Activation of a signaling pathway by the physical translocation of a chromosome

Dev Cell. 2021 Aug 9;56(15):2145-2159.e7. doi: 10.1016/j.devcel.2021.06.014. Epub 2021 Jul 8.

Abstract

In every organism, the cell cycle requires the execution of multiple processes in a strictly defined order. However, the mechanisms used to ensure such order remain poorly understood, particularly in bacteria. Here, we show that the activation of the essential CtrA signaling pathway that triggers cell division in Caulobacter crescentus is intrinsically coupled to the initiation of DNA replication via the physical translocation of a newly replicated chromosome, powered by the ParABS system. We demonstrate that ParA accumulation at the new cell pole during chromosome segregation recruits ChpT, an intermediate component of the CtrA signaling pathway. ChpT is normally restricted from accessing the selective PopZ polar microdomain until the new chromosome and ParA arrive. Consequently, any disruption to DNA replication initiation prevents ChpT polarization and, in turn, cell division. Collectively, our findings reveal how major cell-cycle events are coordinated in Caulobacter and, importantly, how chromosome translocation triggers an essential signaling pathway.

Keywords: bacteria; cell cycle; cell polarity; chromosome segregation; signal transduction.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Caulobacter crescentus / genetics
  • Caulobacter crescentus / metabolism*
  • Cell Cycle / genetics
  • Cell Cycle / physiology
  • Cell Division / genetics
  • Chromosome Segregation / genetics
  • Chromosomes / genetics
  • DNA Replication / genetics
  • DNA Replication / physiology*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Protein Transport
  • Signal Transduction
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Translocation, Genetic / genetics

Substances

  • Bacterial Proteins
  • CtrA protein, Caulobacter
  • DNA-Binding Proteins
  • Transcription Factors