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The Vibrio cholerae colonization factor GbpA possesses a modular structure that governs binding to different host surfaces.

ABSTRACT: Vibrio cholerae is a bacterial pathogen that colonizes the chitinous exoskeleton of zooplankton as well as the human gastrointestinal tract. Colonization of these different niches involves an N-acetylglucosamine binding protein (GbpA) that has been reported to mediate bacterial attachment to both marine chitin and mammalian intestinal mucin through an unknown molecular mechanism. We report structural studies that reveal that GbpA possesses an unusual, elongated, four-domain structure, with domains 1 and 4 showing structural homology to chitin binding domains. A glycan screen revealed that GbpA binds to GlcNAc oligosaccharides. Structure-guided GbpA truncation mutants show that domains 1 and 4 of GbpA interact with chitin in vitro, whereas in vivo complementation studies reveal that domain 1 is also crucial for mucin binding and intestinal colonization. Bacterial binding studies show that domains 2 and 3 bind to the V. cholerae surface. Finally, mouse virulence assays show that only the first three domains of GbpA are required for colonization. These results explain how GbpA provides structural/functional modular interactions between V. cholerae, intestinal epithelium and chitinous exoskeletons.

SUBMITTER: Wong E

PROVIDER: S-EPMC3257281 | biostudies-literature | 2012 Jan

REPOSITORIES: biostudies-literature

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The Vibrio cholerae colonization factor GbpA possesses a modular structure that governs binding to different host surfaces.

Wong Edmond E Vaaje-Kolstad Gustav G Ghosh Avishek A Hurtado-Guerrero Ramon R Konarev Peter V PV Ibrahim Adel F M AF Svergun Dmitri I DI Eijsink Vincent G H VG Chatterjee Nabendu S NS van Aalten Daan M F DM

PLoS pathogens 20120112 1

Vibrio cholerae is a bacterial pathogen that colonizes the chitinous exoskeleton of zooplankton as well as the human gastrointestinal tract. Colonization of these different niches involves an N-acetylglucosamine binding protein (GbpA) that has been reported to mediate bacterial attachment to both marine chitin and mammalian intestinal mucin through an unknown molecular mechanism. We report structural studies that reveal that GbpA possesses an unusual, elongated, four-domain structure, with domai ...[more]

PMID: 22253590

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Project description:Vibrio cholerae is an important human pathogen and environmental microflora species that can both propagate in the human intestine and proliferate in zooplankton and aquatic organisms. Cholera is transmitted through food and water. In recent years, outbreaks caused by V. cholerae-contaminated soft-shelled turtles, contaminated mainly with toxigenic serogroup O139, have been frequently reported, posing a new foodborne disease public health problem. In this study, the colonization by toxigenic V. cholerae on the body surfaces and intestines of soft-shelled turtles was explored. Preferred colonization sites on the turtle body surfaces, mainly the carapace and calipash of the dorsal side, were observed for the O139 and O1 strains. Intestinal colonization was also found. The colonization factors of V. cholerae played different roles in the colonization of the soft-shelled turtle's body surface and intestine. Mannose-sensitive hemagglutinin (MSHA) of V. cholerae was necessary for body surface colonization, but no roles were found for toxin-coregulated pili (TCP) or N-acetylglucosamine-binding protein A (GBPA). Both TCP and GBPA play important roles for colonization in the intestine, whereas the deletion of MSHA revealed only a minor colonization-promoting role for this factor. Our study demonstrated that V. cholerae can colonize the surfaces and the intestines of soft-shelled turtles and indicated that the soft-shelled turtles played a role in the transmission of cholera. In addition, this study showed that the soft-shelled turtle has potential value as an animal model in studies of the colonization and environmental adaption mechanisms of V. cholerae in aquatic organisms.IMPORTANCE Cholera is transmitted through water and food. Soft-shelled turtles contaminated with Vibrio cholerae (commonly the serogroup O139 strains) have caused many foodborne infections and outbreaks in recent years, and they have become a foodborne disease problem. Except for epidemiological investigations, no experimental studies have demonstrated the colonization by V. cholerae on soft-shelled turtles. The present studies will benefit our understanding of the interaction between V. cholerae and the soft-shelled turtle. We demonstrated the colonization by V. cholerae on the soft-shelled turtle's body surface and in the intestine and revealed the different roles of major V. cholerae factors for colonization on the body surface and in the intestine. Our work provides experimental evidence for the role of soft-shelled turtles in cholera transmission. In addition, this study also shows the possibility for the soft-shelled turtle to serve as a new animal model for studying the interaction between V. cholerae and aquatic hosts.

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The Vibrio cholerae colonization factor GbpA possesses a modular structure that governs binding to different host surfaces.

Publications

The Vibrio cholerae colonization factor GbpA possesses a modular structure that governs binding to different host surfaces.

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