Transcriptomic dissection of the horizontally acquired response regulator EsrB reveals its global regulatory roles in the physiological adaptation and activation of T3SS and the cognate effector repertoire in<i>Edwardsiella piscicida</i>during infection toward turbot

Liu, Yang; Zhao, Luyao; Yang, Minjun; Yin, Kaiyu; Zhou, Xiaohui; Leung, Ka Yin; Liu, Qin; Zhang, Yuanxing; Wang, Qiyao

doi:10.1080/21505594.2017.1323157

Cited by 56 publications

(53 citation statements)

References 70 publications

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“…Three parallel RNA samples of each strain were sequenced using the illumina HiSeq (GENEWIZ, Suzhou, China). The subsequent procedures and statistical analysis were conducted as previously described in Reference [39].…”

Section: Rna-seq Analysismentioning

confidence: 99%

A GntR Family Transcription Factor (VPA1701) for Swarming Motility and Colonization of Vibrio parahaemolyticus

Meng

Yang

et al. 2019

Pathogens

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Motility is important for virulence, biofilm formation, and the environmental adaptation of many bacteria. Vibrio parahaemolyticus (V. parahaemolyticus) contains two flagellar systems that are responsible for motility, and are tightly regulated by transcription regulators and sigma factors. In this study, we identified a novel transcription factor, VPA1701, which regulates the swarming motility of V. parahaemolyticus. The VPA1701 deletion mutant (ΔVPA1701) eliminated the swarming motility on the surface of BHI agar plates and reduced colonization in infant rabbits. RNA-seq assays, confirmed by qRT-PCR, indicated that VPA1701 regulated the expression of lateral flagellar cluster genes. Further analyses revealed that VPA1701 directly binds to the promoter region of the flgBCDEFGHIJKL cluster to regulate the expression of lateral flagellar genes. CalR was originally identified as a repressor for the swarming motility of V. parahaemolyticus, and it was inhibited by calcium. In this study, we found that VPA1701 could inhibit the expression of the calR gene to increase the swarming motility of V. parahaemolyticus. Calcium downregulated the expression of calR, indicating that calcium could increase swarming motility of ΔVPA1701 by inhibiting calR. Thus, this study illustrates how the transcription factor VPA1701 regulates the expression of lateral flagellar genes and calR to control the swarming motility of V. parahaemolyticus.

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Section: Rna-seq Analysismentioning

confidence: 99%

A GntR Family Transcription Factor (VPA1701) for Swarming Motility and Colonization of Vibrio parahaemolyticus

Meng

Yang

et al. 2019

Pathogens

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“…Previous time-resolved TIS analysis indicates that ϳ540 and ϳ417 genes, respectively, are essential for E. piscicida grown in LB medium and in turbot (19). T3SS and T6SS genes are essential for in vivo colonization in the bacterium (11,(31)(32)(33). Here, T3SS genes linked in a genomic island and the nuoA-nuoN genes in the same cistron (6) were shown to be involved in the growth fitness in lower and higher temperatures of seawater ( Fig.…”

Section: Discussionmentioning

confidence: 70%

“…The growth of the mutants of the T6SS genes, i.e., evpP, evpC, and evpI, did not display significant differences in either 16 or 28°C seawater ( Fig. 3), suggesting that the enhanced survival resulting from the deletion of esrA, esrB, or esrC, encoding pivotal regulators for both T3SS and T6SS (10)(11)(12), might be associated with their regulatory roles in T3SS but not T6SS expression. Thus, these data validated the above TIS analysis.…”

Section: Resultsmentioning

confidence: 99%

“…E. piscicida is a member of the Enterobacteriaceae and has a broad host range, such as turbot, flounder, and ϳ20 other piscine species (9). The major virulence determinants are the type III secretion system (T3SS) and the T6SS in E. piscicida, and their expression is subjected to a complex regulatory network with involvement of the key regulators EsrA, EsrB, and EsrC (10)(11)(12) upon bacterial entrance of appropriate niches in the host. Little is known about how these virulence factors and other factors contribute to the environmental adaptation and survival for E. piscicida in a broad range of fish species, especially in some farmed marine fish (13).…”

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confidence: 99%

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Genome-Wide Identification of Fitness Factors in Seawater for Edwardsiella piscicida

