Dataset Information

Direct phylogenetic evidence for lateral transfer of elongation factor-like gene.

ABSTRACT: Genes encoding elongation factor-like (EFL) proteins, which show high similarity to elongation factor-1alpha (EF-1alpha), have been found in phylogenetically distantly related eukaryotes. The sporadic distribution of "EFL-containing" lineages within "EF-1alpha-containing" lineages indirectly, but strongly, suggests lateral gene transfer as the principal driving force in EFL evolution. However, one of the most critical aspects in the above hypothesis, the donor lineages in any putative cases of lateral EFL gene transfer, remained unclear. In this study, we provide direct evidence for lateral transfer of an EFL gene through the analyses of 10 diatom EFL genes. All diatom EFL homologues tightly clustered in phylogenetic analyses, suggesting acquisition of the exogenous EFL gene early in diatom evolution. Our survey additionally identified Thalassiosira pseudonana as a eukaryote bearing EF-1alpha and EFL genes and secondary EFL gene loss in Phaeodactylum tricornutum, the complete genome of which encodes only the EF-1alpha gene. Most importantly, the EFL phylogeny recovered a robust grouping of homologues from diatoms, the cercozoan Bigelowiella natans, and the foraminifer Planoglabratella opecularis, with the diatoms nested within the Bigelowiella plus Planoglabratella (Rhizaria) grouping. The particular relationships recovered are further consistent with two characteristic sequence motifs. The best explanation of our data analyses is an EFL gene transfer from a foraminifer to a diatom, the first case in which the donor-recipient relationship was clarified. Finally, based on a reverse transcriptase quantitative PCR assay and the genome information of Thalassiosira and Phaeodactylum, we propose the loss of elongation factor function in Thalassiosira EF-1alpha.

SUBMITTER: Kamikawa R

PROVIDER: S-EPMC2383962 | biostudies-literature | 2008 May

REPOSITORIES: biostudies-literature

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Direct phylogenetic evidence for lateral transfer of elongation factor-like gene.

Kamikawa Ryoma R Inagaki Yuji Y Sako Yoshihiko Y

Proceedings of the National Academy of Sciences of the United States of America 20080505 19

Genes encoding elongation factor-like (EFL) proteins, which show high similarity to elongation factor-1alpha (EF-1alpha), have been found in phylogenetically distantly related eukaryotes. The sporadic distribution of "EFL-containing" lineages within "EF-1alpha-containing" lineages indirectly, but strongly, suggests lateral gene transfer as the principal driving force in EFL evolution. However, one of the most critical aspects in the above hypothesis, the donor lineages in any putative cases of l ...[more]

PMID: 18458344

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Project description:The elongation factor Tu, encoded by tuf genes, is a GTP binding protein that plays a central role in protein synthesis. One to three tuf genes per genome are present, depending on the bacterial species. Most low-G+C-content gram-positive bacteria carry only one tuf gene. We have designed degenerate PCR primers derived from consensus sequences of the tuf gene to amplify partial tuf sequences from 17 enterococcal species and other phylogenetically related species. The amplified DNA fragments were sequenced either by direct sequencing or by sequencing cloned inserts containing putative amplicons. Two different tuf genes (tufA and tufB) were found in 11 enterococcal species, including Enterococcus avium, Enterococcus casseliflavus, Enterococcus dispar, Enterococcus durans, Enterococcus faecium, Enterococcus gallinarum, Enterococcus hirae, Enterococcus malodoratus, Enterococcus mundtii, Enterococcus pseudoavium, and Enterococcus raffinosus. For the other six enterococcal species (Enterococcus cecorum, Enterococcus columbae, Enterococcus faecalis, Enterococcus sulfureus, Enterococcus saccharolyticus, and Enterococcus solitarius), only the tufA gene was present. Based on 16S rRNA gene sequence analysis, the 11 species having two tuf genes all have a common ancestor, while the six species having only one copy diverged from the enterococcal lineage before that common ancestor. The presence of one or two copies of the tuf gene in enterococci was confirmed by Southern hybridization. Phylogenetic analysis of tuf sequences demonstrated that the enterococcal tufA gene branches with the Bacillus, Listeria, and Staphylococcus genera, while the enterococcal tufB gene clusters with the genera Streptococcus and Lactococcus. Primary structure analysis showed that four amino acid residues encoded within the sequenced regions are conserved and unique to the enterococcal tufB genes and the tuf genes of streptococci and Lactococcus lactis. The data suggest that an ancestral streptococcus or a streptococcus-related species may have horizontally transferred a tuf gene to the common ancestor of the 11 enterococcal species which now carry two tuf genes.

Project description:Lateral gene transfer (LGT) is an important mechanism of natural variation among prokaryotes. Over the full course of evolution, most or all of the genes resident in a given prokaryotic genome have been affected by LGT, yet the frequency of LGT can vary greatly across genes and across prokaryotic groups. The proteobacteria are among the most diverse of prokaryotic taxa. The prevalence of LGT in their genome evolution calls for the application of network-based methods instead of tree-based methods to investigate the relationships among these species. Here, we report networks that capture both vertical and horizontal components of evolutionary history among 1,207,272 proteins distributed across 329 sequenced proteobacterial genomes. The network of shared proteins reveals modularity structure that does not correspond to current classification schemes. On the basis of shared protein-coding genes, the five classes of proteobacteria fall into two main modules, one including the alpha-, delta-, and epsilonproteobacteria and the other including beta- and gammaproteobacteria. The first module is stable over different protein identity thresholds. The second shows more plasticity with regard to the sequence conservation of proteins sampled, with the gammaproteobacteria showing the most chameleon-like evolutionary characteristics within the present sample. Using a minimal lateral network approach, we compared LGT rates at different phylogenetic depths. In general, gene evolution by LGT within proteobacteria is very common. At least one LGT event was inferred to have occurred in at least 75% of the protein families. The average LGT rate at the species and class depth is about one LGT event per protein family, the rate doubling at the phylum level to an average of two LGT events per protein family. Hence, our results indicate that the rate of gene acquisition per protein family is similar at the level of species (by recombination) and at the level of classes (by LGT). The frequency of LGT per genome strongly depends on the species lifestyle, with endosymbionts showing far lower LGT frequencies than free-living species. Moreover, the nature of the transferred genes suggests that gene transfer in proteobacteria is frequently mediated by conjugation.

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Direct phylogenetic evidence for lateral transfer of elongation factor-like gene.

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Direct phylogenetic evidence for lateral transfer of elongation factor-like gene.

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