Abstract
BackgroundBacterial lipoproteins have important functions in bacterial pathogenesis and physiology. In Campylobacter jejuni, a major foodborne pathogen causing gastroenteritis in humans, the majority of lipoproteins have not been functionally characterized. Previously, we showed by DNA microarray that CmeR, a transcriptional regulator repressing the expression of the multidrug efflux pump CmeABC, modulates the expression of a three-gene operon (cj0089, cj0090, and cj0091) encoding a cluster of lipoproteins in C. jejuni.Methodology/Principal FindingsIn this work, we characterized the function and regulation of the cj0089-cj0090-cj0091 operon. In contrast to the repression of cmeABC, CmeR activates the expression of the lipoprotein genes and the regulation is confirmed by immunoblotting using anti-Cj0089 and anti-Cj0091 antibodies. Gel mobility shift assay showed that CmeR directly binds to the promoter of the lipoprotein operon, but the binding is much weaker compared with the promoter of cmeABC. Analysis of different cellular fractions indicated that Cj0089 was associated with the inner membrane, while Cj0091 was located on the outer membrane. Inactivation of cj0091, but not cj0089, significantly reduced the adherence of C. jejuni to INT 407 cells in vitro, indicating that Cj0091 has a function in adherence. When inoculated into chickens, the Cj0091 mutant also showed a defect in early colonization of the intestinal tract, suggesting that Cj0091 contributes to Campylobacter colonization in vivo. It was also shown that Cj0091 was produced and immunogenic in chickens that were naturally infected by C. jejuni.Conclusion/SignificanceThese results indicate that the lipoprotein operon is subject to direct regulation by CmeR and that Cj0091 functions as an adhesion mechanism in C. jejuni and contributes to Campylobacter colonization of the intestinal tract in animal hosts.
Highlights
Campylobacter jejuni is a Gram-negative, curved or spirally shaped bacterium with a single, polar, unsheathed flagellum at one or both ends [1]
In a previous study comparing the global gene expression profiles of in vitro grown NCTC 11168 and its isogenic CmeR mutant using DNA microarray [26], we found that CmeR, which is a transcriptional repressor for the multidrug efflux pump CmeABC [27], functions as a pleiotropic regulator modulating the expression of multiple genes in C. jejuni NCTC 11168 [26]
The three genes encoding the cluster of lipoproteins are tandemly positioned in the chromosome of C. jejuni NCTC 11168 (Figure 1A). cj0089 and cj0090 are separated by 9 nucleotides, while cj0090 and cj0091 are separated by 23 nucleotides
Summary
Campylobacter jejuni is a Gram-negative, curved or spirally shaped bacterium with a single, polar, unsheathed flagellum at one or both ends [1]. It is a commensal organism existing in the intestinal tracts of a variety of wild and domestic animals, especially in birds. C. jejuni is a leading cause of acute diarrhea in humans worldwide [2]. Campylobacter infections can develop to Guillain-Barresyndrome (GBS), an autoimmune-mediated neurodegenerative disorder which causes acute neuromuscular paralysis [4]. In Campylobacter jejuni, a major foodborne pathogen causing gastroenteritis in humans, the majority of lipoproteins have not been functionally characterized. We showed by DNA microarray that CmeR, a transcriptional regulator repressing the expression of the multidrug efflux pump CmeABC, modulates the expression of a three-gene operon (cj0089, cj0090, and cj0091) encoding a cluster of lipoproteins in C. jejuni
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