Type VI secretion system-associated FHA domain protein TagH regulates the hemolytic activity and virulence of Vibrio cholerae

Wang, Guangli; Cheng, Fan; Wang, Hui; Jia, Chengyi; Li, Xiaoting; Yang, Jianru; Zhang, Tao; Gao, Song; Min, Xun; Huang, Jian

doi:10.1080/19490976.2022.2055440

Cited by 13 publications

(13 citation statements)

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“…Vibrio cholerae is classified into more than 200 serogroups based on surface O-antigens, among which the O1 and O139 serotypes are characterized as pathogenic strains responsible for cholera epidemics and pandemics, whereas non-O1/non-O139 V. cholerae (NOVC) produce no cholera toxins and consequently do not cause cholera ( Lekshmi et al, 2018 ). However, NOVC are now recognized as pathogens responsible for sporadic and local infectious outbreaks ( Xie et al, 2020 ), in which they can cause gastrointestinal infection ( Lee et al, 2007 ), as well as extra-intestinal disease, such as bacteremia ( Li et al, 2020b ; Wang et al, 2022 ), meningitis ( Hao et al, 2015 ), bacterial emphysema ( Marinello et al, 2017 ), and have even been associated with significant mortality ( Engel et al, 2016 ). Although in recent years, an increasing number of cases of NOVC infection have been reported, the pathogenic mechanisms of non-O1/non-O139 V. cholerae have yet to be sufficiently established.…”

Section: Introductionmentioning

confidence: 99%

DegS protease regulates the motility, chemotaxis, and colonization of Vibrio cholerae

et al. 2023

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In bacteria, DegS protease functions as an activating factor of the σE envelope stress response system, which ultimately activates the transcription of stress response genes in the cytoplasm. On the basis of high-throughput RNA sequencing, we have previously found that degS knockout inhibits the expression of flagellum synthesis- and chemotaxis-related genes, thereby indicating that DegS may be involved in the regulation of V. cholerae motility. In this study, we examined the relationships between DegS and motility in V. cholerae. Swimming motility and chemotaxis assays revealed that degS or rpoE deletion promotes a substantial reduction in the motility and chemotaxis of V. cholerae, whereas these activities were restored in ΔdegS::degS and ΔdegSΔrseA strains, indicating that DegS is partially dependent on σE to positively regulate V. cholerae activity. Gene-act network analysis revealed that the cAMP–CRP–RpoS signaling pathway, which plays an important role in flagellar synthesis, is significantly inhibited in ΔdegS mutants, whereas in response to the overexpression of cyaA/crp and rpoS in the ΔdegS strain, the motility and chemotaxis of the ΔdegS + cyaA/crp and ΔdegS + rpoS strains were partially restored compared with the ΔdegS strain. We further demonstrated that transcription levels of the flagellar regulatory gene flhF are regulated by DegS via the cAMP–CRP–RpoS signaling pathway. Overexpression of the flhF gene in the ΔdegS strain partially restored motility and chemotaxis. In addition, suckling mouse intestinal colonization experiments indicated that the ΔdegS and ΔrpoE strains were characterized by the poor colonization of mouse intestines, whereas colonization efficacy was restored in the ΔdegSΔrseA, ΔdegS + cyaA/crp, ΔdegS + rpoS, and ΔdegS + flhF strains. Collectively, our findings indicate that DegS regulates the motility and chemotaxis of V. cholerae via the cAMP–CRP–RpoS–FlhF pathway, thereby influencing the colonization of suckling mouse intestines.

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Section: Introductionmentioning

confidence: 99%

DegS protease regulates the motility, chemotaxis, and colonization of Vibrio cholerae

et al. 2023

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“…Our proteomic analysis also revealed that the immunity protein TsaB (14, 73), the innermembrane complex subunit VasK (74), and the FHA protein VasC (TagH), required for secretion (61), are more abundant in the presence of PmB. VasK (TssM) is part of the innermembrane complex (74) along with VasF (TssL) and VasD (TssJ), a complex randomly distributed in the membrane.…”

Section: Discussionmentioning

confidence: 79%

“…As expected, the main component of the T6SS syringe, Hcp (VC_1415, VC_A0017), was also more abundant (2.3 times) in the presence of PmB (46). VasC (VC_A0112), a cytoplasmic protein with an FHA domain essential for secretion (61), and ClpV (VC_A0116), the ATPase responsible for recycling of the contractile sheath, presented abundances that were 2.7 and 3.0 times higher in the presence of PmB, respectively. The abundance of VasK (VC_A0120), a part of the inner-membrane complex (62) was increased by 5.5 times by PmB (Table IV).…”

