Embracing the enemy: the diversification of microbial gene repertoires by phage-mediated horizontal gene transfer
Graphical abstract
Section snippets
Lysogenic conversion
Lysogeny often involves the integration of the temperate phage genome in the host chromosome, even if a growing number of prophages are found to replicate in cells as plasmids [8, 9]. The expression of prophage genes leads to phenotypic changes in the host that may affect many different traits, including virulence, motility, and inter-bacterial competition (see Refs. [5, 10] for reviews). The identification of the determinants of the decision between lysis and lysogeny can thus illuminate the
Specialized transduction
Specialized transduction results from an event of inaccurate excision of the prophage from the chromosome, for example, by ‘illegitimate’ recombination, that leads to the packaging of a section of the prophage and the contiguous chromosomal DNA (Figure 1). Illegitimate recombination depends on the local density of repeats [32], with the consequence that specialized transduction rates may vary widely in function of the chromosomal context of the prophage. Specialized transduction occurs at very
Generalized transduction
Generalized transduction results from errors in discriminating phage from chromosomal DNA during packaging. This mechanism can transfer any chromosomal sequence, including rDNA [38], and its integration in the host chromosome may require homologous recombination. Generalized transduction has been identified in phages packaging their genome using the headful (pac) mechanism [39], one of several packaging systems of dsDNA phages [3]. Mu-like phages systematically transfer a few kilobases of
Determinants of transfer
Many variables affect phage-mediated HGT, and further theoretical work is needed to understand how they could interact in transmission networks (Box 1). The phage host range is a key variable that affects the ability of these processes to spread genes in communities. The analysis of the networks of gene homology between bacteria and phages (so-called transduction networks) suggests that most transfer takes place between closely related taxa [47], in agreement with the traditional view that
Antibiotic resistance
The role of transduction in the spread of antibiotic resistance genes (ARG) is a relatively recent topic of research because these genes are much often identified in conjugative elements than in phages. However, work in this topic is being spurred by several studies that identified ARGs in gut viromes following antibiotic perturbation [58••, 59], and in natural environments [60]. The analysis of viromes is technically challenging because bacterial contamination can be mistaken by transducing
Conclusions
Much remains to be known regarding the role of phages in HGT (Box 2). Even if metagenomics data suggests that generalized transduction may contribute significantly to HGT in prokaryotes, quantitative data on this process is still lacking. Our ignorance is even more dramatic regarding the significance of the contribution of specialized transduction, whose role in prokaryotic evolution remains to be demonstrated. At this stage, the relevance of lysogeny in HGT is well-established, but novel
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
Work in our laboratory is funded by credits from the CNRS and the Pasteur Institute. We thank Mireille Ansaldi, David Bikard, and a reviewer for comments on a previous version of this manuscript, and Louis-Marie Bobay and Aude Bernheim for discussions.
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