Stress adaptation and virulence in Vibrio alginolyticus is mediated by two (p)ppGpp synthetase genes, relA and spoT

Yin, Wen-Liang; Zhang, Na; Xu, Hao; Gong, Xiaoxiao; Long, Heng; Ren, Wei; Zhang, Xiang; Cai, Xiaoni; Huang, Aiyou; Xie, Zhenyu

doi:10.1016/j.micres.2021.126883

Cited by 14 publications

(9 citation statements)

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“…There was no doubt that spoT played a critical role in synthesizing flagellum. Previous study revealed that the swimming ability of Δ relA Δ spoT decreased sharply ( Yin et al, 2021 ). Here we further investigated whether the absence of spoT would affect its swarming ability.…”

Section: Resultsmentioning

confidence: 99%

“…The (p)ppGpp synthetase gene mutants of V. alginolyticus HN08155 were generated by allelic exchange ( Milton et al, 1996 ). This method has been described in detail in our previous work ( Yin et al, 2021 ), and the oligonucleotides used in these procedures are listed in Supplementary Table 2 . In brief, the sucrose-sensitive suicide plasmid pDM4- relA containing the fusion product of a 542 bp upstream fragment and a 542 bp downstream fragment of relA coding sequence was introduced into E. coli β2163 cells by heat shock.…”

Section: Methodsmentioning

confidence: 99%

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Two (p)ppGpp Synthetase Genes, relA and spoT, Are Involved in Regulating Cell Motility, Exopolysaccharides Production, and Biofilm Formation of Vibrio alginolyticus

et al. 2022

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The stringent response mediated by the signal molecule (p)ppGpp is involved in response to multiple environmental stresses and control of various physiological processes. Studies have revealed that (p)ppGpp strongly affects the formation and maintenance of several bacterial biofilms. However, the specific regulatory roles of (p)ppGpp in biofilms, especially in the expression of genes related to cell motility and exopolysaccharides (EPSs) production, remain poorly understood. We recently reported two (p)ppGpp synthetase genes relA and spoT from the epizootic pathogen Vibrio alginolyticus. Herein, we found that the (p)ppGpp synthetase genes of V. alginolyticus contributed to biofilm formation at low cell density and biofilm detachment at high cell density, respectively, in polystyrene microtiter plates. Quantitative reverse transcription PCR (qRT-PCR) analysis revealed that the expression levels of both EPSs and motility associated genes were consistent with the development of biofilms. Besides, the (p)ppGpp synthetase gene spoT was found to be closely involved in the regulation of flagellum, smooth/translucent colony morphology and spotty pellicle at the air-liquid interface. Interestingly, pleiotropic phenotypes of ΔrelAΔspoT were similar to that of the rpoN (σ54) deletion mutant. Meanwhile, the absence of (p)ppGpp synthetase genes significantly reduced the expression levels of rpoN at low cell density, suggesting that (p)ppGpp may mediate the formation via positively affecting the alternative sigma factor RpoN. These findings allow us to propose (p)ppGpp as a crucial regulator for biofilm development in V. alginolyticus, in view of the regulatory roles of relA and spoT in cell motility and EPSs production.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Two (p)ppGpp Synthetase Genes, relA and spoT, Are Involved in Regulating Cell Motility, Exopolysaccharides Production, and Biofilm Formation of Vibrio alginolyticus

et al. 2022

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“…For example, Zhou et al recently revealed the role of pivotal virulence regulator ToxR in switching on the viable, but non-culturable state by sensing unfavorable environmental signals such as endogenous reactive oxygen species (hydrogen peroxide, H 2 O 2 ) in Vibrio alginolyticus , which infects humans and aquatic animals causing severe economic losses (Zhou et al, 2022 ). Yin et al ( 2021 ) provided evidence for putative roles of two (p)ppGpp synthetase genes ( relA and spoT ) attributing environmental adaption and virulence regulation in V. alginolyticus . A lipid II flippase MviN was found to mediate the regulation of environmental osmotic pressure on esrB of the EsrA-EsrB two-component system to control the virulence in the marine fish pathogen Edwardsiella piscicida (Yin et al, 2020b ).…”

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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“…Although colistin is the last resort for clinical treatment of multi-drug resistant Gram-negative bacteria infection, the continuous emergence of colistin-resistant bacteria posed a serious threat to the efficacy of antibiotic therapy ( Laplante et al, 2018 ; Huang et al, 2021 ; Jang et al, 2021 ). In addition, bacteria can be adapted to adverse and detrimental conditions through stress-triggered regulatory systems ( Yin et al, 2021 ; Dawan and Ahn, 2022 ), such as TCS, which has increased the difficulty of prevention and control of pathogenic bacteria. Numerous studies have identified EnvZ/OmpR functioning as a factor in bacterial survival and development in response to various harsh environments ( Chakraborty and Kenney, 2018 ; Gerken et al, 2020 ; Kunkle et al, 2020 ).…”

Section: Discussionmentioning

confidence: 99%

Contribution of the EnvZ/OmpR two-component system to growth, virulence and stress tolerance of colistin-resistant Aeromonas hydrophila

Gang

Zheng

et al. 2022

Front. Microbiol.

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Aeromonas hydrophila is an important zoonotic pathogen responsible for septicemia, diarrhea and gastroenteritis, and has attracted considerable attention. The EnvZ/OmpR two-component system (TCS) mediates environmental stress responses in gram-negative bacteria. We investigated the role of the TCS in A. hydrophila by comparing the characteristics of the parental (23-C-23), EnvZ/OmpR knockout (23-C-23:ΔEnvZ/OmpR), and complemented strains (23-C-23:CΔEnvZ/OmpR). Under non-stress conditions, the 23-C-23:ΔEnvZ/OmpR strain showed a significant decrease in growth rate compared to that of 23-C-23. Transcriptome and metabonomic analysis indicated that many metabolic pathways were remarkably affected in the ΔEnvZ/OmpR strain, including the TCA cycle and arginine biosynthesis. In addition, the virulence of the ΔEnvZ/OmpR strain was attenuated in a Kunming mouse model. The ΔEnvZ/OmpR strain exhibited notably reduced tolerance to environmental stresses, including high temperature, different pH conditions, oxidative stress, and high osmotic stress. The downregulated expression of genes related to cell metabolism, motility, and virulence in the ΔEnvZ/OmpR mutant strain was further validated by real-time quantitative PCR. Consequently, our data suggest that the EnvZ/OmpR TCS is required for growth, motility, virulence, and stress response in A. hydrophila, which has significant implications in the development of novel antibacterial and vaccine therapies targeting EnvZ/OmpR against A. hydrophila.

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Stress adaptation and virulence in Vibrio alginolyticus is mediated by two (p)ppGpp synthetase genes, relA and spoT

Cited by 14 publications

References 59 publications

Two (p)ppGpp Synthetase Genes, relA and spoT, Are Involved in Regulating Cell Motility, Exopolysaccharides Production, and Biofilm Formation of Vibrio alginolyticus

Two (p)ppGpp Synthetase Genes, relA and spoT, Are Involved in Regulating Cell Motility, Exopolysaccharides Production, and Biofilm Formation of Vibrio alginolyticus

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

Contribution of the EnvZ/OmpR two-component system to growth, virulence and stress tolerance of colistin-resistant Aeromonas hydrophila

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