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

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

doi:10.1038/s41467-021-26520-4

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

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

^*Corresponding author for this work

Strathclyde Institute Of Pharmacy And Biomedical Sciences

Research output: Contribution to journal › Article › peer-review

44 Citations (Scopus)

4 Downloads (Pure)

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.

Original language	English
Article number	6510
Number of pages	12
Journal	Nature Communications
Volume	12
DOIs	https://doi.org/10.1038/s41467-021-26520-4
Publication status	Published - 8 Nov 2021

Funding

This work was supported in part by the Singapore Ministry of Education MOE2017-T2-2-163 and MOE2019-T2-2-162 to J.C.; and by MR/M003876/1, MR/V000772/1 and MR/ S00940X/1 from the Medical Research Council (UK), BB/N002873/1, BB/V002376/1 and BB/S003835/1 from the Biotechnology and Biological Sciences Research Council (BBSRC, UK), ERC-ADG-2014 Proposal n° 670932 Dut-signal (from EU), to J.R.P; and Wellcome Trust 201531/Z/16/Z to J.R.P.

Keywords

lysogenic induction
bacteriophage
Salmonella phage
lateral transduction

Access to Document

10.1038/s41467-021-26520-4Licence: CC BY 4.0

Fillol-Salom-etal-NC-2021-Lateral-transduction-is-inherent-to-the-life-cycle-of-the-archetypical-Salmonella-phage-P22Final published version, 2.16 MBLicence: CC BY 4.0

Cite this

@article{2c6f12eafeec442e92e4464d4369f04d,

title = "Lateral transduction is inherent to the life cycle of the archetypical Salmonella phage P22",

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.",

keywords = "lysogenic induction, bacteriophage, Salmonella phage, lateral transduction",

author = "Alfred Fillol-Salom and Rodrigo Bacigalupe and Suzanne Humphrey and Chiang, {Yin Ning} and John Chen and Penad{\'e}s, {Jos{\'e} R.}",

year = "2021",

month = nov,

day = "8",

doi = "10.1038/s41467-021-26520-4",

language = "English",

volume = "12",

journal = "Nature Communications",

issn = "2041-1723",

}

TY - JOUR

T1 - Lateral transduction is inherent to the life cycle of the archetypical Salmonella phage P22

AU - Fillol-Salom, Alfred

AU - Bacigalupe, Rodrigo

AU - Humphrey, Suzanne

AU - Chiang, Yin Ning

AU - Chen, John

AU - Penadés, José R.

PY - 2021/11/8

Y1 - 2021/11/8

N2 - 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.

AB - 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.

KW - lysogenic induction

KW - bacteriophage

KW - Salmonella phage

KW - lateral transduction

U2 - 10.1038/s41467-021-26520-4

DO - 10.1038/s41467-021-26520-4

M3 - Article

C2 - 34751192

AN - SCOPUS:85118609759

SN - 2041-1723

VL - 12

JO - Nature Communications

JF - Nature Communications

M1 - 6510

ER -

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

Abstract

Funding

Keywords

Access to Document

Fingerprint

Cite this