Mechanism of phage sensing and abortion by toxin-antitoxin-chaperone systems

Author:

Mets ToomasORCID,Kurata TatsuakiORCID,Ernits KarinORCID,Johansson Marcus J. O.ORCID,Craig Sophie Z.,Evora Gabriel Medina,Buttress Jessica A.ORCID,Odai Roni,Coppieters‘t Wallant KyoORCID,Nakamoto Jose A.ORCID,Shyrokova Lena,Egorov Artyom A.ORCID,Doering Christopher Ross,Brodiazhenko TetianaORCID,Laub Michael T.,Tenson Tanel,Strahl Henrik,Martens Chloe,Harms AlexanderORCID,Garcia-Pino AbelORCID,Atkinson Gemma C.ORCID,Hauryliuk VasiliORCID

Abstract

SummaryToxin-antitoxins (TAs) are prokaryotic two-gene systems comprised of a toxin neutralised by an antitoxin. Toxin-antitoxin-chaperone (TAC) systems additionally include a SecB-like chaperone that stabilises the antitoxin by recognising its chaperone addiction (ChAD) element. TACs have been shown to mediate antiphage defence, but the mechanisms of viral sensing and restriction are unexplored. We identify and characterise twoEscherichia coliantiphage TAC systems containing HigBA and CmdTA TA units, HigBAC and CmdTAC. The HigBAC is triggered through recognition of the gpV major tail protein of phage λ. Both the ChAD and gpV are recognised by the HigC chaperone through analogous aromatic molecular patterns, explaining the mechanism of activation. We show that the CmdT ADP-ribosyltransferase toxin modifies mRNA to shut down protein synthesis. We establish the modularity of TACs by creating a hybrid broad-spectrum antiphage system combining the CmdTA TA warhead with the HigC chaperone phage sensor.HighlightsE. coliHigBAC and CmdTAC are translation-targeting phage immunity TAC systems HigC chaperone recognises phage λ major tail protein to trigger HigBAC toxicityCmdT ADP-ribosyltransferase toxin abrogates translation through modification of mRNA HigC combined with CmdTA yields hybrid broad-spectrum antiphage defence system

Publisher

Cold Spring Harbor Laboratory

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