Co-ordination of iron acquisition, iron porphyrin chelation and iron-protoporphyrin export via the cytochrome c biogenesis protein CcmC in Pseudomonas fluorescens

Microbiology. 2003 Dec;149(Pt 12):3543-3552. doi: 10.1099/mic.0.26566-0.

Abstract

The cytoplasmic membrane protein CcmC is, together with other Ccm proteins, a component for the maturation of c-type cytochromes in Gram-negative bacteria. A Pseudomonas fluorescens ATCC 17400 ccmC mutant is cytochrome c-deficient and shows considerably reduced production of the two siderophores pyoverdine and quinolobactin, paralleled by a general inability to utilize various iron sources, with the exception of haem. The ccmC mutant accumulates in a 5-aminolevulinic acid-dependent synthesis a reddish, fluorescent pigment identified as protoporphyrin IX. As a consequence a visA phenotype similar to that of a ferrochelatase-deficient hemH mutant characterized by drastically reduced growth upon light exposure was observed for the ccmC mutant. The defect of iron-protoporphyrin formation was further demonstrated by the failure of ccmC cell-free proteinase K-treated extracts to stimulate the growth of a haem auxotrophic hemH indicator strain, compared to similarly prepared wild-type extracts. In addition, the ccmC mutant did not sustain hemH growth in cross-feeding experiments while the wild-type did. Significantly reduced resistance to oxidative stress mediated by haem-containing catalases was observed for the ccmC mutant. A double hemH ccmC mutant could not be obtained in the presence of external haem without the hemH gene in trans, indicating that the combination of the two mutations is lethal. It was concluded that CcmC, apart from its known function in cytochrome c biogenesis, plays a role in haem biosynthesis. A function in the regulatory co-ordination of iron acquisition via siderophores, iron insertion into porphyrin via ferrochelatase and iron-protoporphyrin export for cytochrome c formation is predicted.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Base Sequence
  • Biological Transport, Active
  • Cytochromes c / metabolism*
  • DNA, Bacterial / genetics
  • Ferrochelatase / genetics
  • Ferrochelatase / metabolism
  • Genes, Bacterial
  • Heme / metabolism
  • Iron / metabolism*
  • Iron Chelating Agents / metabolism
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Models, Biological
  • Mutation
  • Oligopeptides*
  • Oxidative Stress
  • Phenotype
  • Pigments, Biological / metabolism
  • Porphyrins / metabolism
  • Protoporphyrins / metabolism
  • Pseudomonas fluorescens / genetics
  • Pseudomonas fluorescens / metabolism*
  • Quinolines*
  • Siderophores / metabolism

Substances

  • Bacterial Proteins
  • CcmC protein, bacteria
  • DNA, Bacterial
  • Iron Chelating Agents
  • Membrane Proteins
  • Oligopeptides
  • Pigments, Biological
  • Porphyrins
  • Protoporphyrins
  • Quinolines
  • Siderophores
  • quinolobactin
  • Heme
  • pyoverdin
  • Cytochromes c
  • Iron
  • Ferrochelatase