Survival Characteristics and Transcriptomic Analyses Reveal the Adaptive Response of the Aquatic Pathogen Non-O1/O139 Vibrio cholerae to Starvation Stress

Gao, Xiaojian; Zhang, Zirui; Qian, Qieqi; Chen, Qiyun; Gu, Shuwen; Li, Jie; Zhang, Yingjie; Wu, Congcong; Jiang, Qun; Zhang, Xiaojun

doi:10.1128/spectrum.01939-21

Cited by 3 publications

(4 citation statements)

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“…regulate natural competence in V. cholereae Comparative analysis of qRT-PCR and transcriptome sequencing results of DEGs of V. mimicus before and after starvation stress. (Gao, et al, 2022). In our study, the size reduction in V. mimicus was also found after starvation, which might contribute to reduce the requirements for cell maintenance and to protect bacteria from environmental stress.…”

Section: Groupsupporting

confidence: 62%

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Survival virulent characteristics and transcriptomic analyses of Vibrio mimicus exposed to starvation

Jiang

Qian

et al. 2022

Front. Mar. Sci.

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Vibrio mimicus is a global causative agent of vibriosis in a variety of aquatic animals and causes major economic losses to aquaculture. It could survive in water for extended periods of time under environmental stress, but its survival strategy remains unknow. This study described the survival, virulent and gene expression changes of V. mimicus cells undergoing starvation stress. After 4 weeks’ cultivation in media without nutrients, V. mimicus Y4 showed reduced rates of activity with marked changes in morphology and physiological activities. The culturable cell counts declined gradually to 104 CFU/mL and the shape changed from rod-shaped to coccoid with short rods or spherical. The motility of starved cells decreased after starvation and the biofilm production was significantly lower than wild cells. The starved cells still produced β-hemolysis, lecithinase and caseinase, but its infectivity to Macrobrachium nipponense was weakened. To investigate the mechanism behind morphological and physiological changes, we further analyzed differently expressed genes (DEGs) between starved and wild cells at the whole transcriptional level. The RNA-seq analysis demonstrated that large-scale DEGs were involved in transferase, membrane, dehydrogenase, synthase, flagellar, hemolysin, pilus assembly, and starvation, etc. Among them, the well-known virulence-related genes were downregulated significantly, including vmh, pilA, vipA, capB, tadC, huvX, ompA, etc. These data provide a key resource to understand the regulatory mechanisms of V. mimicus to starvation stress.

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Section: Groupsupporting

confidence: 62%

“…Reportedly, flagellar assembly KEGG pathway was also downregulated in starved cells of V. cholerae (Gao, et al, 2022). Apart from motility, flagella can also influence biofilm formation by affecting bacterial adhesion (Choy et al, 2004).…”

Section: Groupmentioning

confidence: 97%

Survival virulent characteristics and transcriptomic analyses of Vibrio mimicus exposed to starvation

Jiang

Qian

et al. 2022

Front. Mar. Sci.

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“…It is well known that aquatic pathogenic bacteria are frequently subjected to a variety of stresses in the aquatic environments or host systems, and must adapt to survive in these environmental stresses, especially during infection ( Sun et al, 2016 ; Awan et al, 2018 ; Gao et al, 2018 , 2022 ). As a result, to investigate the environmental adaptation mechanism of bacterial pathogens, many studies focused to identify the key stress resistance related genes ( Kamareddine et al, 2018 ; Zhan et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

“…After incubating at 28°C for 1 h, the cultures were serially diluted and plated onto LB agar plates, colonies were counted after 24 h incubation. Additionally, the starvation stress assay was performed as described by Gao et al (2022) , the starved cells were sampled at day 7, 14, 21, and 28 for colonies counts. The survival rate was calculated as follows: (CFU of stressed cells/CFU of untreated cells) × 100%.…”

Section: Methodsmentioning

confidence: 99%

Transcriptomic and phenotype analysis revealed the role of rpoS in stress resistance and virulence of pathogenic Enterobacter cloacae from Macrobrachium rosenbergii

Gao

Qian²,

Zhu³

et al. 2022

Front. Microbiol.

