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Repression of motility during fimbrial expression: identification of 14 mrpJ gene paralogues in Proteus mirabilis.

ABSTRACT: Proteus mirabilis alternates between motile and adherent forms. MrpJ, a transcriptional regulator previously reported to repress motility, is encoded at the 3' end of the mrp fimbrial operon in P. mirabilis. Sequencing of the P. mirabilis genome revealed 14 additional paralogues of mrpJ, 10 of which are associated with fimbrial operons. Twelve of these genes, when overexpressed, repressed motility; several distinct patterns of swarming motility were noted. Expression of 10 of the 14 mrpJ paralogues repressed flagellin (FlaA) synthesis. Alignment of the predicted amino acid sequences of MrpJ and its 14 paralogues revealed a conserved consensus motif (SQQQFSRYE) within the helix-turn-helix domain. Site-directed mutagenesis of these residues coupled with linker insertion mutagenesis of MrpJ confirmed the importance of this domain for repression of motility. Gel shift assays demonstrated that MrpJ and another paralogue UcaJ bind directly to the promoter region of the flagellar master regulator flhDC. Thus, P. mirabilis appears to use a related mechanism to inhibit motility during the production of at least 10 of its predicted fimbriae.

SUBMITTER: Pearson MM

PROVIDER: S-EPMC2572203 | biostudies-literature | 2008 Jul

REPOSITORIES: biostudies-literature

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Repression of motility during fimbrial expression: identification of 14 mrpJ gene paralogues in Proteus mirabilis.

Pearson Melanie M MM Mobley Harry L T HL

Molecular microbiology 20080701 2

Proteus mirabilis alternates between motile and adherent forms. MrpJ, a transcriptional regulator previously reported to repress motility, is encoded at the 3' end of the mrp fimbrial operon in P. mirabilis. Sequencing of the P. mirabilis genome revealed 14 additional paralogues of mrpJ, 10 of which are associated with fimbrial operons. Twelve of these genes, when overexpressed, repressed motility; several distinct patterns of swarming motility were noted. Expression of 10 of the 14 mrpJ paralog ...[more]

PMID: 18630347

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Project description:Proteus mirabilis contributes to a significant number of catheter-associated urinary tract infections, where coordinated regulation of adherence and motility is critical for ascending disease progression. Previously, the mannose-resistant Proteus-like (MR/P) fimbria-associated transcriptional regulator MrpJ has been shown to both repress motility and directly induce the transcription of its own operon; in addition, it affects the expression of a wide range of cellular processes. Interestingly, 14 additional mrpJ paralogs are included in the P. mirabilis genome. Looking at a selection of MrpJ paralogs, we discovered that these proteins, which consistently repress motility, also have nonidentical functions that include cross-regulation of fimbrial operons. A subset of paralogs, including AtfJ (encoded by the ambient temperature fimbrial operon), Fim8J, and MrpJ, are capable of autoinduction. We identified an element of the atf promoter extending from 487 to 655 nucleotides upstream of the transcriptional start site that is responsive to AtfJ, and we found that AtfJ directly binds this fragment. Mutational analysis of AtfJ revealed that its two identified functions, autoregulation and motility repression, are not invariably linked. Residues within the DNA-binding helix-turn-helix domain are required for motility repression but not necessarily autoregulation. Likewise, the C-terminal domain is dispensable for motility repression but is essential for autoregulation. Supported by a three-dimensional (3D) structural model, we hypothesize that the C-terminal domain confers unique regulatory capacities on the AtfJ family of regulators.Balancing adherence with motility is essential for uropathogens to successfully establish a foothold in their host. Proteus mirabilis uses a fimbria-associated transcriptional regulator to switch between these antagonistic processes by increasing fimbrial adherence while simultaneously downregulating flagella. The discovery of multiple related proteins, many of which also function as motility repressors, encoded in the P. mirabilis genome has raised considerable interest as to their functionality and potential redundancy in this organism. This study provides an important advance in this field by elucidating the nonidentical effects of these paralogs on a molecular level. Our mechanistic studies of one member of this group, AtfJ, shed light on how these differing functions may be conferred despite the limited sequence variety exhibited by the paralogous proteins.

Dataset Information

Repression of motility during fimbrial expression: identification of 14 mrpJ gene paralogues in Proteus mirabilis.

Publications

Repression of motility during fimbrial expression: identification of 14 mrpJ gene paralogues in Proteus mirabilis.

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