Phylogenomics and protein signatures elucidating the evolutionary relationships among the Gammaproteobacteria

Abstract

The class Gammaproteobacteria, which forms one of the largest groups within bacteria, is currently distinguished from other bacteria solely on the basis of its branching in phylogenetic trees. No molecular or biochemical characteristic is known that is unique to the class Gammaproteobacteria or its different subgroups (orders). The relationship among different orders of gammaproteobacteria is also not clear. In this study, we present detailed phylogenomic and comparative genomic analyses on gammaproteobacteria that clarify some of these issues. Phylogenetic trees based on concatenated sequences for 13 and 36 universally distributed proteins were constructed for 45 members of the class Gammaproteobacteria covering 13 of its 14 orders. In these trees, species from a number of the subgroups formed distinct clades and their relative branching order was indicated as follows (from the most recent to the earliest diverging): Enterobacteriales .Pasteurellales .Vibrionales, Aeromonadales .Alteromonadales .Oceanospirillales, Pseudomonadales .Chromatiales, Legionellales, Methylococcales, Xanthomonadales, Cardiobacteriales, Thiotrichales. Four conserved indels in four widely distributed proteins that are specific for gammaproteobacteria are also described. A 2 aa deletion in 59-phosphoribosyl-5-aminoimidazole-4-carboxamide transformylase (AICAR transformylase; PurH) was a distinctive characteristic of all gammaproteobacteria (except Francisella tularensis). Two other conserved indels (a 4 aa deletion in RNA polymerase b-subunit and a 1 aa deletion in ribosomal protein L16) were found uniquely in various species of the orders Enterobacteriales, Pasteurellales, Vibrionales, Aeromonadales and Alteromonadales, but were not found in other gammaproteobacteria. Lastly, a 2 aa deletion in leucyl-tRNA synthetase was commonly present in the above orders of the class Gammaproteobacteria and also in some members of the order Oceanospirillales. The presence of the conserved indels in these gammaproteobacterial orders indicates that species from these orders shared a common ancestor that was separate from other bacteria, a suggestion that is supported by phylogenetic studies. Systematic BLASTP searches were also conducted on various open reading frames (ORFs) in the genome of Escherichia coli K-12. These analyses identified 75 proteins that were unique to most members of the class Gammaproteobacteria or were restricted to species from some of its main orders (Enterobacteriales; Enterobacteriales and Pasteurellales; Enterobacteriales, Pasteurellales, Vibrionales, Aeromonadales and Alteromonadales; and the Enterobacteriales, Pasteurellales, Vibrionales, Aeromonadales, Alteromonadales, Oceanospirillales and Pseudomonadales etc.). The genes for these proteins have evolved at various stages during the evolution of gammaproteobacteria and their species distribution pattern, in conjunction with other results presented here, provide valuable information regarding the evolutionary relationships among these bacteria.Abbreviations: AICAR transformy...

Phylogeny of Gammaproteobacteria

“…Taxonomic families represented by more than one taxon, except in cases in which the lone family represents the order, are bracketed, extending brackets to include unassigned taxa as necessary; only two of these nine families are split in our tree. Two nodes of interest are marked: the X indicates a node supported by a rare indel (10), and the star indicates a fully supported node that groups members of Pseudomonadales, Alteromonadales, and Oceanospirillales while excluding other members of each order. All known members of the latter clade, and no other known bacteria, autoregulate a ribosomal protein operon through strong mimicry of a 23S rRNA domain (38).…”

“…Previous phylogenetic studies of this group indicate deep branches that make it difficult to obtain a large well-resolved phylogeny (10,40). Taking advantage of the large number of genomes available for the class, we have followed a multiprotein approach to gammaproteobacterial phylogeny (39).…”

The Spot 42 RNA: A regulatory small RNA with roles in the central metabolism

“…The circular phylogenetic tree (made using the iTol web tool) shows all major branches of Bacteria. The gamma-proteobacteria phylogeny in the right panel is based on Gao et al 25 Here, numbers in parentheses indicate the number of complete genomes that contain spf (first number) and the total number of available complete genomes (second number) in each order. In addition, spf is found in 8 Chromatiales draft genomes (asterisk).…”

Phylogeny of γ-proteobacteria inferred from comparisons of 3’ end 16S rRNA gene and 5’ end 16S-23S ITS nucleotide sequences

“…Very recently, Gao et al, [26] have used a combination of phylogenomic and comparative genomic approaches to reconstruct the phylogeny of γ-proteobacteria.…”