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Prophage-mediated defence against viral attack and viral counter-defence.

ABSTRACT: Temperate phages are common, and prophages are abundant residents of sequenced bacterial genomes. Mycobacteriophages are viruses that infect mycobacterial hosts including Mycobacterium tuberculosis and Mycobacterium smegmatis, encompass substantial genetic diversity and are commonly temperate. Characterization of ten Cluster N temperate mycobacteriophages revealed at least five distinct prophage-expressed viral defence systems that interfere with the infection of lytic and temperate phages that are either closely related (homotypic defence) or unrelated (heterotypic defence) to the prophage. Target specificity is unpredictable, ranging from a single target phage to one-third of those tested. The defence systems include a single-subunit restriction system, a heterotypic exclusion system and a predicted (p)ppGpp synthetase, which blocks lytic phage growth, promotes bacterial survival and enables efficient lysogeny. The predicted (p)ppGpp synthetase coded by the Phrann prophage defends against phage Tweety infection, but Tweety codes for a tetrapeptide repeat protein, gp54, which acts as a highly effective counter-defence system. Prophage-mediated viral defence offers an efficient mechanism for bacterial success in host-virus dynamics, and counter-defence promotes phage co-evolution.

SUBMITTER: Dedrick RM

PROVIDER: S-EPMC5508108 | biostudies-literature | 2017 Jan

REPOSITORIES: biostudies-literature

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Prophage-mediated defence against viral attack and viral counter-defence.

Dedrick Rebekah M RM Jacobs-Sera Deborah D Bustamante Carlos A Guerrero CA Garlena Rebecca A RA Mavrich Travis N TN Pope Welkin H WH Reyes Juan C Cervantes JC Russell Daniel A DA Adair Tamarah T Alvey Richard R Bonilla J Alfred JA Bricker Jerald S JS Brown Bryony R BR Byrnes Deanna D Cresawn Steven G SG Davis William B WB Dickson Leon A LA Edgington Nicholas P NP Findley Ann M AM Golebiewska Urszula U Grose Julianne H JH Hayes Cory F CF Hughes Lee E LE Hutchison Keith W KW Isern Sharon S Johnson Allison A AA Kenna Margaret A MA Klyczek Karen K KK Mageeney Catherine M CM Michael Scott F SF Molloy Sally D SD Montgomery Matthew T MT Neitzel James J Page Shallee T ST Pizzorno Marie C MC Poxleitner Marianne K MK Rinehart Claire A CA Robinson Courtney J CJ Rubin Michael R MR Teyim Joseph N JN Vazquez Edwin E Ware Vassie C VC Washington Jacqueline J Hatfull Graham F GF

Nature microbiology 20170109

Temperate phages are common, and prophages are abundant residents of sequenced bacterial genomes. Mycobacteriophages are viruses that infect mycobacterial hosts including Mycobacterium tuberculosis and Mycobacterium smegmatis, encompass substantial genetic diversity and are commonly temperate. Characterization of ten Cluster N temperate mycobacteriophages revealed at least five distinct prophage-expressed viral defence systems that interfere with the infection of lytic and temperate phages that ...[more]

PMID: 28067906

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Project description:The arms race between bacteria and their bacteriophages profoundly influences microbial evolution. With an estimated 1023 phage infections occurring per second, there is strong selection for both bacterial survival and phage coevolution for continued propagation. Many phage resistance systems, including restriction-modification systems, clustered regularly interspaced short palindromic repeat-Cas (CRISPR-Cas) systems, a variety of abortive infection systems, and many others that are not yet mechanistically defined, have been described. Temperate bacteriophages are common and form stable lysogens that are immune to superinfection by the same or closely related phages. However, temperate phages collude with their hosts to confer defense against genomically distinct phages, to the mutual benefit of the bacterial host and the prophage. Prophage-mediated viral systems have been described in Mycobacterium phages and Pseudomonas phages but are predicted to be widespread throughout the microbial world. Here we describe a new viral defense system in which the mycobacteriophage Sbash prophage colludes with its Mycobacterium smegmatis host to confer highly specific defense against infection by the unrelated mycobacteriophage Crossroads. Sbash genes 30 and 31 are lysogenically expressed and are necessary and sufficient to confer defense against Crossroads but do not defend against any of the closely related phages grouped in subcluster L2. The mapping of Crossroads defense escape mutants shows that genes 132 and 141 are involved in recognition by the Sbash defense system and are proposed to activate a loss in membrane potential mediated by Sbash gp30 and gp31.IMPORTANCE Viral infection is an ongoing challenge to bacterial survival, and there is strong selection for development or acquisition of defense systems that promote survival when bacteria are attacked by bacteriophages. Temperate phages play central roles in these dynamics through lysogenic expression of genes that defend against phage attack, including those unrelated to the prophage. Few prophage-mediated viral defense systems have been characterized, but they are likely widespread both in phage genomes and in the prophages integrated in bacterial chromosomes.

Dataset Information

Prophage-mediated defence against viral attack and viral counter-defence.

Publications

Prophage-mediated defence against viral attack and viral counter-defence.

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