Section: Resultsmentioning

confidence: 99%

Comprehension of Antimicrobial Peptides Modulation of the Type VI Secretion System inVibrio cholerae

Mathieu-Denoncourt

Duperthuy

2022

Preprint

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The Type VI secretion System (T6SS) is a versatile weapon used by bacteria for virulence, resistance to grazing and competition with other bacteria. We previously demonstrated that the role of the T6SS in interbacterial competition and in resistance to grazing is enhanced in Vibrio cholerae in the presence of subinhibitory concentrations of polymyxin B (PmB). In this study, we performed a global quantitative proteomic analysis by liquid chromatography coupled to mass spectrometry and a transcriptomic analysis by quantitative PCR of the T6SS known regulators in V. cholerae grown with and without PmB. The proteome of V. cholerae is greatly modified in the presence of PmB at subinhibitory concentrations with more than 39 % of the identified cellular proteins displaying a difference in their abundance, including T6SS-related proteins (Hcp, VasC, TsaB and ClpV). We identified a regulator whose abundance and expression are increased in the presence of PmB, vxrB, the response regulator of the two-component system VxrAB. In a vxrAB deficient mutant, the expression of hcp measured by quantitative PCR, although globally reduced, was not modified in the presence of PmB, confirming its role in hcp upregulation with PmB. The upregulation of the T6SS in the presence of PmB appears to be, at least in part, due to the two-component system VxrAB.

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“…Manneh-Roussel et al ( 2018 ) reported that the cAMP receptor protein controled V. cholerae gene expression in response to host colonization. The hemolysin protein (Spots F527), expressed by V. cholerae J9-62 in C. auratus matrix, was considered as an important toxic factor of S. aureus , and V. cholerae toxicity (Liu et al, 2020 ; Wang et al, 2022 ).…”

Section: Discussionmentioning

confidence: 99%

Diverse Aquatic Animal Matrices Play a Key Role in Survival and Potential Virulence of Non-O1/O139 Vibrio cholerae Isolates

et al. 2022

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Vibrio cholerae can cause pandemic cholera in humans. The waterborne bacterium is frequently isolated from aquatic products worldwide. However, current literature on the impact of aquatic product matrices on the survival and pathogenicity of cholerae is rare. In this study, the growth of eleven non-O1/0O139 V. cholerae isolates recovered from eight species of commonly consumed fish and shellfish was for the first time determined in the eight aquatic animal matrices, most of which highly increased the bacterial biomass when compared with routine trypsin soybean broth (TSB) medium. Secretomes of the V. cholerae isolates (draft genome size: 3,852,021–4,144,013 bp) were determined using two-dimensional gel electrophoresis (2DE-GE) and liquid chromatography-tandem mass spectrometry (LC-MS/MS) techniques. Comparative secretomic analyses revealed 74 differential extracellular proteins, including several virulence- and resistance-associated proteins secreted by the V. cholerae isolates when grown in the eight matrices. Meanwhile, a total of 8,119 intracellular proteins were identified, including 83 virulence- and 8 resistance-associated proteins, of which 61 virulence-associated proteins were absent from proteomes of these isolates when grown in the TSB medium. Additionally, comparative genomic and proteomic analyses also revealed several strain-specific proteins with unknown functions in the V. cholerae isolates. Taken, the results in this study demonstrate that distinct secretomes and proteomes induced by the aquatic animal matrices facilitate V. cholerae resistance in the edible aquatic animals and enhance the pathogenicity of the leading waterborne pathogen worldwide.

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Type VI secretion system-associated FHA domain protein TagH regulates the hemolytic activity and virulence of Vibrio cholerae

Cited by 13 publications

References 71 publications

DegS protease regulates the motility, chemotaxis, and colonization of Vibrio cholerae

DegS protease regulates the motility, chemotaxis, and colonization of Vibrio cholerae

Comprehension of Antimicrobial Peptides Modulation of the Type VI Secretion System inVibrio cholerae

Diverse Aquatic Animal Matrices Play a Key Role in Survival and Potential Virulence of Non-O1/O139 Vibrio cholerae Isolates

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