Reciprocal control of motility and biofilm formation by the PdhS2 two-component sensor kinase of Agrobacterium tumefaciens

Microbiology (Reading). 2019 Feb;165(2):146-162. doi: 10.1099/mic.0.000758. Epub 2019 Jan 8.

Abstract

A core regulatory pathway that directs developmental transitions and cellular asymmetries in Agrobacterium tumefaciens involves two overlapping, integrated phosphorelays. One of these phosphorelays putatively includes four histidine sensor kinase homologues, DivJ, PleC, PdhS1 and PdhS2, and two response regulators, DivK and PleD. In several different alphaproteobacteria, this pathway influences a conserved downstream phosphorelay that ultimately controls the phosphorylation state of the CtrA master response regulator. The PdhS2 sensor kinase reciprocally regulates biofilm formation and swimming motility. In the current study, the mechanisms by which the A. tumefaciens sensor kinase PdhS2 directs this regulation are delineated. PdhS2 lacking a key residue implicated in phosphatase activity is markedly deficient in proper control of attachment and motility phenotypes, whereas a kinase-deficient PdhS2 mutant is only modestly affected. A genetic interaction between DivK and PdhS2 is revealed, unmasking one of several connections between PdhS2-dependent phenotypes and transcriptional control by CtrA. Epistasis experiments suggest that PdhS2 may function independently of the CckA sensor kinase, the cognate sensor kinase for CtrA, which is inhibited by DivK. Global expression analysis of the pdhS2 mutant reveals a restricted regulon, most likely functioning through CtrA to separately control motility and regulate the levels of the intracellular signal cyclic diguanylate monophosphate (cdGMP), thereby affecting the production of adhesive polysaccharides and attachment. We hypothesize that in A. tumefaciens the CtrA regulatory circuit has expanded to include additional inputs through the addition of PdhS-type sensor kinases, likely fine-tuning the response of this organism to the soil microenvironment.

Keywords: Agrobacterium tumefaciens; biofilm; development; motility; phosphorelay; sensor kinase.

Publication types

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

MeSH terms

  • Agrobacterium tumefaciens / genetics
  • Agrobacterium tumefaciens / growth & development
  • Agrobacterium tumefaciens / metabolism
  • Agrobacterium tumefaciens / physiology*
  • Bacterial Adhesion
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Biofilms / growth & development*
  • Cyclic GMP / analogs & derivatives
  • Cyclic GMP / metabolism
  • Epistasis, Genetic
  • Gene Expression Regulation, Bacterial
  • Histidine Kinase / genetics
  • Histidine Kinase / metabolism*
  • Locomotion*
  • Mutation
  • Phosphorylation
  • Polysaccharides, Bacterial / biosynthesis
  • Signal Transduction
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Bacterial Proteins
  • Polysaccharides, Bacterial
  • Transcription Factors
  • bis(3',5')-cyclic diguanylic acid
  • Histidine Kinase
  • Cyclic GMP