The Independent cue and cus Systems Confer Copper Tolerance during Aerobic and Anaerobic Growth in Escherichia coli

F. Wayne Outten, David L. Huffman, Jeremy A. Hale, Thomas V. O'Halloran*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

365 Scopus citations

Abstract

Copper is essential but can be toxic even at low concentrations. Coping with this duality requires multiple pathways to control intracellular copper availability. Three copper-inducible promoters, controlling expression of six copper tolerance genes, were recently identified in Escherichia coli. The cue system employs an inner membrane copper transporter, whereas the cus system includes a tripartite transporter spanning the entire cell envelope. Although cus is not essential for aerobic copper tolerance, we show here that a copper-sensitive phenotype can be observed when cus is inactivated in a cueR background. Furthermore, a clear copper-sensitive phenotype for the cus system is revealed in the absence of O2. These results indicate that the cue pathway, which includes a copper exporter, CopA, and a periplasmic oxidase, CueO, is the primary aerobic system for copper tolerance. During anaerobic growth, however, copper toxicity increases, and the independent cus copper exporter is also necessary for full copper tolerance. We conclude that the cytosolic (CueR) and periplasmic (CusRS) sensor systems differentially regulate copper export systems in response to changes in copper and oxygen availability. These results underscore the increased toxicity of copper under anaerobic conditions and the complex adaptation of copper export in E. coli.

Original languageEnglish (US)
Pages (from-to)30670-30677
Number of pages8
JournalJournal of Biological Chemistry
Volume276
Issue number33
DOIs
StatePublished - Aug 17 2001

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Cell Biology

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