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J. Biol. Chem., Vol. 280, Issue 39, 33324-33330, September 30, 2005

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The EAL Domain Protein VieA Is a Cyclic Diguanylate Phosphodiesterase^*

Rita Tamayo, Anna D. Tischler, and Andrew Camilli, An investigator of the Howard Hughes Medical Institute.1

From the Howard Hughes Medical Institute and Tufts University School of Medicine and the Department of Molecular Biology and Microbiology, Tufts University, Boston, Massachusetts 02111

The newly recognized bacterial second messenger 3',5'-cyclic diguanylic acid (cyclic diguanylate (c-di-GMP)) has been shown to regulate a wide variety of bacterial behaviors and traits. Biosynthesis and degradation of c-di-GMP have been attributed to the GGDEF and EAL protein domains, respectively, based primarily on genetic evidence. Whereas the GGDEF domain was demonstrated to possess diguanylate cyclase activity in vitro, the EAL domain has not been tested directly for c-di-GMP phosphodiesterase activity. This study describes the analysis of c-di-GMP hydrolysis by an EAL domain protein in a purified system. The Vibrio cholerae EAL domain protein VieA has been shown to inversely regulate biofilm-specific genes (vps) and virulence genes (ctxA), presumably by decreasing the cellular pool of c-di-GMP. VieA was maximally active at neutral pH, physiological ionic strength, and ambient temperatures and demonstrated c-di-GMP hydrolytic activity with a K_m of 0.06 µM. VieA was unable to hydrolyze cGMP. The putative metal coordination site of the EAL domain, Glu¹⁷⁰, was demonstrated to be necessary for VieA activity. Furthermore, the divalent cations Mg²⁺ and Mn²⁺ were necessary for VieA activity; conversely, Ca²⁺ and Zn²⁺ were potent inhibitors of the VieA phosphodiesterase. Calcium inhibition of the VieA EAL domain provides a potential mechanism for regulation of c-di-GMP degradation.

Received for publication, June 15, 2005 , and in revised form, July 27, 2005.

^* This work was supported by National Institutes of Health Grant AI45746 (to A. C.) and Center for Gastroenterology Research on Absorptive and Secretory Processes, New England Medical Center, Grant P30DK34928. 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.

¹ To whom correspondence should be addressed: Dept. of Molecular Biology and Microbiology, Tufts University, 136 Harrison Ave., Boston, MA 02111. Tel.: 617-636-2144; Fax: 617-636-2175; E-mail: Andrew.camilli{at}tufts.edu.

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