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Virulence and Prodigiosin Antibiotic Biosynthesis in Serratia Are Regulated Pleiotropically by the GGDEF/EAL Domain Protein, PigX

Peter C. Fineran, Neil R. Williamson, Kathryn S. Lilley, and George P. C. Salmond^*

Department of Biochemistry, University of Cambridge, Cambridge CB2 1QW, United Kingdom

Received 28 April 2007/ Accepted 22 August 2007

Gram-negative bacteria of the genus Serratia are opportunistic human, plant, and insect pathogens. Serratia sp. strain ATCC 39006 secretes pectinases and cellulases and produces the secondary metabolites carbapenem and prodigiosin. Mutation of a gene (pigX) resulted in an extremely pleiotropic phenotype: prodigiosin antibiotic biosynthesis, plant virulence, and pectinase production were all elevated. PigX controlled secondary metabolism by repressing the transcription of the target prodigiosin biosynthetic operon (pigA-pigO). The transcriptional start site of pigX was determined, and pigX expression occurred in parallel with Pig production. Detailed quantitative intracellular proteome analyses enabled the identification of numerous downstream targets of PigX, including OpgG, mutation of which reduced the production of the plant cell wall-degrading enzymes and virulence. The highly pleiotropic PigX regulator contains GGDEF and EAL domains with noncanonical motifs and is predicted to be membrane associated. Genetic evidence suggests that PigX might function as a cyclic dimeric GMP phosphodiesterase. This is the first characterization of a GGDEF and EAL domain protein in Serratia and the first example of the regulation of antibiotic production by a GGDEF/EAL domain protein.

Published ahead of print on 31 August 2007.

These authors contributed equally to the manuscript.