Structure, regulation, and host interaction of outer membrane protein U (OmpU) of Vibrio species

Ganie, Hilal A.; Choudhary, Aaina; Baranwal, Somesh

doi:10.1016/j.micpath.2021.105267

Cited by 16 publications

(9 citation statements)

References 53 publications

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“…For example, the OmpU is a major porin, which is highly conserved among Vibrio species. It facilitates movement of uncharged small molecules from the outer membrane to periplasmic space as well as involved in the adhesion/colonization of the bacteria ( 37 ). It has also been reported that in iron depletion, the expression of omp is downregulated as they act as a receptor of the siderophore complex and heme-compound transporter in V. cholerae ( 38 ).…”

Section: Resultsmentioning

confidence: 99%

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Unraveling the mechanistic insights of sophorolipid-capped gold nanoparticle-induced cell death in Vibrio cholerae

Shikha,

Kumar,

Jain

et al. 2023

Microbiol Spectr

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Cholera is one of the leading causes of mortality and morbidity worldwide. The treatment of cholera includes rehydration therapy, often combined with the administration of antibiotics (in severe cases). With the emergence and rapid spread of antimicrobial resistance, such microbial pathogens have become a compelling medical problem and a global threat. To combat the resistance to antibiotics, there is an urgent need for the discovery of novel and potent antimicrobial agents. The discovery of antimicrobial nanoparticles as an alternative to the existing antimicrobial regime has increased the hope for its use as one of the most promising tools against an array of microbial pathogens, including multidrug-resistant bacteria. Our recent report demonstrated that sophorolipid-capped gold nanoparticles (AuNPs-SL) exhibit potent antibacterial activity against Vibrio cholerae ; however, the killing mechanism remained obscure. Metal nanoparticle-mediated killing of microbes occurs through non-specific mechanisms. To develop antimicrobial nanoparticles with better efficacy, knowledge of their specific mechanism of action is essential. In this work, we deduced the mechanistic insights of AuNPs-SL mediated cell death of V. cholerae . We observed that AuNPs-SL treatment evokes reactive oxygen species (ROS) formation. The surge in the ROS level triggers the overexpression of ROS-responsive genes, depolarization of the membrane, change in membrane permeability and leakage of intracellular proteins and DNA, depletion of ATP levels in the cell, DNA damage, and subsequent cell death. This study shows the possibility of use of AuNPs-SL as an alternative potential antimicrobial agent. IMPORTANCE Vibrio cholerae , a Gram-negative bacterium, is the causative agent of a fatal disease, “cholera.” Prevention of cholera outbreak is possible by eliminating the bacteria from the environment. However, antimicrobial resistance developed in microorganisms has posed a threat and challenges to its treatment. Application of nanoparticles is a useful and effective option for the elimination of such microorganisms. Metal-based nanopaticles exhibit microbial toxicity through non-specific mechanisms. To prevent resistance development and increase antibacterial efficiency, rational designing of nanoparticles is required. Thus, knowledge on the exact mechanism of action of nanoparticles is highly essential. In this study, we explore the possible mechanisms of antibacterial activity of AuNPs-SL against V. cholerae . We show that the interaction of AuNPs-SL with V. cholerae enhances ROS production and membrane depolarization, change in permeability, and leakage of intracellular content. This action leads to the depletion of cellular ATP level, DNA damage, and subsequent cell death.

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Section: Resultsmentioning

confidence: 99%

“…Downregulation of ompU facilitates the selective entry of nanoparticles and may also control the free iron levels to slow down the Fenton reaction. Moreover, the downregulation of ompU is also an indicator of impaired cell evasion and biofilm formation ( 37 ). Biofilm formation requires cell-to-cell communication and quorum sensing.…”

Section: Resultsmentioning

confidence: 99%

Unraveling the mechanistic insights of sophorolipid-capped gold nanoparticle-induced cell death in Vibrio cholerae

Shikha,

Kumar,

Jain

et al. 2023

Microbiol Spectr

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“…The significance of OMPs in biofilm formation, structure, and function is emerging. OmpU is well-conserved across Vibrio species and is the most abundant and best-studied OMP in V. cholerae ( 56 ). OmpU confers resistance to host-derived antimicrobial peptides, and bile connects envelope stress to activation of the σE pathway, facilitates the adhesion of V. cholerae to mammalian cells, and modulates host immune responses ( 45 , 57 – 59 ).…”

Section: Discussionmentioning

confidence: 99%

Outer membrane vesicles and the outer membrane protein OmpU govern Vibrio cholerae biofilm matrix assembly

