VqsA, a Novel LysR-Type Transcriptional Regulator, Coordinates Quorum Sensing (QS) and Is Controlled by QS To Regulate Virulence in the Pathogen Vibrio alginolyticus

Gao, Xiating; Wang, Xuetong; Mao, Qiaoqiao; Xu, Rongjing; Zhou, Xiaohui; Ma, Yue; Liu, Qin; Zhang, Yuanxing; Wang, Qiyao

doi:10.1128/aem.00444-18

Cited by 24 publications

(12 citation statements)

References 49 publications

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“…AphA, another master regulator of QS, could also modulate the in vivo survival of V. alginolyticus in zebrafish [25]. In addition, QS was proved to control the activation of T6SS2 in V. alginolyticus [26,27]. Some studies also explored the role of other virulence factors in V. alginolyticus, but in general, most of the studies on V. alginolyticus in the last 20 years focused on virulence-related genes.…”

Section: Introductionmentioning

confidence: 99%

Mechanisms underlying the virulence regulation of new Vibrio alginolyticus ncRNA Vvrr1 with a comparative proteomic analysis

Zuo

Zhao

et al. 2019

Emerging Microbes & Infections

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The incidence of Vibrio alginolyticus infections has increased in recent years due to the influence of climate change and rising sea temperature. Vibrio virulence regulatory RNA 1 (Vvrr1) is a newly found noncoding RNA (ncRNA) predicted to be closely related to the adhesion ability of V. alginolyticus based on the previous RNA-seq. In this study, the target genes of Vvrr1 were fully screened and verified by constructing Vvrr1-overexpressing strains and using the proteome sequencing technology. Pyruvate kinase I (pykF) gene was predicted to be a chief target gene of Vvrr1 involved in virulence regulation. The adhesion ability, biofilm formation and virulence were significantly reduced in the Vvrr1-overexpressing and the pykFsilenced strain compared with the wild strains. Similar to the overexpression of Vvrr1, the silencing of pykF also reduced the expression level of virulence genes, such as ndk, eno, sdhB, glpF, and cysH. Meanwhile, by constructing the "pykF-GFP" fusion expression plasmid and using the GFP reporter gene analysis in Escherichia coli, the fluorescence intensity of the strain containing Vvrr1 whole ncRNA sequence vector was found to be significantly weakened. These indicated that Vvrr1 participated in the virulence regulation mechanism of V. alginolyticus by interacting with the virulence gene pykF.

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Section: Introductionmentioning

confidence: 99%

Mechanisms underlying the virulence regulation of new Vibrio alginolyticus ncRNA Vvrr1 with a comparative proteomic analysis

Zuo

Zhao

et al. 2019

Emerging Microbes & Infections

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“…Some transcription factors regulated by LuxR-type proteins have important connections to the quorum-sensing circuit in vibrios, including AphA in V. harveyi and VqsA in Vibrio alginolyticus. These regulators both feed back on the quorum-sensing system to regulate other components as follows: (i) AphA represses the Qrr small RNAs (sRNAs) and luxR and the Qrrs activate aphA, and (ii) VqsA activates luxR and represses aphA (3,49). Of note, V. harveyi does not appear to encode a VqsA homologue; the closest conserved gene product shares only 36% amino acid identity, and the gene is not regulated by LuxR (14, 15).…”

Section: Resultsmentioning

confidence: 99%

Hierarchical Transcriptional Control of the LuxR Quorum-Sensing Regulon of Vibrio harveyi

2020

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In vibrios, quorum sensing controls hundreds of genes that are required for cell density-specific behaviors including bioluminescence, biofilm formation, competence, secretion, and swarming motility. The central transcription factor in the quorum-sensing pathway is LuxR/HapR, which directly regulates ∼100 genes in the >400-gene regulon of Vibrio harveyi. Among these directly controlled genes are 15 transcription factors, which we predicted would comprise the second tier in the hierarchy of the LuxR regulon. We confirmed that LuxR binds to the promoters of these genes in vitro and quantified the extent of LuxR activation or repression of transcript levels. Transcriptome sequencing (RNA-seq) indicates that most of these transcriptional regulators control only a few genes, with the exception of MetJ, which is a global regulator. The genes regulated by these transcription factors are predicted to be involved in methionine and thiamine biosynthesis, membrane stability, RNA processing, c-di-GMP degradation, sugar transport, and other cellular processes. These data support a hierarchical model in which LuxR directly regulates 15 transcription factors that drive the second level of the gene expression cascade to influence cell density-dependent metabolic states and behaviors in V. harveyi. IMPORTANCE Quorum sensing is important for survival of bacteria in nature and influences the actions of bacterial groups. In the relatively few studied examples of quorum-sensing-controlled genes, these genes are associated with competition or cooperation in complex microbial communities and/or virulence in a host. However, quorum sensing in vibrios controls the expression of hundreds of genes, and their functions are mostly unknown or uncharacterized. In this study, we identify the regulators of the second tier of gene expression in the quorum-sensing system of the aquaculture pathogen Vibrio harveyi. Our identification of regulatory networks and metabolic pathways controlled by quorum sensing can be extended and compared to other Vibrio species to understand the physiology, ecology, and pathogenesis of these organisms.

