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Journal of Bacteriology, November 2007, p. 8165-8178, Vol. 189, No. 22
0021-9193/07/$08.00+0     doi:10.1128/JB.00586-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

BifA, a Cyclic-Di-GMP Phosphodiesterase, Inversely Regulates Biofilm Formation and Swarming Motility by Pseudomonas aeruginosa PA14{triangledown} ,{dagger}

Sherry L. Kuchma,1 Kimberly M. Brothers,1 Judith H. Merritt,1 Nicole T. Liberati,2,3 Frederick M. Ausubel,2,3 and George A. O'Toole1*

Department of Microbiology and Immunology, Dartmouth Medical School, Room 505, Vail Building, North College Street, Hanover, New Hampshire 03755,1 Department of Genetics, Harvard Medical School, Boston, Massachusetts 02114,2 Department of Molecular Biology, Massachusetts General Hospital, Boston, Massachusetts 021143

Received 16 April 2007/ Accepted 11 June 2007

The intracellular signaling molecule, cyclic-di-GMP (c-di-GMP), has been shown to influence bacterial behaviors, including motility and biofilm formation. We report the identification and characterization of PA4367, a gene involved in regulating surface-associated behaviors in Pseudomonas aeruginosa. The PA4367 gene encodes a protein with an EAL domain, associated with c-di-GMP phosphodiesterase activity, as well as a GGDEF domain, which is associated with a c-di-GMP-synthesizing diguanylate cyclase activity. Deletion of the PA4367 gene results in a severe defect in swarming motility and a hyperbiofilm phenotype; thus, we designate this gene bifA, for biofilm formation. We show that BifA localizes to the inner membrane and, in biochemical studies, that purified BifA protein exhibits phosphodiesterase activity in vitro but no detectable diguanylate cyclase activity. Furthermore, mutational analyses of the conserved EAL and GGDEF residues of BifA suggest that both domains are important for the observed phosphodiesterase activity. Consistent with these data, the {Delta}bifA mutant exhibits increased cellular pools of c-di-GMP relative to the wild type and increased synthesis of a polysaccharide produced by the pel locus. This increased polysaccharide production is required for the enhanced biofilm formed by the {Delta}bifA mutant but does not contribute to the observed swarming defect. The {Delta}bifA mutation also results in decreased flagellar reversals. Based on epistasis studies with the previously described sadB gene, we propose that BifA functions upstream of SadB in the control of biofilm formation and swarming.

* Corresponding author. Mailing address: Department of Microbiology and Immunology, Dartmouth Medical School, Rm. 505, Vail Building, North College St., Hanover, NH 03755. Phone: (603) 650-1248. Fax: (603) 650-1245. E-mail: georgeo{at}dartmouth.edu

{triangledown} Published ahead of print on 22 June 2007.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

Journal of Bacteriology, November 2007, p. 8165-8178, Vol. 189, No. 22
0021-9193/07/$08.00+0     doi:10.1128/JB.00586-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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