sites, but this is not proven and only one protein (Imp) needed for LPS export is yet known. During its biosynthesis murein is secreted across the cytoplasmic membrane by isoprenol carriers. Lipoprotein (LP) is cotranslationally synthesised in both groups. Conversion of a negibacterial wall to a posibacterial wall as shown would be very much simpler than the reverse, requiring only a mutation causing sudden murein hypertrophy that could have broken the OM away from the Bayer's patches, preventing further lipid transfer and OM regrowth, plus the origin of sortases with a novel recognition system for covalently attaching murein lipoproteins (MLP) to the wall. As the negibacteria most closely related to Posibacteria (Eurybacteria) are glycobacteria with much more complex OM, secretion, and import mechanisms than Chlorobacteria (which lack lipopolysaccharide, most porins, Omp85, type I, II, and III secretion machinery, and probably the LolDE lipoprotein release mechanism, of more advanced bacteria), evolution in the reverse direction of such a complex OM in one step from a posibacteria would be practically impossible (see text) and immensely more difficult than the stepwise increase in its complexity possible with a chlorobacterial root of the tree. As the transitional stage between negibacteria and posibacteria had flagella, adding an outer membrane to a posibacterium and evolving a lipid export mechanism in one step would be even more complicated and improbable, as flagellar biogenesis would have had to be conserved and modified at the same time (see Fig. 8). No satisfactory mechanistic explanation has ever been given of how it could possibly have occurred.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Contrasting cell envelope structure in posibacteria and negibacteria. OM phospholipids, and when present possibly also lipopolysaccharides (LPS), may pass from their site of synthesis in the cytoplasmic membrane to the OM at the Bayer's patch contact sites, but this is not proven and only one protein (Imp) needed for LPS export is yet known. During its biosynthesis murein is secreted across the cytoplasmic membrane by isoprenol carriers. Lipoprotein (LP) is cotranslationally synthesised in both groups. Conversion of a negibacterial wall to a posibacterial wall as shown would be very much simpler than the reverse, requiring only a mutation causing sudden murein hypertrophy that could have broken the OM away from the Bayer's patches, preventing further lipid transfer and OM regrowth, plus the origin of sortases with a novel recognition system for covalently attaching murein lipoproteins (MLP) to the wall. As the negibacteria most closely related to Posibacteria (Eurybacteria) are glycobacteria with much more complex OM, secretion, and import mechanisms than Chlorobacteria (which lack lipopolysaccharide, most porins, Omp85, type I, II, and III secretion machinery, and probably the LolDE lipoprotein release mechanism, of more advanced bacteria), evolution in the reverse direction of such a complex OM in one step from a posibacteria would be practically impossible (see text) and immensely more difficult than the stepwise increase in its complexity possible with a chlorobacterial root of the tree. As the transitional stage between negibacteria and posibacteria had flagella, adding an outer membrane to a posibacterium and evolving a lipid export mechanism in one step would be even more complicated and improbable, as flagellar biogenesis would have had to be conserved and modified at the same time (see Fig. 8). No satisfactory mechanistic explanation has ever been given of how it could possibly have occurred.
Mentions: Fig. 6 contrasts cell envelope structure in posibacteria and negibacteria. In Posibacteria, except for the almost entirely parasitic Mollicutes (mycoplasmas and spiroplasmas, which lost murein walls) the murein peptidoglycan layers are very thick and are attached to the cytoplasmic membrane by covalently attached lipoproteins with their lipid tails embedded in the outer leaflet of the phospholipid bilayer. In negibacteria the murein is usually much thinner and attached instead to the outer membrane (OM) by covalently attached murein lipoproteins with their lipid tails embedded in the inner phospholipid leaflet of the OM lipid bilayer; unlike in mycoplasmas, lipoproteins are retained in negibacteria even when murein is lost (most Planctobacteria). In Chlorobacteria and Hadobacteria the outer leaflet of the OM bilayer is also simple phospholipid, but in all six other phyla it is lipopolysaccharide (within Spirochaetes a greatly modified version is present in Leptospira [58], whereas the obligately parasitic spirochaetes have totally lost it; a few proteobacteria have simplified it to lipooligosaccharide). Unlike the cytoplasmic membrane, the OM is pierced by hollow cylindrical β-barrel porin proteins that allow small molecules to diffuse freely across it [59]. At intervals the OM is in direct and strong adhesive contact with the inner membrane at points known as Bayer's patches where there is a hole in the thin murein wall. As OM proteins and lipids are all synthesized by enzymes associated with the inner, cytoplasmic membrane, they have to be transported to the OM secondarily, through the periplasm for proteins [59] and probably via the Bayer's patches for lipids. Posibacteria entirely lack both the OM and this transport machinery. The OM and Bayer's patch structure can have evolved only once in prokaryote history as its structural and biogenetic complexity is so great. Transition analysis asks would it have been easier for a negibacterium to have lost the OM (evolution from bottom to top in Fig. 6) and make its wall thicker or for a posibacterium simultaneously to add an OM to a cell without them and simultaneously make the wall thinner and invent machinery for export of both lipids and proteins to it and to make the proteins that would make this complex system function (evolution from top to bottom in Fig. 6)?

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