Cell cycle transition from S-phase to G1 in Caulobacter is mediated by ancestral virulence regulators

Nat Commun. 2014 Jun 18;5:4081. doi: 10.1038/ncomms5081.

Abstract

Zinc-finger domain transcriptional regulators regulate a myriad of functions in eukaryotes. Interestingly, ancestral versions (MucR) from Alpha-proteobacteria control bacterial virulence/symbiosis. Whether virulence regulators can also control cell cycle transcription is unknown. Here we report that MucR proteins implement a hitherto elusive primordial S→G1 transcriptional switch. After charting G1-specific promoters in the cell cycle model Caulobacter crescentus by comparative ChIP-seq, we use one such promoter as genetic proxy to unearth two MucR paralogs, MucR1/2, as constituents of a quadripartite and homeostatic regulatory module directing the S→G1 transcriptional switch. Surprisingly, MucR orthologues that regulate virulence and symbiosis gene transcription in Brucella, Agrobacterium or Sinorhizobium support this S→G1 switch in Caulobacter. Pan-genomic ChIP-seq analyses in Sinorhizobium and Caulobacter show that this module indeed targets orthologous genes. We propose that MucR proteins and possibly other virulence regulators primarily control bacterial cell cycle (G1-phase) transcription, rendering expression of target (virulence) genes periodic and in tune with the cell cycle.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Base Sequence
  • Caulobacter / physiology*
  • Chromatin Immunoprecipitation
  • Dimerization
  • Electrophoretic Mobility Shift Assay
  • G1 Phase / genetics
  • G1 Phase / physiology*
  • Gene Expression Regulation, Bacterial / genetics
  • Gene Expression Regulation, Bacterial / physiology*
  • Immunoblotting
  • Models, Biological*
  • Molecular Sequence Data
  • Promoter Regions, Genetic / genetics
  • Real-Time Polymerase Chain Reaction
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • S Phase Cell Cycle Checkpoints / genetics
  • S Phase Cell Cycle Checkpoints / physiology*
  • Sequence Analysis, DNA
  • Species Specificity
  • beta-Galactosidase

Substances

  • Bacterial Proteins
  • Repressor Proteins
  • beta-Galactosidase

Associated data

  • GEO/GSE52849