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

Jason E Heindl, Daniel Crosby, Sukhdev Brar, John F Pinto, Tiyan Singletary, Daniel Merenich, Justin L Eagan, Aaron M Buechlein, Eric L Bruger, Christopher M Waters, Clay Fuqua
Author Information
  1. Jason E Heindl: 1���Department of Biology, Indiana University, Bloomington, IN 47405, USA.
  2. Daniel Crosby: 2���Department of Biological Sciences, University of the Sciences in Philadelphia, Philadelphia, PA 19104, USA.
  3. Sukhdev Brar: 2���Department of Biological Sciences, University of the Sciences in Philadelphia, Philadelphia, PA 19104, USA.
  4. John F Pinto: 2���Department of Biological Sciences, University of the Sciences in Philadelphia, Philadelphia, PA 19104, USA.
  5. Tiyan Singletary: 2���Department of Biological Sciences, University of the Sciences in Philadelphia, Philadelphia, PA 19104, USA.
  6. Daniel Merenich: 2���Department of Biological Sciences, University of the Sciences in Philadelphia, Philadelphia, PA 19104, USA.
  7. Justin L Eagan: 1���Department of Biology, Indiana University, Bloomington, IN 47405, USA.
  8. Aaron M Buechlein: 3���Center for Genomics and Bioinformatics, Indiana University, Bloomington, IN 47405, USA.
  9. Eric L Bruger: 4���Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824, USA.
  10. Christopher M Waters: 4���Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824, USA.
  11. Clay Fuqua: 1���Department of Biology, Indiana University, Bloomington, IN 47405, USA.

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

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Grants

  1. R03 AI130554/NIAID NIH HHS
  2. R01 GM109259/NIGMS NIH HHS
  3. R01 GM080546/NIGMS NIH HHS
  4. R01 GM120337/NIGMS NIH HHS
  5. F32 GM100601/NIGMS NIH HHS

MeSH Term

Agrobacterium tumefaciens
Bacterial Adhesion
Bacterial Proteins
Biofilms
Cyclic GMP
Epistasis, Genetic
Gene Expression Regulation, Bacterial
Histidine Kinase
Locomotion
Mutation
Phosphorylation
Polysaccharides, Bacterial
Signal Transduction
Transcription Factors

Chemicals

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

Word Cloud

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