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Rooting the tree of life: the phylogenetic jury is still out.

ABSTRACT: This article aims to shed light on difficulties in rooting the tree of life (ToL) and to explore the (sociological) reasons underlying the limited interest in accurately addressing this fundamental issue. First, we briefly review the difficulties plaguing phylogenetic inference and the ways to improve the modelling of the substitution process, which is highly heterogeneous, both across sites and over time. We further observe that enriched taxon samplings, better gene samplings and clever data removal strategies have led to numerous revisions of the ToL, and that these improved shallow phylogenies nearly always relocate simple organisms higher in the ToL provided that long-branch attraction artefacts are kept at bay. Then, we note that, despite the flood of genomic data available since 2000, there has been a surprisingly low interest in inferring the root of the ToL. Furthermore, the rare studies dealing with this question were almost always based on methods dating from the 1990s that have been shown to be inaccurate for much more shallow issues! This leads us to argue that the current consensus about a bacterial root for the ToL can be traced back to the prejudice of Aristotle's Great Chain of Beings, in which simple organisms are ancestors of more complex life forms. Finally, we demonstrate that even the best models cannot yet handle the complexity of the evolutionary process encountered both at shallow depth, when the outgroup is too distant, and at the level of the inter-domain relationships. Altogether, we conclude that the commonly accepted bacterial root is still unproven and that the root of the ToL should be revisited using phylogenomic supermatrices to ensure that new evidence for eukaryogenesis, such as the recently described Lokiarcheota, is interpreted in a sound phylogenetic framework.

SUBMITTER: Gouy R

PROVIDER: S-EPMC4571568 | biostudies-literature | 2015 Sep

REPOSITORIES: biostudies-literature

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Rooting the tree of life: the phylogenetic jury is still out.

Gouy Richard R Baurain Denis D Philippe Hervé H

Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20150901 1678

This article aims to shed light on difficulties in rooting the tree of life (ToL) and to explore the (sociological) reasons underlying the limited interest in accurately addressing this fundamental issue. First, we briefly review the difficulties plaguing phylogenetic inference and the ways to improve the modelling of the substitution process, which is highly heterogeneous, both across sites and over time. We further observe that enriched taxon samplings, better gene samplings and clever data re ...[more]

PMID: 26323760

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Project description:BackgroundDespite 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.ResultsI 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.ConclusionChlorobacteria 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.

Project description:UnlabelledThe emerging Middle East respiratory syndrome coronavirus (MERS-CoV) causes lethal respiratory infections mainly on the Arabian Peninsula. The evolutionary origins of MERS-CoV are unknown. We determined the full genome sequence of a CoV directly from fecal material obtained from a South African Neoromicia capensis bat (NeoCoV). NeoCoV shared essential details of genome architecture with MERS-CoV. Eighty-five percent of the NeoCoV genome was identical to MERS-CoV at the nucleotide level. Based on taxonomic criteria, NeoCoV and MERS-CoV belonged to one viral species. The presence of a genetically divergent S1 subunit within the NeoCoV spike gene indicated that intraspike recombination events may have been involved in the emergence of MERS-CoV. NeoCoV constitutes a sister taxon of MERS-CoV, placing the MERS-CoV root between a recently described virus from African camels and all other viruses. This suggests a higher level of viral diversity in camels than in humans. Together with serologic evidence for widespread MERS-CoV infection in camelids sampled up to 20 years ago in Africa and the Arabian Peninsula, the genetic data indicate that camels act as sources of virus for humans rather than vice versa. The majority of camels on the Arabian Peninsula is imported from the Greater Horn of Africa, where several Neoromicia species occur. The acquisition of MERS-CoV by camels from bats might have taken place in sub-Saharan Africa. Camelids may represent mixing vessels for MERS-CoV and other mammalian CoVs.ImportanceIt is unclear how, when, and where the highly pathogenic MERS-CoV emerged. We characterized the full genome of an African bat virus closely related to MERS-CoV and show that human, camel, and bat viruses belong to the same viral species. The bat virus roots the phylogenetic tree of MERS-CoV, providing evidence for an evolution of MERS-CoV in camels that preceded that in humans. The revised tree suggests that humans are infected by camels rather than vice versa. Although MERS-CoV cases occur mainly on the Arabian Peninsula, the data from this study together with serologic and molecular investigations of African camels indicate that the initial host switch from bats may have taken place in Africa. The emergence of MERS-CoV likely involved exchanges of genetic elements between different viral ancestors. These exchanges may have taken place either in bat ancestors or in camels acting as mixing vessels for viruses from different hosts.

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Rooting the tree of life: the phylogenetic jury is still out.

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Rooting the tree of life: the phylogenetic jury is still out.

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