Quorum Sensing Gene Regulation by LuxR/HapR Master Regulators in Vibrios

Ball, Alyssa S.; Chaparian, Ryan R.; Kessel, Julia C. van

doi:10.1128/jb.00105-17

Cited by 110 publications

(101 citation statements)

References 142 publications

(205 reference statements)

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“…While QS circuitry differs between organisms, the core function remains constant – to enable locally unified gene expression. The QS system of Vibrio harveyi , a significant marine pathogen, has been studied for decades and has yielded a wealth of knowledge about communication in Gram-negative bacteria (2–4). In this bacterium, three distinct AIs are produced intracellularly and diffuse into the local surroundings.…”

Section: Introductionmentioning

confidence: 99%

“…Once at quorum, LuxR is maximally expressed and gene expression programs are adjusted to produce group behaviors. This circuitry is conserved across vibrios, and LuxR/HapR-type proteins are the core regulators of genes at HCD in all vibrios, including the human pathogens Vibrio cholerae (HapR), Vibrio parahaemolyticus (OpaR), and Vibrio vulnificus (SmcR) (4).…”

Section: Introductionmentioning

confidence: 99%

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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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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Hierarchical transcriptional regulation of quorum-sensing genes inVibrio harveyi

Chaparian

Ball

Kessel

2020

Preprint

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“…At the end of this phosphorylation cascade at high cell density, the master transcription factor called LuxR is activated, which controls expression of hundreds of genes (6). LuxR is the name of the master transcription factor in Vibrio campbellii (previously called Vibrio harveyi ), whereas the homologs in other Vibrio species have different names: HapR ( V. cholerae ), SmcR ( Vibrio vulnificus ), and OpaR ( Vibrio parahaemolyticus ) (7). In V. cholerae , Δ hapR mutants are not competent, and this is due to HapR regulation of various competence genes, including comEA, comEC, qstR , and dns (1, 8, 9).…”

Section: Introductionmentioning

confidence: 99%

Diversity in natural transformation frequencies and regulation acrossVibriospecies

Simpson

Podicheti

Rusch

et al. 2019

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24In marine Vibrio species, chitin-induced natural transformation enables bacteria to take up DNA 25 from the external environment and integrate it into their genome via homologous recombination. 26Expression of the master competence regulator TfoX bypasses the need for chitin induction and 27 drives expression of the genes required for competence in several Vibrio species. Here, we 28 show that TfoX expression in two Vibrio campbellii strains, DS40M4 and NBRC 15631, enables 29 high frequencies of natural transformation. Conversely, transformation was not achieved in the 30 model quorum-sensing strain V. campbellii BB120 (previously classified as Vibrio harveyi).31 Surprisingly, we find that quorum sensing is not required for transformation in V. campbellii 55 Natural transformation is a physiological state in which bacteria are able to take up 56 extracellular DNA from the environment, transport it across the cell envelope, and integrate it 57 into their genome via homologous recombination. In marine Vibrio species, competence is 58 induced by growth on the chitinous exoskeletons of crustaceans (1, 2). This process has been 59 best studied in Vibrio cholerae (reviewed in (2)). Insoluble polysaccharide chitin is broken down 60 by secreted extracellular chitinases (3). Soluble chitin oligosaccharides ultimately induce 61 expression of the master competence regulator TfoX (4), which activates expression of 62 numerous components of the competence machinery required to take up extracellular DNA. In 63 addition to the chitin-sensing system, V. cholerae cells must also have a functional quorum- 64sensing system for natural transformation to be successful (1). Quorum sensing, the process of 65 cell-cell communication, allows bacterial cells to respond to changes in population density and 66 alter gene expression (5). The quorum-sensing systems in Vibrio species rely on detection of 67 extracellular autoinducers that are sensed by membrane-bound sensor kinases, which shuttle 68 phosphate to or away from the core response regulator LuxO at low cell density or high cell 69 density, respectively (5). At the end of this phosphorylation cascade at high cell density, the 70 master transcription factor called LuxR is activated, which controls expression of hundreds of 71 genes (6). LuxR is the name of the master transcription factor in Vibrio campbellii (previously 72 called Vibrio harveyi), whereas the homologs in other Vibrio species have different names:73 HapR (V. cholerae), SmcR (Vibrio vulnificus), and OpaR (Vibrio parahaemolyticus) (7). In V. 74 cholerae, DhapR mutants are not competent, and this is due to HapR regulation of various 75 competence genes, including comEA, comEC, qstR, and dns (1, 8, 9). HapR directly activates 76 qstR (encoding a transcriptional regulator) and represses dns (encoding an extracellular DNase) 77 (8). QstR subsequently activates downstream genes required for DNA uptake and integration, 78 such as comEA, comEC, and comM (10). The requirement for HapR for competence can be79 circumvented if qs...