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Enterobacter cloacae is widely distributed in the aquatic environment, and has been determined as a novel pathogen of various aquatic animals recently. Our previous studies have indicated E. cloacae caused repeated infections in Macrobrachium rosenbergii, suggesting a high survival ability of the bacteria, and rpoS gene has been known to regulate stress response and virulence of many bacteria. In this study, the E. cloacae-rpoS RNAi strain was constructed by RNAi technology, and the regulation role of rpoS in stress resistance and virulence of E. cloacae was explored by transcriptomic and phenotype analysis. The transcriptome analysis showed a total of 488 differentially expressed genes (DEGs) were identified between rpoS-RNAi and wild-type strains, including 30 up-regulated genes and 458 down-regulated genes, and these down-regulated DEGs were mainly related to environmental response, biofilm formation, bacterial type II secretory system, flagellin, fimbrillin, and chemotactic protein which associated with bacterial survival and virulence. The phenotype changes also showed the E. cloacae-rpoS RNAi strain exhibited significantly decreasing abilities of survival in environmental stresses (starvation, salinity, low pH, and oxidative stress), biofilm production, movement, adhesion to cells, pathogenicity, and colonization to M. rosenbergii. These results reveal that rpoS plays an important regulatory role in environmental stress adaptation and virulence of E. cloacae.

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Flagella-related gene mutations in Vibrio cholerae during extended cultivation in nutrient-limited media impair cell motility and prolong culturability

Okada,

Roobthaisong,

Hamada

2023

mSystems

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Understanding the survival strategies of pandemic cholera pathogens in aquatic environments is important for preventing their dissemination. Here, we report a phenomenon wherein long-term cultivation of Vibrio cholerae under nutrient-limited condition (M9 minimal medium supplemented with 0.2% glucose) causes mutations in flagella-related genes, thus inhibiting motility. Moreover, the motility defect reduced the transition of the viable but nonculturable state of the organisms. Maintenance of proliferative capability allows for the rapid population growth and prolonged survival in environments with nutrient sources. Diverse flagella-related genes, including flrA, flrC, flrD, flhA, flhF, fliD, fliF, fliG, fliH, fliI, fliP, fliQ, flgF, flgL, flgK, motX, and pomA, underwent mutations during the cultivation. However, only one gene (site) was mutated in a single V. cholerae . Longer cultivation for up to 300 days yielded further mutations in metabolism-related genes and the loss of virulence factors (e.g., CTX phage) and large DNA regions (~35 kb). These mutations were detected in most organisms of V. cholerae , accompanying the loss of genomic integrity. Motility-defective variants with mutations in the acetate kinase gene had become predominant in culturable cells after long-term cultivation in independently replicated experiments. These findings shed light on a survival mechanism in which V. cholerae adapts to an environmental niche by accumulating mutations. IMPORTANCE Vibrio cholerae undergoes a transition to a viable but non-culturable (VNC) state when subjected to various environmental stresses. We showed here that flagellar motility was involved in the development of the VNC state of V. cholerae . In this study, motility-defective isolates with mutations in various flagella-related genes, but not motile isolates, were predominantly obtained under the stress of long-term batch culture. Other genomic regions were highly conserved, suggesting that the mutations were selective. During the stationary phase of long-term culture, V. cholerae isolates with mutations in the acetate kinase and flagella-related genes were predominant. This study suggests that genes involved in specific functions in V. cholerae undergo mutations under certain environmental conditions.

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Survival Characteristics and Transcriptomic Analyses Reveal the Adaptive Response of the Aquatic Pathogen Non-O1/O139 Vibrio cholerae to Starvation Stress

Abstract: Non-O1/O139 V. cholerae is a causal agent of vibriosis that can be subject to nutrient insufficiency and cause high rates of mortality in aquatic animals. However, its molecular mechanisms of survival in response to starvation stress have been investigated only partially.

Cited by 3 publications

References 32 publications

Survival virulent characteristics and transcriptomic analyses of Vibrio mimicus exposed to starvation

Survival virulent characteristics and transcriptomic analyses of Vibrio mimicus exposed to starvation

Transcriptomic and phenotype analysis revealed the role of rpoS in stress resistance and virulence of pathogenic Enterobacter cloacae from Macrobrachium rosenbergii

Flagella-related gene mutations in Vibrio cholerae during extended cultivation in nutrient-limited media impair cell motility and prolong culturability

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