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Phylogenomic networks reveal limited phylogenetic range of lateral gene transfer by transduction.

ABSTRACT: Bacteriophages are recognized DNA vectors and transduction is considered as a common mechanism of lateral gene transfer (LGT) during microbial evolution. Anecdotal events of phage-mediated gene transfer were studied extensively, however, a coherent evolutionary viewpoint of LGT by transduction, its extent and characteristics, is still lacking. Here we report a large-scale evolutionary reconstruction of transduction events in 3982 genomes. We inferred 17 158 recent transduction events linking donors, phages and recipients into a phylogenomic transduction network view. We find that LGT by transduction is mostly restricted to closely related donors and recipients. Furthermore, a substantial number of the transduction events (9%) are best described as gene duplications that are mediated by mobile DNA vectors. We propose to distinguish this type of paralogy by the term autology. A comparison of donor and recipient genomes revealed that genome similarity is a superior predictor of species connectivity in the network in comparison to common habitat. This indicates that genetic similarity, rather than ecological opportunity, is a driver of successful transduction during microbial evolution. A striking difference in the connectivity pattern of donors and recipients shows that while lysogenic interactions are highly species-specific, the host range for lytic phage infections can be much wider, serving to connect dense clusters of closely related species. Our results thus demonstrate that DNA transfer via transduction occurs within the context of phage-host specificity, but that this tight constraint can be breached, on rare occasions, to produce long-range LGTs of profound evolutionary consequences.

SUBMITTER: Popa O

PROVIDER: S-EPMC5183456 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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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Phylogenomic networks reveal limited phylogenetic range of lateral gene transfer by transduction.

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