Bacteriophages benefit from generalized transduction.
Bacteriophages
/ genetics
Computer Simulation
DNA Packaging
/ genetics
Drug Resistance, Bacterial
/ genetics
Evolution, Molecular
Humans
Lysogeny
/ genetics
Models, Biological
Prophages
/ genetics
Salmonella typhimurium
/ drug effects
Staphylococcus aureus
/ drug effects
Transduction, Genetic
Virulence
/ genetics
Journal
PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921
Informations de publication
Date de publication:
07 2019
07 2019
Historique:
received:
31
03
2019
accepted:
03
06
2019
revised:
17
07
2019
pubmed:
6
7
2019
medline:
3
1
2020
entrez:
6
7
2019
Statut:
epublish
Résumé
Temperate phages are bacterial viruses that as part of their life cycle reside in the bacterial genome as prophages. They are found in many species including most clinical strains of the human pathogens, Staphylococcus aureus and Salmonella enterica serovar Typhimurium. Previously, temperate phages were considered as only bacterial predators, but mounting evidence point to both antagonistic and mutualistic interactions with for example some temperate phages contributing to virulence by encoding virulence factors. Here we show that generalized transduction, one type of bacterial DNA transfer by phages, can create conditions where not only the recipient host but also the transducing phage benefit. With antibiotic resistance as a model trait we used individual-based models and experimental approaches to show that antibiotic susceptible cells become resistant to both antibiotics and phage by i) integrating the generalized transducing temperate phages and ii) acquiring transducing phage particles carrying antibiotic resistance genes obtained from resistant cells in the environment. This is not observed for non-generalized transducing temperate phages, which are unable to package bacterial DNA, nor for generalized transducing virulent phages that do not form lysogens. Once established, the lysogenic host and the prophage benefit from the existence of transducing particles that can shuffle bacterial genes between lysogens and for example disseminate resistance to antibiotics, a trait not encoded by the phage. This facilitates bacterial survival and leads to phage population growth. We propose that generalized transduction can function as a mutualistic trait where temperate phages cooperate with their hosts to survive in rapidly-changing environments. This implies that generalized transduction is not just an error in DNA packaging but is selected for by phages to ensure their survival.
Identifiants
pubmed: 31276485
doi: 10.1371/journal.ppat.1007888
pii: PPATHOGENS-D-19-00604
pmc: PMC6636781
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1007888Subventions
Organisme : Wellcome Trust
ID : 201531/Z/16Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 209397/Z/17/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M003876/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/S00940X/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 201531/Z/16/Z
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/S003835/1
Pays : United Kingdom
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
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