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Applied and Environmental Microbiology, June 2008, p. 3461-3470, Vol. 74, No. 11
0099-2240/08/$08.00+0     doi:10.1128/AEM.02733-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

The Cyclic AMP-Dependent Catabolite Repression System of Serratia marcescens Mediates Biofilm Formation through Regulation of Type 1 Fimbriae{triangledown}

Eric J. Kalivoda,1 Nicholas A. Stella,1 Dawn M. O'Dee,2 Gerard J. Nau,2 and Robert M. Q. Shanks1,2*

Charles T. Campbell Laboratory of Ophthalmic Microbiology, Department of Ophthalmology, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania 15213,1 Department of Molecular Genetics and Biochemistry, University of Pittsburgh, Pittsburgh, Pennsylvania 152612

Received 4 December 2007/ Accepted 8 April 2008

The mechanisms by which environmental carbon sources regulate biofilm formation are poorly understood. This study investigates the roles of glucose and the catabolite repression system in Serratia marcescens biofilm formation. The abilities of this opportunistic pathogen to proliferate in a wide range of environments, to cause disease, and to resist antimicrobials are linked to its ability to form biofilms. We observed that growth of S. marcescens in glucose-rich medium strongly stimulated biofilm formation, which contrasts with previous studies showing that biofilm formation is inhibited by glucose in Escherichia coli and other enteric bacteria. Glucose uptake is known to inversely mediate intracellular cyclic AMP (cAMP) synthesis through regulation of adenylate cyclase (cyaA) activity, which in turn controls fundamental processes such as motility, carbon utilization and storage, pathogenesis, and cell division in many bacteria. Here, we demonstrate that mutation of catabolite repression genes that regulate cAMP levels (crr and cyaA) or the ability to respond to cAMP (crp) confers a large increase in biofilm formation. Suppressor analysis revealed that phenotypes of a cAMP receptor protein (crp) mutant require the fimABCD operon, which is responsible for type 1 fimbria production. Consistently, fimA transcription and fimbria production were determined to be upregulated in a cyaA mutant background by using quantitative real-time reverse transcription-PCR and transmission electron microscopy analysis. The regulatory pathway by which environmental carbon sources influence cAMP concentrations to alter production of type 1 fimbrial adhesins establishes a novel mechanism by which bacteria control biofilm development.

* Corresponding author. Mailing address: University of Pittsburgh, Dept. of Ophthalmology, EEI 1015, 203 Lothrop St., Pittsburgh, PA 15213. Phone: (412) 647-3537. Fax: (412) 647-5880. E-mail: shanksrm{at}upmc.edu

{triangledown} Published ahead of print on 18 April 2008.

Applied and Environmental Microbiology, June 2008, p. 3461-3470, Vol. 74, No. 11
0099-2240/08/$08.00+0     doi:10.1128/AEM.02733-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



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