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Vanadium interferes with siderophore-mediated iron uptake in Pseudomonas aeruginosa

Laboratory of Microbial Interactions, Department of Immunology, Parasitology and Ultrastructure, Flanders Interuniversity Institute of Biotechnology and Vrije Universiteit Brussel, Paardenstraat 65, B-1640 Sint Genesius Rode, Belgium¹
University of Colorado Health Sciences Center, Microbiology, Box B-175, 4200 E Ninth Avenue, Denver, CO 80202, USA²
Laboratoire de Microbiologie et de Génétique, Université Louis Pasteur, UPRES-A 7010, F-67000 Strasbourg, France³
Institut für Organische Chemie der Universität zu Köln, Greinstrasse 4,D-50939 Köln, Germany⁴

Author for correspondence: Pierre Cornelis. Tel: +32 2 3590221. Fax: +32 2 3590390. e-mail: pcornel{at}vub.ac.be

Vanadium is a metal that under physiological conditions can exist in two oxidation states, V(IV) (vanadyl ion) and V(V) (vanadate ion). Here, it was demonstrated that both ions can form complexes with siderophores. Pseudomonas aeruginosa produces two siderophores under iron-limiting conditions, pyoverdine (PVD) and pyochelin (PCH). Vanadyl sulfate, at a concentration of 1–2 mM, strongly inhibited growth of P. aeruginosa PAO1, especially under conditions of severe iron limitation imposed by the presence of non-utilizable Fe(III) chelators. PVD-deficient mutants were more sensitive to vanadium than the wild-type, but addition of PVD did not stimulate their growth. Conversely, PCH-negative mutants were more resistant to vanadium than the wild-type strain. Both siderophores could bind and form complexes with vanadium after incubation with vanadyl sulfate (1:1, in the case of PVD; 2:1, in the case of PCH). Although only one complex with PVD, V(IV)–PVD, was found, both V(IV)– and V(V)–PCH were detected. V–PCH, but not V–PVD, caused strong growth reduction, resulting in a prolonged lag phase. Exposure of PAO1 cells to vanadium induced resistance to the superoxide-generating compound paraquat, and conversely, exposure to paraquat increased resistance to V(IV). Superoxide dismutase (SOD) activity of cells grown in the presence of V(IV) was augmented by a factor of two. Mutants deficient in the production of Fe-SOD (SodB) were particularly sensitive to vanadium, whilst sodA mutants deficient for Mn-SOD were only marginally affected. In conclusion, it is suggested that V–PCH catalyses a Fenton-type reaction whereby the toxic superoxide anion is generated, and that vanadium compromises PVD utilization.

Keywords: Pseudomonas, vanadium, siderophores, oxidative stress

Abbreviations: CAS, chrome azurol; EDDHA, ethylenediamine-di(o-hydroxyphenylacetic acid); ESI, electrospray ion; PCH, pyochelin; PVD, pyoverdine; SOD, superoxide dismutase

^a Present address: Brandwonden Centrum, Militair Hospitaal Koningin Astrid, B-1120 Brussels, Belgium.

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