Abstract
BackgroundHorizontal transfer plays an important role in the evolution of bacterial genomes, yet it obeys several constraints, including the ecological opportunity to meet other organisms, the presence of transfer systems, and the fitness of the transferred genes. Bacteria from the Planctomyctetes, Verrumicrobia, Chlamydiae (PVC) super-phylum have a compartmentalized cell plan delimited by an intracytoplasmic membrane that might constitute an additional constraint with particular impact on bacterial evolution. In this investigation, we studied the evolution of 33 genomes from PVC species and focused on the rate and the nature of horizontally transferred sequences in relation to their habitat and their cell plan.ResultsUsing a comparative phylogenomic approach, we showed that habitat influences the evolution of the bacterial genome’s content and the flux of horizontal transfer of DNA (HT). Thus bacteria from soil, from insects and ubiquitous bacteria presented the highest average of horizontal transfer compared to bacteria living in water, extracellular bacteria in vertebrates, bacteria from amoeba and intracellular bacteria in vertebrates (with a mean of 379 versus 110 events per species, respectively and 7.6% of each genomes due to HT against 4.8%). The partners of these transfers were mainly bacterial organisms (94.9%); they allowed us to differentiate environmental bacteria, which exchanged more with Proteobacteria, and bacteria from vertebrates, which exchanged more with Firmicutes. The functional analysis of the horizontal transfers revealed a convergent evolution, with an over-representation of genes encoding for membrane biogenesis and lipid metabolism, among compartmentalized bacteria in the different habitats.ConclusionsThe presence of an intracytoplasmic membrane in PVC species seems to affect the genome’s evolution through the selection of transferred DNA, according to their encoded functions.
Highlights
Horizontal transfer plays an important role in the evolution of bacterial genomes, yet it obeys several constraints, including the ecological opportunity to meet other organisms, the presence of transfer systems, and the fitness of the transferred genes
When using OrthoMCL, 124,175 out of 206,508 proteins that form the pangenome of the PVC group bacteria, could be assigned to 16,918 different orthologous groups (OG)
When species were clustered according to their gene contents, some bacteria sharing a same ecological niche were preferentially grouped together, forming subclusters within the clusters, determined by phylogenetic relationships or disturbing the phylogenetic unity of some groups, like the Verrucomicrobiae, Spirochaetes and Planctomycetes (Additional file 5)
Summary
Horizontal transfer plays an important role in the evolution of bacterial genomes, yet it obeys several constraints, including the ecological opportunity to meet other organisms, the presence of transfer systems, and the fitness of the transferred genes. Bacteria from the Planctomyctetes, Verrumicrobia, Chlamydiae (PVC) super-phylum have a compartmentalized cell plan delimited by an intracytoplasmic membrane that might constitute an additional constraint with particular impact on bacterial evolution. In this investigation, we studied the evolution of 33 genomes from PVC species and focused on the rate and the nature of horizontally transferred sequences in relation to their habitat and their cell plan. The intrinsic constraints that influence the entrance and integration of foreign DNA into a recipient genome include the exclusion surface that limits the entrance of specific sequences in some bacteria [3], the presence of CRISPR that decreases the quantity of transferred sequences insertion in recipient genomes [19, 20] and the presence of some endonucleases that can destroy foreign DNA [3, 21]
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