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“…Deciphering the molecular mechanism for biofilm 1 development identified VpsR and cyclic-di-GMP mediated pathways as the key modulators in V. 2 cholerae (Hsieh et al, 2018). Biofilm formation by the pathogen is directly linked to its 3 pathogenesis (Silva and Benitez, 2016) and increased antibiotic resistance has been shown in Materials and methods 1 Selection of representative triterpenoid, bacterial strains and growth condition 2 Representative triterpenoids from each of the three major groups, namely betulinic acid (BA) 3 from lupine; glycyrrhetinic acid (GA) from β-amyrin and ursolic acid (UA) (Sigma) from ursane 4 families of triterpenoids were selected. For the studies batch cultures of Vibrio cholarae C6709 5 strains (bacterium O1, biotype El tor, serotype Inaba) were grown at 37°C with shaking in 6 Luria-Bertani (LB) or Mueller-Hinton medium (for antibiotic assays).…”

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confidence: 99%

“…Spectrum 100 and the spectra were obtained in the wave number range of 1000-3500 cm−1 using 23 Spectrum software. Total protein content was measured by adding trichloroacetic acid (TCA) 1 (final concentration, 12%) to the EPS solution, incubating the mixture on ice for 30 min before 2 centrifugation at 13000 rpm for 20 min. The TCA precipitates were washed twice with 10 ml 3 acetone and resuspended in 2 ml of 2-N-morpholinoethanesulfonic acid (MES) buffer (pH 5.0).…”

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confidence: 99%

A comprehensive and comparative study on the action of pentacyclic triterpenoids on Vibrio cholerae biofilms

Bhattacharya¹,

Bhattacharya²,

Şen³

2020

Preprint

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2 While serving as environmental reservoir for V. cholerae infection, biofilms are also crucial for 3 intestinal colonization of the pathogen. Triterpenoids, a group of bioactive phytochemicals, have 4 been tested for antibiofilm activity against model biofilm forming bacteria in recent times. In this 5 context, glycyrrhetinic acid (GRA), ursolic acid (UA) and betulinic acid (BA), representing three 6 categorically distinct groups of pentacyclic triterpenoids, are targeted for profiling their impact 7 on Vibrio cholerae C6709 biofilms. The triterpenoids substantially affected biofilm associated 8 attributes like formation, substratum adherence and dispersion from preformed biofilms. Though 9 at variable degree, the compounds decreased cell surface hydrophobicity and composition in 10 terms of macromolecular content. Not only EPS-associated extracellular enzyme activities were 11 estimated to be reduced by triterpenoid exposure, ultra structural analysis also revealed that 12 GRA, UA and BA can affect extracellular polymeric substance (EPS) content. Albeit total 13 extracellular proteolytic activity remained unaffected by the triterpenoids, GRA treatment 14 resulted in considerable reduction of extracellular gelatinase activity. Molecular docking analysis 15 indicated potential interaction with cyclic di-GMP sensor VpsT, autoinducer-2 sensor kinase 16 LuxP-LuxQ and transcriptional activator HapR, component of complex quorum sensing 17 networks modulating biofilm formation. Comprehensive analysis of antibiotic action revealed 18 accentuation of cephalosporin antibiotics with GRA and UA while BA potentiated action of 19 fluoroquinolones, widening the scope of combinatorial therapeutic strategy.20

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Quorum Sensing Gene Regulation by LuxR/HapR Master Regulators in Vibrios

Cited by 110 publications

References 142 publications

Hierarchical transcriptional regulation of quorum-sensing genes inVibrio harveyi

Hierarchical transcriptional regulation of quorum-sensing genes inVibrio harveyi

Diversity in natural transformation frequencies and regulation acrossVibriospecies

A comprehensive and comparative study on the action of pentacyclic triterpenoids on Vibrio cholerae biofilms

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