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J. Biol. Chem., Vol. 283, Issue 23, 15558-15567, June 6, 2008

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The Influence of Iron on Pseudomonas aeruginosa Physiology

A REGULATORY LINK BETWEEN IRON AND QUORUM SENSING^*

Amanda G. Oglesby¹, John M. Farrow, III, Joon-Hee Lee^¶, Andrew P. Tomaras, E. P. Greenberg^||, Everett C. Pesci, and Michael L. Vasil

From the University of Colorado Denver, Aurora, Colorado 80231, the East Carolina University, Greenville, North Carolina 27858, the ^¶College of Pharmacy, Pusan National University, Pusan, 609-735, South Korea, and the ^||University of Washington School of Medicine, Seattle, Washington 98195

In iron-replete environments, the Pseudomonas aeruginosa Fur (ferric uptake regulator) protein represses expression of two small regulatory RNAs encoded by prrF1 and prrF2. Here we describe the effects of iron and PrrF regulation on P. aeruginosa physiology. We show that PrrF represses genes encoding enzymes for the degradation of anthranilate (i.e. antABC), a precursor of the Pseudomonas quinolone signal (PQS). Under iron-limiting conditions, PQS production was greatly decreased in a prrF1,2 mutant as compared with wild type. The addition of anthranilate to the growth medium restored PQS production to the prrF1,2 mutant, indicating that its defect in PQS production is a consequence of anthranilate degradation. PA2511 was shown to encode an anthranilate-dependent activator of the ant genes and was subsequently renamed antR. AntR was not required for regulation of antA by PrrF but was required for optimal iron activation of antA. Furthermore, iron was capable of activating both antA and antR in a prrF1,2 mutant, indicating the presence of two distinct yet overlapping pathways for iron activation of antA (AntR-dependent and PrrF-dependent). Additionally, several quorum-sensing regulators, including PqsR, influenced antA expression, demonstrating that regulation of anthranilate metabolism is intimately woven into the quorum-sensing network of P. aeruginosa. Overall, our data illustrate the extensive control that both iron regulation and quorum sensing exercise in basic cellular physiology, underlining how intermediary metabolism can affect the regulation of virulence factors in P. aeruginosa.

Received for publication, September 19, 2007 , and in revised form, April 18, 2008.

^* This work was supported, in whole or in part, by National Institutes of Health Grants R37-NIH AI15940 (to M. L. V.) and R01-AI46682 and 5R01-GM059026-09 (to E. P. G.). This work was also supported by the Korea Research Foundation Grant KRF-2007-331-C00222 funded by the Korean Government (to J.-H. L.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains two supplemental tables.

¹ To whom correspondence should be addressed: UCHSC, 12800 East 19th Ave., Mail Stop 8333, Aurora, CO 80045. Fax: 303-724-4226; E-mail: amanda.oglesby{at}uchsc.edu.

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