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J. Biol. Chem., Vol. 277, Issue 4, 2385-2395, January 25, 2002

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Chrysobactin-dependent Iron Acquisition in Erwinia chrysanthemi
FUNCTIONAL STUDY OF A HOMOLOG OF THE ESCHERICHIA COLI FERRIC ENTEROBACTIN ESTERASE^*

Lise Rauscher, Dominique Expert^§, Berthold F. Matzanke^¶, and Alfred X. Trautwein^¶**

From the  Laboratoire de Pathologie Végétale, UMR 217 Institut National de la Recherche Agronomique, Institut National Agronomique Paris-Grignon, Université Paris 6, 16 rue Claude Bernard, 75231 Paris Cedex 05, France and the ^¶ Medical University Lübeck, the  Institute of Physics and the ^** Isotope Laboratory, Ratzeburger Alle 160, D-23538 Lübeck, Germany

Under iron limitation, the plant pathogen Erwinia chrysanthemi produces the catechol-type siderophore chrysobactin, which acts as a virulence factor. It can also use enterobactin as a xenosiderophore. We began this work by sequencing the 5'-upstream region of the fct-cbsCEBA operon, which encodes the ferric chrysobactin receptor and proteins involved in synthesis of the catechol moiety. We identified a new iron-regulated gene (cbsH) transcribed divergently relative to the fct gene, the translated sequence of which is 45.6% identical to that of Escherichia coli ferric enterobactin esterase. Insertions within this gene interrupt the chrysobactin biosynthetic pathway by exerting a polar effect on a downstream gene with some sequence identity to the E. coli enterobactin synthase gene. These mutations had no effect on the ability of the bacterium to obtain iron from enterobactin, showing that a functional cbsH gene is not required for iron removal from ferric enterobactin in E. chrysanthemi. The cbsH-negative mutants were less able to utilize ferric chrysobactin, and this effect was not caused by a defect in transport per se. In a nonpolar cbsH-negative mutant, chrysobactin accumulated intracellularly. These defects were rescued by the cbsH gene supplied on a plasmid. The amino acid sequence of the CbsH protein revealed characteristics of the S9 prolyl oligopeptidase family. Ferric chrysobactin hydrolysis was detected in cell extracts from a cbsH-positive strain that was inhibited by diisopropyl fluorophosphate. These data are consistent with the fact that chrysobactin is a D-lysyl-L-serine derivative. Mössbauer spectroscopy of whole cells at various states of ⁵⁷Fe-labeled chrysobactin uptake showed that this enzyme is not required for iron removal from chrysobactin in vivo. The CbsH protein may therefore be regarded as a peptidase that prevents the bacterial cells from being intracellularly iron-depleted by chrysobactin.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AF011334.

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