Crystal structure of the outer membrane protein OmpU from<i>Vibrio cholerae</i>at 2.2 Å resolution

Li, Huanyu; Zhang, Weijiao; Dong, Changjiang

doi:10.1107/s2059798317017697

Cited by 21 publications

(24 citation statements)

References 26 publications

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“…Consistent with this hypothesis is the presence, within the soluble contents of the OMVs, of an activity that induces hemocyte trafficking; this activity acts like, but is not chemically identical to, peptidoglycan monomer (1,38). If OMVs are able to deliver soluble molecules in such a context-dependent manner, OmpU would be a plausible conduit, as it has two predicted structural gates and adaptively increases the frequency of its "closed" configuration under acidic conditions (63,104). Defining the soluble molecular contents of OMVs would inform our predictions of the physiological importance of these vesicles to host and bacterium and would likely improve our understanding of the variable mechanism of their biogenesis.…”

Section: Discussionmentioning

confidence: 88%

“…For instance, it is possible that epithelial cells in the light organ sense OMVs and emit a cytokine-like signal that attracts hemocytes to the appendages, an activity not unlike that reported in mammalian tissues (103). Physiologically, OmpU is described as a size-selective porin that dynamically dilates and constricts (61,63); however, to our knowledge, the specific substrates that pass through the pore under biologically relevant conditions remain unknown. Our work advances an understanding of the role of OMPs in the effector activity of OMVs.…”

Section: Discussionmentioning

confidence: 99%

“…Additionally, OMVs from several Vibrio species carry OmpU, a major Vibrio outer membrane protein (OMP). OmpU is annotated as a size-selective porin (27,(61)(62)(63)(64) that can act as a virulence factor (65)(66)(67)(68)(69), inducing a variety of innate immune responses in mammalian and invertebrate hosts (37,39,(70)(71)(72)(73).…”

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confidence: 99%

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Ambient pH Alters the Protein Content of Outer Membrane Vesicles, Driving Host Development in a Beneficial Symbiosis

et al. 2019

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Outer membrane vesicles (OMVs) are continuously produced by Gram-negative bacteria and are increasingly recognized as ubiquitous mediators of bacterial physiology. In particular, OMVs are powerful effectors in interorganismal interactions, driven largely by their molecular contents. These impacts have been studied extensively in bacterial pathogenesis but have not been well documented within the context of mutualism. Here, we examined the proteomic composition of OMVs from the marine bacterium Vibrio fischeri, which forms a specific mutualism with the Hawaiian bobtail squid, Euprymna scolopes. We found that V. fischeri upregulates transcription of its major outer membrane protein, OmpU, during growth at an acidic pH, which V. fischeri experiences when it transitions from its environmental reservoir to host tissues. We used comparative genomics and DNA pulldown analyses to search for regulators of ompU and found that differential expression of ompU is governed by the OmpR, H-NS, and ToxR proteins. This transcriptional control combines with nutritional conditions to govern OmpU levels in OMVs. Under a host-encountered acidic pH, V. fischeri OMVs become more potent stimulators of symbiotic host development in an OmpU-dependent manner. Finally, we found that symbiotic development could be stimulated by OMVs containing a homolog of OmpU from the pathogenic species Vibrio cholerae, connecting the role of a well-described virulence factor with a mutualistic element. This work explores the symbiotic effects of OMV variation, identifies regulatory machinery shared between pathogenic and mutualistic bacteria, and provides evidence of the role that OMVs play in animal-bacterium mutualism. IMPORTANCE Beneficial bacteria communicate with their hosts through a variety of means. These communications are often carried out by a combination of molecules that stimulate responses from the host and are necessary for development of the relationship between these organisms. Naturally produced bacterial outer membrane vesicles (OMVs) contain many of those molecules and can stimulate a wide range of responses from recipient organisms. Here, we describe how a marine bacterium, Vibrio fischeri, changes the makeup of its OMVs under conditions that it experiences as it goes from its free-living lifestyle to associating with its natural host, the Hawaiian bobtail squid. This work improves our understanding of how bacteria change their signaling profile as they begin to associate with their beneficial partner animals.

