Plastic phages – evolution of mosaically related tailed bacteriophage genomes

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Bacteriophage animation It is well established that the genomes of many dsDNA tailed bacteriophages have mosaic relationships, where the mosaicism is defined as patchy sequence similarity when two related phage genomes are compared. The regions with different extents of similarity have been interpreted to be genome sections with different evolutionary histories that have been horizontally exchanged among phages. Such exchangeable genome segments have been called “modules”, and these modules are hypothesized to be minimal autonomously functional units, such as groups of genes that must function together or single proteins or even protein domains that function independently. Phage genome mosaicism can range from quantitative differences in the extent of sequence similarity between homologous regions to parallel non-homologous genome sections that encode completely different proteins.

A quantitative understanding of the extant diversity, exchange rates and precise boundaries of these genetic “modules” has remained elusive. Recent advances in the ease of DNA sequence determination have resulted in a rapid increase in the number of phage genome sequences available, and these provide an opportunity for much more detailed and robust analyses of phage genome mosaicism. This paper focuses on the virion assembly genes of fifty-seven different of phages that are “closely” related to Salmonella enterica phage P22. Analysis of such a large number of unambiguously orthologous gene sets is powerful, and analysis of phage P22 is particularly informative because of the extensive body of experimental work on phage P22 virion structure and the specific roles and interactions of its morphogenetic proteins.

Evolution of mosaically related tailed bacteriophage genomes seen through the lens of phage P22 virion assembly. Virology. 2011 411(2): 393-415
The mosaic composition of the genomes of dsDNA tailed bacteriophages (Caudovirales) is well known. Observations of this mosaicism have generally come from comparisons of small numbers of often rather distantly related phages, and little is known about the frequency or detailed nature of the processes that generate this kind of diversity. Here we review and examine the mosaicism within fifty-seven clusters of virion assembly genes from bacteriophage P22 and its “close” relatives. We compare these orthologous gene clusters, discuss their surprising diversity and document horizontal exchange of genetic information between subgroups of the P22-like phages as well as between these phages and other phage types. We also point out apparent restrictions in the locations of mosaic sequence boundaries in this gene cluster. The relatively large sample size and the fact that phage P22 virion structure and assembly are exceptionally well understood make the conclusions especially informative and convincing.

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