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.

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Figure 1: Two evolutionary modes correlate with phage lifestyle.
Figure 2: Phage clusters exhibit unique evolutionary trajectories.
Figure 3: Evolutionary modes correlate with different rates of HGT.
Figure 4: Host phyla exhibit diversity in phage evolutionary modes.

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Acknowledgements

The authors thank J. Lawrence, R. Hendrix and N. Clark for discussions and R. Dedrick, D. Jacobs-Sera and W. Pope for comments on the manuscript. This research was supported by funding from National Institutes of Health grant GM116884, by Howard Hughes Medical Institute grant 54308198 and by National Science Foundation Graduate Research Fellowship grant 1247842.

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T.N.M. performed the experiments. T.N.M. and G.F.H. interpreted the results and wrote the paper.

Corresponding author

Correspondence to Graham F. Hatfull.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1–11. (PDF 8366 kb)

Supplementary Data 1

This file contains list of phages used in this study, together with associated information. (CSV 558 kb)

Supplementary Data 2

This file contains raw data with all pairwise genome comparisons. (CSV 178319 kb)

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Mavrich, T., Hatfull, G. Bacteriophage evolution differs by host, lifestyle and genome. Nat Microbiol 2, 17112 (2017). https://doi.org/10.1038/nmicrobiol.2017.112

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