Tetrathionate stimulated growth of Campylobacter jejuni identifies a new type of bi-functional tetrathionate reductase (TsdA) that is widely distributed in bacteria

Mol Microbiol. 2013 Apr;88(1):173-88. doi: 10.1111/mmi.12176. Epub 2013 Mar 11.

Abstract

Tetrathionate (S4 O6 (2-) ) is used by some bacteria as an electron acceptor and can be produced in the vertebrate intestinal mucosa from the oxidation of thiosulphate (S2 O3 (2-) ) by reactive oxygen species during inflammation. Surprisingly, growth of the microaerophilic mucosal pathogen Campylobacter jejuni under oxygen-limited conditions was stimulated by tetrathionate, although it does not possess any known type of tetrathionate reductase. Here, we identify a dihaem cytochrome c (C8j_0815; TsdA) as the enzyme responsible. Kinetic studies with purified recombinant C. jejuni TsdA showed it to be a bifunctional tetrathionate reductase/thiosulphate dehydrogenase with a high affinity for tetrathionate. A tsdA null mutant still slowly reduced, but could not grow on, tetrathionate under oxygen limitation, lacked thiosulphate-dependent respiration and failed to convert thiosulphate to tetrathionate microaerobically. A TsdA paralogue (C8j_0040), lacking the unusual His-Cys haem ligation of TsdA, had low thiosulphate dehydrogenase and tetrathionate reductase activities. Our data highlight a hitherto unrecognized capacity of C. jejuni to use tetrathionate and thiosulphate in its energy metabolism, which may promote growth in the host. Moreover, as TsdA represents a new class of tetrathionate reductase that is widely distributed among bacteria, we predict that energy conserving tetrathionate respiration is far more common than currently appreciated.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aerobiosis / drug effects
  • Biocatalysis / drug effects
  • Campylobacter jejuni / cytology
  • Campylobacter jejuni / drug effects
  • Campylobacter jejuni / enzymology*
  • Campylobacter jejuni / growth & development*
  • Cytochromes c / metabolism
  • Electrons
  • Formates / pharmacology
  • Kinetics
  • Models, Biological
  • Mutation / genetics
  • NADH, NADPH Oxidoreductases / metabolism
  • Oxidation-Reduction / drug effects
  • Oxidoreductases / metabolism*
  • Oxygen / pharmacology
  • Recombinant Proteins / metabolism
  • Spectrum Analysis
  • Tetrathionic Acid / pharmacology*
  • Thiosulfates / pharmacology

Substances

  • Formates
  • Recombinant Proteins
  • Thiosulfates
  • Tetrathionic Acid
  • Cytochromes c
  • Oxidoreductases
  • NADH, NADPH Oxidoreductases
  • ferricyanide reductase
  • tetrathionate reductase
  • thiosulfate dehydrogenase
  • Oxygen