Lateral transduction is inherent to the life cycle of the archetypical Salmonella phage P22

Alfred Fillol-Salom,John Chen,Suzanne Humphrey,Rodrigo Bacigalupe,Yin Ning Chiang,José R Penadés

doi:10.1038/s41467-021-26520-4

Abstract

Lysogenic induction ends the stable association between a bacteriophage and its host, and the transition to the lytic cycle begins with early prophage excision followed by DNA replication and packaging (ERP). This temporal program is considered universal for P22-like temperate phages, though there is no direct evidence to support the timing and sequence of these events. Here we report that the long-standing ERP program is an observation of the experimentally favored Salmonella phage P22 tsc229 heat-inducible mutant, and that wild-type P22 actually follows the replication-packaging-excision (RPE) program. We find that P22 tsc229 excises early after induction, but P22 delays excision to just before it is detrimental to phage production. This allows P22 to engage in lateral transduction. Thus, at minimal expense to itself, P22 has tuned the timing of excision to balance propagation with lateral transduction, powering the evolution of its host through gene transfer in the interest of self-preservation.

Highlights

Lysogenic induction ends the stable association between a bacteriophage and its host, and the transition to the lytic cycle begins with early prophage excision followed by DNA replication and packaging (ERP)
Some are mantained as episomes, most temperate phages reproduce by integrating their genomes into the bacterial host chromosome where they persist in a dormant state as a prophage and replicate passively as part of the bacterial chromosome during cell division[1]
Recently we found that some staphylococcal prophages delay excision until later in their lytic cycle[20], and others have shown that some Salmonella prophages likely do the same[21]

Summary

Introduction

Lysogenic induction ends the stable association between a bacteriophage and its host, and the transition to the lytic cycle begins with early prophage excision followed by DNA replication and packaging (ERP). Λ- and P22-like prophages are presumed to excise (and circularize) early as the first step in the temporal program of excision–replication–packaging (the ERP cycle; Fig. 1) This sequence of events is widely accepted and believed to be universal for these type of phages because it was thought that DNA packaging prior to excision would split the viral genome and prevent the production of infectious phage particles. To prevent splitting the integrated viral genome in two, bidirectional in situ replication (prior to DNA packaging) creates sufficient genomic redundancy to enable LT and phage maturation to proceed in parallel Together, this results in a mode of transduction that produces normal phage titers and transfers bacterial chromosomal DNA at frequencies far greater than previously observed for known mechanisms of host gene transfer. LT was described using S. aureus phages, raising the question whether this mechanism of gene transfer is exclusive to this species or widespread in nature

Methods

Results

Conclusion