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Pervasive domestication of defective prophages by bacteria
Edited by W. Ford Doolittle, Dalhousie University, Halifax, NS, Canada, and approved July 7, 2014 (received for review March 21, 2014)

Significance
Several molecular systems with important adaptive roles have originated from the domestication of integrated phages (prophages). However, the evolutionary mechanisms and extent of prophage domestication remain poorly understood. In this work, we detected several hundred prophages originating from common integration events and described their dynamics of degradation within their hosts. Surprisingly, we observed strong conservation of the sequence of most vertically inherited prophages, including selection for genes encoding phage-specific functions. These results suggest pervasive domestication of parasites by the bacterial hosts. Because prophages account for a large fraction of bacterial genomes, phage domestication may drive bacterial adaptation.
Abstract
Integrated phages (prophages) are major contributors to the diversity of bacterial gene repertoires. Domestication of their components is thought to have endowed bacteria with molecular systems involved in secretion, defense, warfare, and gene transfer. However, the rates and mechanisms of domestication remain unknown. We used comparative genomics to study the evolution of prophages within the bacterial genome. We identified over 300 vertically inherited prophages within enterobacterial genomes. Some of these elements are very old and might predate the split between Escherichia coli and Salmonella enterica. The size distribution of prophage elements is bimodal, suggestive of rapid prophage inactivation followed by much slower genetic degradation. Accordingly, we observed a pervasive pattern of systematic counterselection of nonsynonymous mutations in prophage genes. Importantly, such patterns of purifying selection are observed not only on accessory regions but also in core phage genes, such as those encoding structural and lysis components. This suggests that bacterial hosts select for phage-associated functions. Several of these conserved prophages have gene repertoires compatible with described functions of adaptive prophage-derived elements such as bacteriocins, killer particles, gene transfer agents, or satellite prophages. We suggest that bacteria frequently domesticate their prophages. Most such domesticated elements end up deleted from the bacterial genome because they are replaced by analogous functions carried by new prophages. This puts the bacterial genome in a state of continuous flux of acquisition and loss of phage-derived adaptive genes.
Footnotes
- ↵1To whom correspondence should be addressed. Email: lbobay{at}pasteur.fr.
Author contributions: L.-M.B., M.T., and E.P.C.R. designed research; L.-M.B. performed research; L.-M.B. analyzed data; and L.-M.B., M.T., and E.P.C.R. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1405336111/-/DCSupplemental.
Freely available online through the PNAS open access option.