De- and repolarization mechanism of flagellar morphogenesis during a bacterial cell cycle

Nicole J. Davis, Yaniv Cohen, Stefano Sanselicio, Coralie Fumeaux, Shogo Ozaki, Jennifer Luciano, Ricardo C. Guerrero-Ferreira, Elizabeth R. Wright, Urs Jenal, Patrick H. Viollier

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

Eukaryotic morphogenesis is seeded with the establishment and subsequent amplification of polarity cues at key times during the cell cycle, often using (cyclic) nucleotide signals. We discovered that flagellum de- and repolarization in the model prokaryote Caulobacter crescentus is precisely orchestrated through at least three spatiotemporal mechanisms integrated at TipF. We show that TipF is a cell cycle-regulated receptor for the second messenger-bis-(3′-5′)-cyclic dimeric guanosine monophosphate (c-di-GMP)-that perceives and transduces this signal through the degenerate c-di-GMP phosphodiesterase (EAL) domain to nucleate polar flagellum biogenesis. Once c-di-GMP levels rise at the G1 → S transition, TipF is activated, stabilized, and polarized, enabling the recruitment of downstream effectors, including flagellar switch proteins and the PflI positioning factor, at a preselected pole harboring the TipN landmark. These c-di-GMP-dependent events are coordinated with the onset of tipF transcription in early S phase and together enable the correct establishment and robust amplification of TipF-dependent polarization early in the cell cycle. Importantly, these mechanisms also govern the timely removal of TipF at cell division coincident with the drop in c-di-GMP levels, thereby resetting the flagellar polarization state in the next cell cycle after a preprogrammed period during which motility must be suspended.

Original languageEnglish
Pages (from-to)2049-2062
Number of pages14
JournalGenes and Development
Volume27
Issue number18
DOIs
Publication statusPublished - Sep 1 2013
Externally publishedYes

Fingerprint

Cyclic GMP
Morphogenesis
Cell Cycle
Flagella
Caulobacter crescentus
Cyclic Nucleotides
Phosphoric Diester Hydrolases
Second Messenger Systems
S Phase
Cell Division
Cues
Proteins

All Science Journal Classification (ASJC) codes

  • Genetics
  • Developmental Biology

Cite this

Davis, N. J., Cohen, Y., Sanselicio, S., Fumeaux, C., Ozaki, S., Luciano, J., ... Viollier, P. H. (2013). De- and repolarization mechanism of flagellar morphogenesis during a bacterial cell cycle. Genes and Development, 27(18), 2049-2062. https://doi.org/10.1101/gad.222679.113

De- and repolarization mechanism of flagellar morphogenesis during a bacterial cell cycle. / Davis, Nicole J.; Cohen, Yaniv; Sanselicio, Stefano; Fumeaux, Coralie; Ozaki, Shogo; Luciano, Jennifer; Guerrero-Ferreira, Ricardo C.; Wright, Elizabeth R.; Jenal, Urs; Viollier, Patrick H.

In: Genes and Development, Vol. 27, No. 18, 01.09.2013, p. 2049-2062.

Research output: Contribution to journalArticle

Davis, NJ, Cohen, Y, Sanselicio, S, Fumeaux, C, Ozaki, S, Luciano, J, Guerrero-Ferreira, RC, Wright, ER, Jenal, U & Viollier, PH 2013, 'De- and repolarization mechanism of flagellar morphogenesis during a bacterial cell cycle', Genes and Development, vol. 27, no. 18, pp. 2049-2062. https://doi.org/10.1101/gad.222679.113
Davis, Nicole J. ; Cohen, Yaniv ; Sanselicio, Stefano ; Fumeaux, Coralie ; Ozaki, Shogo ; Luciano, Jennifer ; Guerrero-Ferreira, Ricardo C. ; Wright, Elizabeth R. ; Jenal, Urs ; Viollier, Patrick H. / De- and repolarization mechanism of flagellar morphogenesis during a bacterial cell cycle. In: Genes and Development. 2013 ; Vol. 27, No. 18. pp. 2049-2062.
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