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“…Some transcription factors regulated by LuxR have important connections to the quorum-sensing circuit in vibrios, including AphA in V. harveyi and VqsA in Vibrio alginolyticus . These regulators both feed back on the quorum-sensing system to regulate other components: 1) AphA represses the Qrr sRNAs and luxR , and the Qrrs activate aphA , and 2) VqsA activates luxR and represses aphA (3, 64). Of note, V. harveyi does not appear to encode a VqsA homolog; the closest conserved gene shares only 36% amino acid identity and is not regulated by LuxR (11, 12).…”

Section: Resultsmentioning

confidence: 99%

Hierarchical transcriptional regulation of quorum-sensing genes inVibrio harveyi

Chaparian

Ball

Kessel

2020

Preprint

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17In vibrios, quorum sensing controls hundreds of genes that are required for cell density-specific 18 behaviors including bioluminescence, biofilm formation, competence, secretion, and swarming 19 motility. The central transcription factor in the quorum-sensing pathway is LuxR/HapR, which 20 directly regulates ~100 genes in the >400-gene regulon of Vibrio harveyi. Among these directly 21 controlled genes are 15 transcription factors, which we predicted would comprise the second 22 tier in the hierarchy of the quorum-sensing regulon. We confirmed that LuxR binds to the 23 promoters of these genes in vitro and quantified the extent of LuxR activation or repression of 24 transcript levels. RNA-seq indicates that most of these transcriptional regulators control only a 25 few genes, with the exception of MetJ, which is a global regulator. The genes regulated by 26 these transcription factors are predicted to be involved in methionine and thiamine biosynthesis, 27 membrane stability, RNA processing, c-di-GMP degradation, sugar transport, and other cellular 28 processes. These data support a hierarchical model in which LuxR directly regulates 15 29 transcription factors that drive the second level of the gene expression cascade to influence cell 30 density-dependent metabolic states and behaviors in V. harveyi. 31 32 33 Importance 34 Quorum sensing is important for survival of bacteria in nature and influences the actions of 35 bacterial groups. In the relatively few studied examples of quorum sensing-controlled genes, 36 these genes are associated with competition or cooperation in complex microbial communities 37 and/or virulence in a host. However, quorum sensing in vibrios controls the expression of 38 hundreds of genes, and their functions are mostly unknown or uncharacterized. In this study, we 39 identify the regulators of the second-tier of gene expression in the quorum-sensing system of 40 the aquatic pathogen Vibrio harveyi. Our identification of regulatory networks and metabolic 41 pathways controlled by quorum sensing can be extended and compared to other Vibrio species 42 to understand the physiology, ecology, and pathogenesis of these organisms. 43 44 45 Introduction 46 47 Bacteria coordinate gene expression in response to an array of external stimuli including 48 nutrients, pH, and temperature. Other environmental cues that control gene expression are 49 autoinducers (AIs) -signaling molecules that are produced by bacterial communication systems 50 termed quorum sensing (QS) (1). In nature, bacteria live in complex microbial communities 51 where population-wide synchronization is critical for survival. While QS circuitry differs between 52 organisms, the core function remains constant -to enable locally unified gene expression. The 53 QS system of Vibrio harveyi, a significant marine pathogen, has been studied for decades and 54 has yielded a wealth of knowledge about communication in Gram-negative bacteria (2-4). In this 55 bacterium, three distinct AIs are produced intracellularly and diffuse into the ...

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VqsA, a Novel LysR-Type Transcriptional Regulator, Coordinates Quorum Sensing (QS) and Is Controlled by QS To Regulate Virulence in the Pathogen Vibrio alginolyticus

Cited by 24 publications

References 49 publications

Mechanisms underlying the virulence regulation of new Vibrio alginolyticus ncRNA Vvrr1 with a comparative proteomic analysis

Mechanisms underlying the virulence regulation of new Vibrio alginolyticus ncRNA Vvrr1 with a comparative proteomic analysis

Hierarchical Transcriptional Control of the LuxR Quorum-Sensing Regulon of Vibrio harveyi

Hierarchical transcriptional regulation of quorum-sensing genes inVibrio harveyi

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