Secretion Relieves Translational Co-repression by a Specialized Flagellin Paralog

• Published in: Developmental cell Vol. 55; no. 4; pp. 500 - 513.e4
• Main Authors: Ardissone, Silvia, Kint, Nicolas, Petrignani, Bianca, Panis, Gaël, Viollier, Patrick H.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 23.11.2020
• Subjects: 5' Untranslated Regions - genetics; Bacterial Proteins - metabolism; Base Sequence; Binding, Competitive; Brucella melitensis; Caulobacter crescentus; Caulobacter crescentus - genetics; cell cycle; Co-Repressor Proteins - metabolism; FlaF; Flagella - metabolism; Flagellin - metabolism; flagellum; FlbT; FljJ; Gene Expression Regulation, Bacterial; morphological coupling; Protein Binding; Protein Biosynthesis; RNA, Messenger - genetics; RNA, Messenger - metabolism; Tn-Seq; translational regulation; UTR; Caulobacter crescentus; UTR; flagellum; cell cycle; Tn-Seq; FljJ; FlbT; morphological coupling; translational regulation; FlaF; Brucella melitensis
• DOI: 10.1016/j.devcel.2020.10.005
• ISSN: 1534-5807

How cellular checkpoints couple the orderly assembly of macromolecular machines with cell-cycle progression is poorly understood. The alpha-proteobacterium Caulobacter crescentus assembles a single polar flagellum during each cell cycle. We discovered that the expression of multiple flagellin transcripts is licensed by a translational checkpoint responsive to a dual input signal: a secretion-competent hook-basal-body (HBB) structure and a surge in the FlaF secretion chaperone during cytokinesis, instructed by the cell-cycle program. We find that the unorthodox FljJ flagellin, one of the six flagellin paralogs, acts as a checkpoint linchpin, binding both FlaF and the FlbT translational regulator. FljJ recruits FlbT to inhibit translation at the 5′ untranslated region in other flagellin transcripts before HBB assembly. Once FlaF is synthesized and stabilized, it directs FljJ secretion through the HBB, thereby separating FlbT from its co-activator and relieving translational inhibition. The FlbT/FlaF pair is wide spread and its functional properties are conserved in alpha-proteobacteria, including pathogens. [Display omitted] •The FljJ flagellin paralog is secreted but cannot assemble a flagellar homo filament•The secretion chaperone FlaF is required for translation of the structural flagellins•FlbT negatively regulates flagellin translation at the 5′UTR when secretion is blocked•FljJ is a secretion coupler required for FlbT activity and it specifically binds FlbT Ardissone et al. unravel the mechanism of secretion coupling in the Caulobacter crescentus flagellation system that encodes six flagellin paralogs. The FljJ flagellin has adopted a regulatory role, binding the negative regulator FlbT that blocks translation of flagellin transcripts before the flagellar secretion machine exports FljJ to license flagellin synthesis.