Potapova,

Garvey,

Dahl

et al. 2024

mBio

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Biofilms are matrix-encased microbial communities that increase the environmental fitness and infectivity of many human pathogens including Vibrio cholerae . Biofilm matrix assembly is essential for biofilm formation and function. Known components of the V. cholerae biofilm matrix are the polysaccharide Vibrio polysaccharide (VPS), matrix proteins RbmA, RbmC, Bap1, and extracellular DNA, but the majority of the protein composition is uncharacterized. This study comprehensively analyzed the biofilm matrix proteome and revealed the presence of outer membrane proteins (OMPs). Outer membrane vesicles (OMVs) were also present in the V. cholerae biofilm matrix and were associated with OMPs and many biofilm matrix proteins suggesting that they participate in biofilm matrix assembly. Consistent with this, OMVs had the capability to alter biofilm structural properties depending on their composition. OmpU was the most prevalent OMP in the matrix, and its absence altered biofilm architecture by increasing VPS production. Single-cell force spectroscopy revealed that proteins critical for biofilm formation, OmpU, the matrix proteins RbmA, RbmC, Bap1, and VPS contribute to cell-surface adhesion forces at differing efficiency, with VPS showing the highest efficiency whereas Bap1 showing the lowest efficiency. Our findings provide new insights into the molecular mechanisms underlying biofilm matrix assembly in V. cholerae , which may provide new opportunities to develop inhibitors that specifically alter biofilm matrix properties and, thus, affect either the environmental survival or pathogenesis of V. cholerae . IMPORTANCE Cholera remains a major public health concern. Vibrio cholerae , the causative agent of cholera, forms biofilms, which are critical for its transmission, infectivity, and environmental persistence. While we know that the V. cholerae biofilm matrix contains exopolysaccharide, matrix proteins, and extracellular DNA, we do not have a comprehensive understanding of the majority of biofilm matrix components. Here, we discover outer membrane vesicles (OMVs) within the biofilm matrix of V. cholerae . Proteomic analysis of the matrix and matrix-associated OMVs showed that OMVs carry key matrix proteins and Vibrio polysaccharide (VPS) to help build biofilms. We also characterize the role of the highly abundant outer membrane protein OmpU in biofilm formation and show that it impacts biofilm architecture in a VPS-dependent manner. Understanding V. cholerae biofilm formation is important for developing a better prevention and treatment strategy framework.

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“…It has a four-domain structure, and three of them are involved in the colonization process (Wong et al, 2012 ). Other adhesion factors such as OmpU and MAM7 are also identified in Vibrio species (including non-cholerae ones) and their role depends on the context of the pathogenic process (Liu et al, 2018 ; Crisan and Hammer, 2020 ; Ganie et al, 2022 ). The MAM7, T3SS, and T6SS are the main factors associated with V. cholerae, V. parahaemolyticus , and Vibrio alginolyticus , and T3SS has a little correlation with V. vulnificus ( Table 1 ).…”

Section: Pathogenic Mechanism Of Common Pathogenic Vibrio ...mentioning

confidence: 99%

Effects of intestinal microbiota on physiological metabolism and pathogenicity of Vibrio

Sun

Zhu

et al. 2022

Front. Microbiol.

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Vibrio species are disseminated broadly in the marine environment. Some of them can cause severe gastroenteritis by contaminating seafood and drinking water, such as Vibrio parahaemolyticus, Vibrio cholerae, and Vibrio vulnificus. However, their pathogenic mechanism still needs to be revealed to prevent and reduce morbidity. This review comprehensively introduces and discusses the common pathogenic process of Vibrio including adhesion, cell colonization and proliferation, and resistance to host immunity. Vibrio usually produces pathogenic factors including hemolysin, type-III secretion system, and adhesion proteins. Quorum sensing, a cell molecular communication system between the bacterial cells, plays an important role in Vibrio intestinal invasion and colonization. The human immune system can limit the virulence of Vibrio or even kill the bacteria through different responses. The intestinal microbiota is a key component of the immune system, but information on its effects on physiological metabolism and pathogenicity of Vibrio is seldom available. In this review, the effects of intestinal microorganisms and their metabolites on the invasion and colonization of common pathogenic Vibrio and VBNC status cells are discussed, which is conducive to finding the next-generation prebiotics. The strategy of dietary intervention is discussed for food safety control. Finally, future perspectives are proposed to prevent Vibrio infection in aquaculture.

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Structure, regulation, and host interaction of outer membrane protein U (OmpU) of Vibrio species

Cited by 16 publications

References 53 publications

Unraveling the mechanistic insights of sophorolipid-capped gold nanoparticle-induced cell death in Vibrio cholerae

Unraveling the mechanistic insights of sophorolipid-capped gold nanoparticle-induced cell death in Vibrio cholerae

Outer membrane vesicles and the outer membrane protein OmpU govern Vibrio cholerae biofilm matrix assembly

Effects of intestinal microbiota on physiological metabolism and pathogenicity of Vibrio

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