CtrA Controls Cell Division and Outer Membrane Composition of the Pathogen Brucella abortus

Nayla Francis, Katy Poncin, Antonella Fioravanti, Victoria Vassen, Kevin Willemart, Thi Anh Phuong Ong, Luca Rappez, Jean-Jacques Letesson, Emanuele G Biondi, Xavier De Bolle

Research output: Contribution to journalArticlepeer-review

Abstract

Brucella abortus is a pathogen infecting cattle, able to survive, traffic, and proliferate inside host cells. It belongs to the Alphaproteobacteria, a phylogenetic group comprising bacteria with free living, symbiotic, and pathogenic lifestyles. An essential regulator of cell cycle progression named CtrA was described in the model bacterium Caulobacter crescentus. This regulator is conserved in many alphaproteobacteria, but the evolution of its regulon remains elusive. Here we identified promoters that are CtrA targets using ChIP-seq and we found that CtrA binds to promoters of genes involved in cell cycle progression, in addition to numerous genes encoding outer membrane components involved in export of membrane proteins and synthesis of lipopolysaccharide. Analysis of a conditional B. abortus ctrA loss of function mutant confirmed that CtrA controls cell division. Impairment of cell division generates elongated and branched morphologies, that are also detectable inside HeLa cells. Surprisingly, abnormal bacteria are able to traffic to the endoplasmic reticulum, the usual replication niche of B. abortus in host cells. We also found that CtrA depletion affected outer membrane composition, in particular the abundance and spatial distribution of Omp25. Control of the B. abortus envelope composition by CtrA indicates the plasticity of the CtrA regulon along evolution.

Original languageEnglish
Pages (from-to)780-797
Number of pages18
JournalMolecular Microbiology
Volume103
Issue number5
Early online date2016
DOIs
Publication statusPublished - Mar 2017

Keywords

  • Animals
  • Bacterial Outer Membrane Proteins/chemistry
  • Bacterial Proteins/genetics
  • Binding Sites
  • Brucella abortus/genetics
  • Cattle
  • Cell Cycle/genetics
  • Cell Division/genetics
  • DNA Replication
  • DNA-Binding Proteins/genetics
  • Endoplasmic Reticulum/microbiology
  • Gene Expression Regulation, Bacterial
  • Mutation
  • Phosphorylation
  • Phylogeny
  • Promoter Regions, Genetic
  • Regulon
  • Transcription Factors/genetics

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