Protein signatures distinctive of alpha proteobacteria and its subgroups and a model for α-proteobacterial evolution

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Critical Reviews in Microbiology, 31:101–135, 2005 Copyright c Taylor & Francis Inc. ISSN: 1040-841X print / 1549-7828 online DOI: 10.1080/10408410590922393

Protein Signatures Distinctive of Alpha Proteobacteria and Its Subgroups and a Model for α-Proteobacterial Evolution
Radhey S. Gupta
Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, CanadaAlpha (α) proteobacteria comprise a large and metabolically diverse group. No biochemical or molecular feature is presently known that can distinguish these bacteria from other groups. The evolutionary relationships among this group, which includes numerous pathogens and agriculturally important microbes, are also not understood. Shared conserved inserts and deletions (i.e., indels or signatures) inmolecular sequences provide a powerful means for identification of different groups in clear terms, and for evolutionary studies (see This review describes, for the first time, a large number of conserved indels in broadly distributed proteins that are distinctive and unifying characteristics of either all α-proteobacteria, or many of its constituent subgroups (i.e.,orders, families, etc.). These signatures were identified by systematic analyses of proteins found in the Rickettsia prowazekii (RP) genome. Conserved indels that are unique to αproteobacteria are present in the following proteins: Cytochrome c oxidase assembly protein Ctag, PurC, DnaB, ATP synthase αsubunit, exonuclease VII, prolipoprotein phosphatidylglycerol transferase, RP-400, FtsK, puruvatephosphate dikinase, cytochrome b, MutY, and homoserine dehydrogenase. The signatures in succinyl-CoA synthetase, cytochrome oxidase I, alanyl-tRNA synthetase, and MutS proteins are found in all α-proteobacteria, except the Rickettsiales, indicating that this group has diverged prior to the introduction of these signatures. A number of proteins contain conserved indels that are specific forRickettsiales (XerD integrase and leucine aminopeptidase), Rickettsiaceae (Mfd, ribosomal protein L19, FtsZ, Sigma 70 and exonuclease VII), or Anaplasmataceae (Tgt and RP-314), and they distinguish these groups from all others. Signatures in DnaA, RP-057, and DNA ligase A are commonly shared by various Rhizobiales, Rhodobacterales, and Caulobacter, suggesting that these groups shared a common ancestorexclusive of other α-proteobacteria. A specific relationship between Rhodobacterales and Caulobacter is indicated by a large insert in the Asn-Gln amidotransferase. The Rhizobiales group of species are distinguished from others by a large insert in the Trp-tRNA synthetase. Signature sequences in a number of other proteins (viz. oxoglutarate dehydogenase, succinyl-CoA synthase, LytB, DNA gyrase A, LepA,and Ser-tRNA synthetase) serve to distinguish the Rhizobiaceae, Brucellaceae, and Phyllobacteriaceae families from Bradyrhizobiaceae and Methylobacteriaceae. Based

on the distribution patterns of these signatures, it is now possible to logically deduce a model for the branching order among α-proteobacteria, which is as follows: Rickettsiales → Rhodospirillales-Sphingomonadales →Rhodobacterales-Caulobacterales → Rhizobiales (Rhizobiaceaea-Brucellaceae-Phyllobacteriaceae, and Bradyrhizobiaceae). The deduced branching order is also consistent with the topologies in the 16 rRNA and other phylogenetic trees. Signature sequences in a number of other proteins provide evidence that α-proteobacteria is a late branching taxa within Bacteria, which branched after the δ, -subdivisions but prior tothe β,γproteobacteria. The shared presence of many of these signatures in the mitochondrial (eukaryotic) homologs also provides evidence of the α-proteobacterial ancestry of mitochondria. Keywords Bacterial Phylogeny; Alpha Proteobacteria Trees; Protein Signatures; Rickettsiales; Rhodobacterales; Branching Order; Mitochondrial Origin; Rickettsia prowazekii; Rhizobiales

Received 20 December...
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