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Journal of Bacteriology, July 2005, p. 4792-4803, Vol. 187, No. 14
0021-9193/05/$08.00+0     doi:10.1128/JB.187.14.4792-4803.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

ExpR, a LuxR Homolog of Erwinia carotovora subsp. carotovora, Activates Transcription of rsmA, Which Specifies a Global Regulatory RNA-Binding Protein

Department of Plant Microbiology and Pathology,¹ Department of Chemistry, University of Missouri, Columbia, Missouri 65211²

Received 24 January 2005/ Accepted 18 April 2005

N-acyl homoserine lactone (AHL) is required by Erwinia carotovora subspecies for the expression of various traits, including extracellular enzyme and protein production and pathogenicity. Previous studies with E. carotovora subsp. carotovora have shown that AHL deficiency causes the production of high levels of RsmA, an RNA binding protein that functions as a global negative regulator of extracellular enzymes and proteins and secondary metabolites (Rsm, regulator of secondary metabolites). We document here that ExpR, a putative AHL receptor belonging to the LuxR family of regulators, activates RsmA production. In the absence of AHL, an ExpR⁺ E. carotovora subsp. carotovora strain compared to its ExpR^– mutant, produces higher levels of rsmA RNA and better expresses an rsmA-lacZ transcriptional fusion. Moreover, the expression of the rsmA-lacZ fusion in Escherichia coli is much higher in the presence of expR₇₁ (the expR gene of E. carotovora subsp. carotovora strain Ecc71) than in its absence. We also show that purified preparation of MBP-ExpR₇₁ binds (MBP, maltose binding protein) rsmA DNA. By contrast, MBP-ExpR₇₁ does not bind ahlI (gene for AHL synthase), pel-1 (gene for pectate lyase), or rsmB (gene for regulatory RNA that binds RsmA), nor does ExpR₇₁ activate expression of these genes. These observations strongly suggest transcriptional activation of rsmA resulting from a direct and specific interaction between ExpR₇₁ and the rsmA promoter. Several lines of evidence establish that N-3-oxohexanoyl-L-homoserine lactone (3-oxo-C6-HL), the major AHL analog produced by E. carotovora subsp. carotovora strain Ecc71, inhibits ExpR₇₁-mediated activation of rsmA expression. These findings for the first time establish that the expR effect in E. carotovora subsp. carotovora is channeled via RsmA, a posttranscriptional regulator of E. carotovora subspecies, and AHL neutralizes this ExpR effect.

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