Functional analysis of paralogous thiol-disulfide oxidoreductases in Streptococcus gordonii

J Biol Chem. 2013 Jun 7;288(23):16416-16429. doi: 10.1074/jbc.M113.464578. Epub 2013 Apr 24.

Abstract

Disulfide bonds are important for the stability of many extracellular proteins, including bacterial virulence factors. Formation of these bonds is catalyzed by thiol-disulfide oxidoreductases (TDORs). Little is known about their formation in Gram-positive bacteria, particularly among facultative anaerobic Firmicutes, such as streptococci. To investigate disulfide bond formation in Streptococcus gordonii, we identified five putative TDORs from the sequenced genome. Each of the putative TDOR genes was insertionally inactivated with an erythromycin resistance cassette, and the mutants were analyzed for autolysis, extracellular DNA release, biofilm formation, bacteriocin production, and genetic competence. This analysis revealed a single TDOR, SdbA, which exhibited a pleiotropic mutant phenotype. Using an in silico analysis approach, we identified the major autolysin AtlS as a natural substrate of SdbA and showed that SdbA is critical to the formation of a disulfide bond that is required for autolytic activity. Analysis by BLAST search revealed homologs to SdbA in other Gram-positive species. This study provides the first in vivo evidence of an oxidoreductase, SdbA, that affects multiple phenotypes in a Gram-positive bacterium. SdbA shows low sequence homology to previously identified oxidoreductases, suggesting that it may belong to a different class of enzymes. Our results demonstrate that SdbA is required for disulfide bond formation in S. gordonii and indicate that this enzyme may represent a novel type of oxidoreductase in Gram-positive bacteria.

Keywords: Autolysin; Disulfide Bond; Gram-positive; Microbiology; Oxidation-Reduction; Protein Folding; Streptococcus; Streptococcus gordonii; Thiol; Thiol-disulfide Oxidoreductase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Disulfides / metabolism*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mutation
  • N-Acetylmuramoyl-L-alanine Amidase / genetics
  • N-Acetylmuramoyl-L-alanine Amidase / metabolism
  • Protein Disulfide Reductase (Glutathione) / genetics
  • Protein Disulfide Reductase (Glutathione) / metabolism*
  • Streptococcus gordonii / enzymology*
  • Streptococcus gordonii / genetics
  • Virulence Factors / genetics
  • Virulence Factors / metabolism*

Substances

  • Bacterial Proteins
  • Disulfides
  • Membrane Proteins
  • SdbA protein, bacteria
  • Virulence Factors
  • Protein Disulfide Reductase (Glutathione)
  • N-Acetylmuramoyl-L-alanine Amidase