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Bacteriophage evolution differs by host, lifestyle and genome.

ABSTRACT: Bacteriophages play key roles in microbial evolution1,2, marine nutrient cycling3 and human disease4. Phages are genetically diverse, and their genome architectures are characteristically mosaic, driven by horizontal gene transfer with other phages and host genomes5. As a consequence, phage evolution is complex and their genomes are composed of genes with distinct and varied evolutionary histories6,7. However, there are conflicting perspectives on the roles of mosaicism and the extent to which it generates a spectrum of genome diversity8 or genetically discrete populations9,10. Here, we show that bacteriophages evolve within two general evolutionary modes that differ in the extent of horizontal gene transfer by an order of magnitude. Temperate phages distribute into high and low gene flux modes, whereas lytic phages share only the lower gene flux mode. The evolutionary modes are also a function of the bacterial host and different proportions of temperate and lytic phages are distributed in either mode depending on the host phylum. Groups of genetically related phages fall into either the high or low gene flux modes, suggesting there are genetic as well as ecological drivers of horizontal gene transfer rates. Consequently, genome mosaicism varies depending on the host, lifestyle and genetic constitution of phages.

SUBMITTER: Mavrich TN

PROVIDER: S-EPMC5540316 | biostudies-literature | 2017 Jul

REPOSITORIES: biostudies-literature

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Bacteriophage evolution differs by host, lifestyle and genome.

Mavrich Travis N TN Hatfull Graham F GF

Nature microbiology 20170710

Bacteriophages play key roles in microbial evolution1,2, marine nutrient cycling3 and human disease4. Phages are genetically diverse, and their genome architectures are characteristically mosaic, driven by horizontal gene transfer with other phages and host genomes5. As a consequence, phage evolution is complex and their genomes are composed of genes with distinct and varied evolutionary histories6,7. However, there are conflicting perspecti ...[more]

PMID: 28692019

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Project description:BACKGROUND: Burkholderia rhizoxinica is an intracellular symbiont of the phytopathogenic zygomycete Rhizopus microsporus, the causative agent of rice seedling blight. The endosymbiont produces the antimitotic macrolide rhizoxin for its host. It is vertically transmitted within vegetative spores and is essential for spore formation of the fungus. To shed light on the evolution and genetic potential of this model organism, we analysed the whole genome of B. rhizoxinica HKI 0454 - a type strain of endofungal Burkholderia species. RESULTS: The genome consists of a structurally conserved chromosome and two plasmids. Compared to free-living Burkholderia species, the genome is smaller in size and harbors less transcriptional regulator genes. Instead, we observed accumulation of transposons over the genome. Prediction of primary metabolic pathways and transporters suggests that endosymbionts consume host metabolites like citrate, but might deliver some amino acids and cofactors to the host. The rhizoxin biosynthesis gene cluster shows evolutionary traces of horizontal gene transfer. Furthermore, we analysed gene clusters coding for nonribosomal peptide synthetases (NRPS). Notably, B. rhizoxinica lacks common genes which are dedicated to quorum sensing systems, but is equipped with a large number of virulence-related factors and putative type III effectors. CONCLUSIONS: B. rhizoxinica is the first endofungal bacterium, whose genome has been sequenced. Here, we present models of evolution, metabolism and tools for host-symbiont interaction of the endofungal bacterium deduced from whole genome analyses. Genome size and structure suggest that B. rhizoxinica is in an early phase of adaptation to the intracellular lifestyle (genome in transition). By analysis of tranporters and metabolic pathways we predict how metabolites might be exchanged between the symbiont and its host. Gene clusters for biosynthesis of secondary metabolites represent novel targets for genomic mining of cryptic natural products. In silico analyses of virulence-associated genes, secreted proteins and effectors might inspire future studies on molecular mechanisms underlying bacterial-fungal interaction.

Dataset Information

Bacteriophage evolution differs by host, lifestyle and genome.

Publications

Bacteriophage evolution differs by host, lifestyle and genome.

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