From redox flow to gene regulation: role of the PrrC protein of Rhodobacter sphaeroides 2.4.1

Biochemistry. 2000 Feb 29;39(8):2052-62. doi: 10.1021/bi9923858.

Abstract

Activation of photosynthesis (PS) gene expression by the PrrBA two-component activation system in Rhodobacter sphaeroides 2.4.1 results from the interruption of an inhibitory signal originating from the cbb(3) cytochrome c oxidase via its interaction with oxygen, in conjunction with the Rdx redox proteins. The CcoQ protein, encoded by the ccoNOQP operon, which encodes the cbb(3) cytochrome c oxidase, was shown to act as a "transponder" that conveys the signal derived from reductant flow through cbb(3) to oxygen, to the Prr system. To further define the elements comprising this signal transduction pathway we considered the prrC gene product, which to date possessed no definable role in this signal transduction pathway despite its being part of the prrBCA gene cluster. Similar to mutations in cbb(3) and rdx, suitably constructed prrC deletion mutations lead to PS gene expression in the presence of high oxygen. Unlike mutations that remove cbb(3) terminal oxidase activity or Rdx function, the PrrC deletion mutant shows no effect upon cbb(3) activity, nor does it affect the ratio of the carotenoid (Crt) spheroidene (SE) to spheroidenone (SO). Thus, the PrrC deletion mutant behaves identically to the CcoQ deletion mutant. Taking these and previous results together, we suggest that PrrC is located upstream of the two-component PrrBA activation system in the signal transduction pathway but downstream of the cbb(3) cytochrome c oxidase and its "transponder" CcoQ. The PrrC deletion mutant was also shown to lead to an increase in the DorA protein under aerobic conditions as was shown earlier for the cbb(3) mutant. Finally, PrrC is a member of a highly conserved family of proteins found in both prokaryotes and eukaryotes, and this appears to be the first instance in which a direct regulatory role has been ascribed to a member of this protein family.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Alkaline Phosphatase / metabolism
  • Amino Acid Sequence
  • Bacterial Proteins / genetics*
  • Bacterial Proteins / metabolism*
  • Blotting, Northern
  • Electron Transport Complex IV / metabolism
  • Escherichia coli / metabolism
  • Escherichia coli Proteins*
  • Gene Deletion
  • Gene Expression Regulation, Bacterial*
  • Histidine Kinase
  • Immunoblotting
  • Iron-Sulfur Proteins*
  • Models, Biological
  • Models, Genetic
  • Molecular Sequence Data
  • Mutagenesis
  • Oxidation-Reduction*
  • Oxidoreductases / biosynthesis
  • Photosynthesis / genetics
  • Protein Biosynthesis
  • Protein Kinases / metabolism
  • Rhodobacter sphaeroides / genetics*
  • Rhodobacter sphaeroides / metabolism*
  • Ribonucleases / genetics*
  • Ribonucleases / metabolism*
  • Sequence Homology, Amino Acid
  • Signal Transduction
  • Trans-Activators*
  • beta-Galactosidase / metabolism

Substances

  • Bacterial Proteins
  • Escherichia coli Proteins
  • Iron-Sulfur Proteins
  • REGA protein, Rhodobacter sphaeroides
  • Trans-Activators
  • Oxidoreductases
  • dimethyl sulfoxide reductase
  • Electron Transport Complex IV
  • Protein Kinases
  • Histidine Kinase
  • PrrC protein, E coli
  • Ribonucleases
  • Alkaline Phosphatase
  • beta-Galactosidase