Anaerobic cysteine degradation and potential metabolic coordination in Salmonella enterica and Escherichia coli

Melissa Loddeke, Barbara Schneider, Tamiko Oguri, Iti Mehta, Zhenyu Xuan, Larry Reitzer

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

Salmonella enterica has two CyuR-activated enzymes that degrade cysteine, i.e., the aerobic CdsH and an unidentified anaerobic enzyme; Escherichia coli has only the latter. To identify the anaerobic enzyme, transcript profiling was performed for E. coli without cyuR and with overexpressed cyuR. Thirty-seven genes showed at least 5-fold changes in expression, and the cyuPA (formerly yhaOM) operon showed the greatest difference. Homology suggested that CyuP and CyuA represent a cysteine transporter and an iron-sulfur-containing cysteine desulfidase, respectively. E. coli and S. enterica ΔcyuA mutants grown with cysteine generated substantially less sulfide and had lower growth yields. Oxygen affected the CyuRdependent genes reciprocally; cyuP-lacZ expression was greater anaerobically, whereas cdsH-lacZ expression was greater aerobically. In E. coli and S. enterica, anaerobic cyuP expression required cyuR and cysteine and was induced by L-cysteine, D-cysteine, and a few sulfur-containing compounds. Loss of either CyuA or RidA, both of which contribute to cysteine degradation to pyruvate, increased cyuP-lacZ expression, which suggests that CyuA modulates intracellular cysteine concentrations. Phylogenetic analysis showed that CyuA homologs are present in obligate and facultative anaerobes, confirming an anaerobic function, and in archaeal methanogens and bacterial acetogens, suggesting an ancient origin. Our results show that CyuA is the major anaerobic cysteine-catabolizing enzyme in both E. coli and S. enterica, and it is proposed that anaerobic cysteine catabolism can contribute to coordination of sulfur assimilation and amino acid synthesis.

Original languageEnglish (US)
Article numbere00117-17
JournalJournal of Bacteriology
Volume199
Issue number16
DOIs
StatePublished - Aug 1 2017
Externally publishedYes

Fingerprint

Salmonella enterica
Cysteine
Escherichia coli
Enzymes
Sulfur Amino Acids
Scrapie
Sulfur Compounds
Sulfides
Operon
Pyruvic Acid
Sulfur
Genes
Iron
Oxygen

Keywords

  • Cysteine catabolism
  • Escherichia coli
  • Metabolism
  • Salmonella enterica

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

Anaerobic cysteine degradation and potential metabolic coordination in Salmonella enterica and Escherichia coli. / Loddeke, Melissa; Schneider, Barbara; Oguri, Tamiko; Mehta, Iti; Xuan, Zhenyu; Reitzer, Larry.

In: Journal of Bacteriology, Vol. 199, No. 16, e00117-17, 01.08.2017.

Research output: Contribution to journalArticle

Loddeke, Melissa ; Schneider, Barbara ; Oguri, Tamiko ; Mehta, Iti ; Xuan, Zhenyu ; Reitzer, Larry. / Anaerobic cysteine degradation and potential metabolic coordination in Salmonella enterica and Escherichia coli. In: Journal of Bacteriology. 2017 ; Vol. 199, No. 16.
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