Wei

Yang

et al. 2019

Appl Environ Microbiol

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Marine pathogens are transmitted from one host to another through seawater. Therefore, it is important for marine pathogens to maintain survival or growth in seawater. However, little is known about how marine pathogens adapt to living in seawater environments. Here, transposon insertion sequencing was performed to explore the genetic determinants of Edwardsiella piscicida survival in seawater at 16 and 28°C. Seventy-one mutants with mutations mainly in metabolism-, transportation-, and type III secretion system (T3SS)-related genes showed significantly increased or impaired fitness in 16°C water. In 28°C seawater, 63 genes associated with transcription and translation, as well as energy production and conversion, were essential for optimal survival of the bacterium. In particular, 11 T3SS-linked mutants displayed enhanced fitness in 16°C seawater but not in 28°C seawater. In addition, 13 genes associated with oxidative phosphorylation and 4 genes related to ubiquinone synthesis were identified for survival in 28°C seawater but not in 16°C seawater, which suggests that electron transmission and energy-producing aerobic respiration chain factors are indispensable for E. piscicida to maintain survival in higher-temperature seawater. In conclusion, we defined genes and processes related to metabolism and virulence that operate in E. piscicida to facilitate survival in low-and high-temperature seawater, which may underlie the infection outbreak mechanisms of E. piscicida and facilitate the development of improved vaccines against marine pathogens. IMPORTANCE Edwardsiella piscicida is one of the most important marine pathogens and causes serious edwardsiellosis in farmed fish during the summer-autumn seasonal changes, resulting in enormous losses to aquaculture industries worldwide. Survival and transmission of the pathogen in seawater are critical steps that increase the risk of outbreaks. To investigate the mechanism of survival in seawater for this marine pathogen, we used transposon insertion sequencing analysis to explore the fitness determinants in summer and autumn seawater. Approximately 127 genes linked to metabolism and virulence, as well as other processes, were revealed in E. piscicida to contribute to better adaptations to the seasonal alternations of seawater environments; these genes provide important insights into the infection outbreak mechanisms of E. piscicida and potential improved treatments or vaccines against marine pathogens. Expression of T3SS increased the fitness burden of E. piscicida survival in 16°Cseawater. E. piscicida did not normally grow in 28°C seawater after 24 h of incubation, probably due to the nutrient limitation in filtered natural seawater (Fig. 4A). Afterward, the survival of the WT strain dramatically decreased in 28°C seawater, particularly after 36 h of incubation (Fig. 4A). The survival capabilities of the esrA, esrB, esrC, and esaM FIG 3 Competitive index (CI) assays to validate the TIS data from the 16 and 28°C seawater. (A and B) The indicated strain was mixed with th...

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“…For RNA-seq analysis of the ΔrpoX or ΔrpoE strain, bacteria were incubated overnight and then diluted 1:100 in LBS medium. The bacteria were then grown at 42°C and harvested after 9 h. The subsequent procedures and statistical analysis were performed as previously described (32).…”

Section: Methodsmentioning

confidence: 99%

Alternative Sigma Factor RpoX Is a Part of the RpoE Regulon and Plays Distinct Roles in Stress Responses, Motility, Biofilm Formation, and Hemolytic Activities in the Marine Pathogen Vibrio alginolyticus

Zhang

Yuan

et al. 2019

Appl Environ Microbiol

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Vibrio alginolyticus is one of the most abundant microorganisms in marine environments and is also an opportunistic pathogen mediating high-mortality vibriosis in marine animals. Alternative sigma factors play essential roles in bacterial pathogens in the adaptation to environmental changes during infection and the adaptation to various niches, but little is known about them for V. alginolyticus. Our previous investigation indicated that the transcript level of the gene rpoX significantly decreased in an RpoE mutant. Here, we found that rpoX was highly expressed in response to high temperature and low osmotic stress and was under the direct control of the alternative sigma factor RpoE and its own product RpoX. Moreover, transcriptome sequencing (RNA-seq) results showed that RpoE and RpoX had different regulons, although they coregulated 105 genes at high temperature (42°C), including genes associated with biofilm formation, motility, virulence, regulatory factors, and the stress response. RNA-seq and chromatin immunoprecipitation sequencing (ChIP-seq) analyses as well as electrophoretic mobility shift assays (EMSAs) revealed the distinct binding motifs of RpoE and RpoX proteins. Furthermore, quantitative real-time reverse transcription-PCR (qRT-PCR) analysis also confirmed that RpoX can upregulate genes associated with flagella, biofilm formation, and hemolytic activities at higher temperatures. rpoX abrogation does not appear to attenuate virulence toward model fish at normal temperature. Collectively, data from this study demonstrated the regulatory cascades of RpoE and an alternative sigma factor, RpoX, in response to heat and osmotic stresses and their distinct and overlapping roles in pathogenesis and stress responses in the marine bacterium V. alginolyticus. IMPORTANCE The alternative sigma factor RpoE is essential for the virulence of Vibrio alginolyticus toward marine fish, coral, and other animals in response to sea surface temperature increases. In this study, we characterized another alternative sigma factor, RpoX, which is induced at high temperatures and under low-osmoticstress conditions. The expression of rpoX is under the tight control of RpoE and RpoX. Although RpoE and RpoX coregulate 105 genes, they are programming different regulatory functions in stress responses and virulence in V. alginolyticus. These findings illuminated the RpoE-RpoX-centered regulatory cascades and their distinct and overlapping regulatory roles in V. alginolyticus, which facilitates unraveling of the mechanisms by which the bacterium causes diseases in various sea animals in response to temperature fluctuations as well as the development of appropriate strategies to tackle infections by this bacterium.T he Gram-negative bacterium Vibrio alginolyticus is a halophilic bacterium that is mainly found in marine and estuarine environments, causing high-mortality outbreaks of vibriosis in sea animals; this bacterium is also a notorious foodborne pathogen for humans (1,2). Similar to other bacteria, the virulence of V. alginoly...

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Transcriptomic dissection of the horizontally acquired response regulator EsrB reveals its global regulatory roles in the physiological adaptation and activation of T3SS and the cognate effector repertoire inEdwardsiella piscicidaduring infection toward turbot

Cited by 56 publications

References 70 publications

A GntR Family Transcription Factor (VPA1701) for Swarming Motility and Colonization of Vibrio parahaemolyticus

A GntR Family Transcription Factor (VPA1701) for Swarming Motility and Colonization of Vibrio parahaemolyticus

Genome-Wide Identification of Fitness Factors in Seawater for Edwardsiella piscicida

Alternative Sigma Factor RpoX Is a Part of the RpoE Regulon and Plays Distinct Roles in Stress Responses, Motility, Biofilm Formation, and Hemolytic Activities in the Marine Pathogen Vibrio alginolyticus

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