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Section: Discussionmentioning

confidence: 88%

Section: Discussionmentioning

confidence: 99%

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Ambient pH Alters the Protein Content of Outer Membrane Vesicles, Driving Host Development in a Beneficial Symbiosis

et al. 2019

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“…The OmpU protein is the most abundant outer membrane protein in V. cholerae. It is an important virulence factor involved in host-cell interaction and recognition, as well as being critical for the survival in the host body and in harsh environments [69]. The OmpU protein is involved in resistance to antimicrobial peptides in the gut [52].…”

Section: Discussionmentioning

confidence: 99%

Phenotypic and Genotypic Properties of Vibrio cholerae non-O1, non-O139 Isolates Recovered from Domestic Ducks in Germany

et al. 2020

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Vibrio cholerae non-O1, non-O139 bacteria are natural inhabitants of aquatic ecosystems and have been sporadically associated with human infections. They mostly lack the two major virulence factors of toxigenic V. cholerae serogroups O1 and O139 strains, which are the causative agent of cholera. Non-O1, non-O139 strains are found in water bodies, sediments, and in association with other aquatic organisms. Occurrence of these bacteria in fecal specimens of waterfowl were reported, and migratory birds likely contribute to the long-distance transfer of strains. We investigated four V. cholerae non-O1, non-O139 isolates for phenotypic traits and by whole genome sequencing (WGS). The isolates were recovered from organs of domestic ducks with serious disease symptoms. WGS data revealed only a distant genetic relationship between all isolates. The isolates harbored a number of virulence factors found in most V. cholerae strains. Specific virulence factors of non-O1, non-O139 strains, such as the type III secretion system (TTSS) or cholix toxin, were observed. An interesting observation is that all isolates possess multifunctional autoprocessing repeats-in-toxin toxins (MARTX) closely related to the MARTX of toxigenic El Tor O1 strains. Different primary sequences of the abundant OmpU proteins could indicate a significant role of this virulence factor. Phenotypic characteristics such as hemolysis and antimicrobial resistance (AMR) were studied. Three isolates showed susceptibility to a number of tested antimicrobials, and one strain possessed AMR genes located in an integron. Knowledge of the environmental occurrence of V. cholerae non-O1, non-O139 in Germany is limited. The source of the infection of the ducks is currently unknown. In the context of the ‘One Health’ concept, it is desirable to study the ecology of V. cholerae non-O1, non-O139, as it cannot be excluded that the isolates possess zoonotic potential and could cause infections in humans.

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“…This result contrasts with previous work in E. coli , where Schelling and Conti found that outer membrane porins do not effect prey susceptibility 38 . OmpU is the most abundant outer membrane protein in V. cholerae 39 and could have effects on early predator–prey interactions. B. bacteriovorus encodes 150 putative proteases 40 and may use these enzymes to degrade outer membrane proteins and invade the prey cells.…”

Section: Discussionmentioning

confidence: 99%

Vibrio cholerae motility exerts drag force to impede attack by the bacterial predator Bdellovibrio bacteriovorus

et al. 2018

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The bacterial predator Bdellovibrio bacteriovorus is evolved to attack and kill other bacteria, including the human intestinal pathogen Vibrio cholerae. Although B. bacteriovorus exhibit a broad prey range, little is known about the genetic determinants of prey resistance and sensitivity. Here we perform a genetic screen on V. cholerae and identify five pathways contributing to predation susceptibility. We find that the essential virulence regulators ToxR/S increase susceptibility to predation, as mutants of these genes are more resistant to predation. We observe by flow cytometry that lipopolysaccharide is a critical defense, as mutants lacking O-antigen are rapidly attacked by predatory B. bacteriovorus. Using polymer solutions to alter media viscosity, we find that when B. bacteriovorus attacks motile V. cholerae, increased drag forces slow its ability to prey. These results provide insights into key prey resistance mechanisms, and may be useful in the application of B. bacteriovorus in treating infections.

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Crystal structure of the outer membrane protein OmpU fromVibrio choleraeat 2.2 Å resolution

Cited by 21 publications

References 26 publications

Ambient pH Alters the Protein Content of Outer Membrane Vesicles, Driving Host Development in a Beneficial Symbiosis

Ambient pH Alters the Protein Content of Outer Membrane Vesicles, Driving Host Development in a Beneficial Symbiosis

Phenotypic and Genotypic Properties of Vibrio cholerae non-O1, non-O139 Isolates Recovered from Domestic Ducks in Germany

Vibrio cholerae motility exerts drag force to impede attack by the bacterial predator Bdellovibrio bacteriovorus

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