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Journal of Bacteriology, September 2004, p. 5826-5833, Vol. 186, No. 17
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.17.5826-5833.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Linkage between Catecholate Siderophores and the Multicopper Oxidase CueO in Escherichia coli

Gregor Grass,1,2 Keshari Thakali,1 Phillip E. Klebba,3 Daniel Thieme,2 Axel Müller,4 Günter F. Wildner,4 and Christopher Rensing1*

Department of Soil, Water, and Environmental Science, University of Arizona, Tucson, Arizona,1 Institute for Microbiology, Martin Luther University, Halle,2 Department of Biology, Ruhr University, Bochum, Germany,4 Department of Chemistry and Biochemistry, University of Oklahoma, Norman, Oklahoma3

Received 4 February 2004/ Accepted 21 May 2004

The multicopper oxidase CueO had previously been demonstrated to exhibit phenoloxidase activity and was implicated in intrinsic copper resistance in Escherichia coli. Catecholates can potentially reduce Cu(II) to the prooxidant Cu(I). In this report we provide evidence that CueO protects E. coli cells by oxidizing enterobactin, the catechol iron siderophore of E. coli, in the presence of copper. In vitro, a mixture of enterobactin and copper was toxic for E. coli cells, but the addition of purified CueO led to their survival. Deletion of fur resulted in copper hypersensitivity that was alleviated by additional deletion of entC, preventing synthesis of enterobactin. In addition, copper added together with 2,3-dihydroxybenzoic acid or enterobactin was able to induce a {Phi}(cueO-lacZ) operon fusion more efficiently than copper alone. The reaction product of the 2,3-dihydroxybenzoic acid oxidation by CueO that can complex Cu(II) ions was determined by gas chromatography-mass spectroscopy and identified as 2-carboxymuconate.

* Corresponding author. Mailing address: Department of Soil, Water, and Environmental Science, University of Arizona, Shantz Bldg. #38, Rm. 424, Tucson, AZ 85721. Phone: (520) 626-8482. Fax: (520) 621-1647. E-mail: rensingc{at}ag.arizona.edu.

Journal of Bacteriology, September 2004, p. 5826-5833, Vol. 186, No. 17
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.17.5826-5833.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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