Control of the Type 3 Secretion System in
            <i>Vibrio harveyi</i>
            by Quorum Sensing through Repression of ExsA

Waters, Christopher M.; Wu, Julie Tsu-Yu; Ramsey, Meghan E.; Harris, Rebecca; Bassler, Bonnie L.

doi:10.1128/aem.00886-10

Cited by 40 publications

(55 citation statements)

References 47 publications

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“…5B). A previous study did not find that LuxR bound at the site predicted at position Ϫ63 in P B (25). We assume that this discrepancy is due to different EMSA reaction conditions.…”

Section: Apha and Luxr Directly Control Regulation Of The Ttss Genesmentioning

confidence: 70%

Individual and Combined Roles of the Master Regulators AphA and LuxR in Control of the Vibrio harveyi Quorum-Sensing Regulon

et al. 2013

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bBacteria use a chemical communication process called quorum sensing to control transitions between individual and group behaviors. In the Vibrio harveyi quorum-sensing circuit, two master transcription factors, AphA and LuxR, coordinate the quorum-sensing response. Here we show that AphA regulates 167 genes, LuxR regulates 625 genes, and they coregulate 77 genes. LuxR strongly controls genes at both low cell density and high cell density, suggesting that it is the major quorum-sensing regulator. In contrast, AphA is absent at high cell density and acts to fine-tune quorum-sensing gene expression at low cell density. We examined two loci as case studies of coregulation by AphA and LuxR. First, AphA and LuxR directly regulate expression of the genes encoding the quorum-regulatory small RNAs Qrr2, Qrr3, and Qrr4, the consequence of which is a specifically timed transition between the individual and the group life-styles. Second, AphA and LuxR repress type III secretion system genes but at different times and to different extents. The consequence of this regulation is that type III secretion is restricted to a peak at midcell density. Thus, the asymmetric production of AphA and LuxR coupled with differences in their strengths and timing of target gene regulation generate a precise temporal pattern of gene expression.

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“…5B). A previous study did not find that LuxR bound at the site predicted at position Ϫ63 in P B (25). We assume that this discrepancy is due to different EMSA reaction conditions.…”

Section: Apha and Luxr Directly Control Regulation Of The Ttss Genesmentioning

confidence: 70%

Individual and Combined Roles of the Master Regulators AphA and LuxR in Control of the Vibrio harveyi Quorum-Sensing Regulon

et al. 2013

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“…Although the expression of virulence factors at a low cell density rather than a high cell density seems inverse to the pattern for many pathogenic bacteria, this is the direction of control that is also observed for V. cholerae and V. harveyi. V. harveyi LuxR represses the expression of the T3SS master regulator exsA and prevents the secretion of virulence (26,66). Quorum control of virulence in V. cholerae is used to precisely tune the organism to a cycle of infection and dissemination.…”

Section: Discussionmentioning

confidence: 99%

“…There is some evidence that OpaR regulates T3SS1 (26) and that regulation of swarming and T3SS gene expression are linked (19,20). In Vibrio harveyi, LuxR has been demonstrated to repress the T3SS; it does so by directly binding the regulatory region controlling the expression of exsA, which encodes the master transcriptional regulator of the T3SS (26,66). In V. parahaemolyticus BB22, OpaR is inferred to work similarly, because a T3SS1 effector, VopD, could be detected in concentrated cell-free culture fluids prepared from a TR strain bearing an insertion in opaR, but could not be detected in the OP opaR ϩ strain, by using an antibody directed against V. harveyi VopD (26).…”

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confidence: 99%

“…V. parahaemolyticus OpaR and its V. harveyi ortholog LuxR have been found to negatively affect the secretion of the T3SS substrate VopD by immunoblotting of concentrated cellfree supernatants (26), and LuxR has been demonstrated to repress directly the exsBA operon of V. harveyi (66); however, neither the effects of OpaR on the entire T3SS1 regulon nor the biological significance of OpaR regulation with respect to virulence has been assessed. Genes encoding type III secretion components on chromosome 1 (T3SS1) were derepressed 4.7-to 13.6-fold in the ⌬opaR strain LM5674 compared to the opaR ϩ strains in the microarray analysis (see Table S1 in the supplemental material).…”

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confidence: 99%

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Quorum Sensing and Silencing in Vibrio parahaemolyticus

2011

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The quorum regulatory cascade is poorly characterized in Vibrio parahaemolyticus, in part because swarming and virulence factors-the hallmarks of the organism-are repressed by this scheme of gene control, and quorum sensing seems to be silenced in many isolates. In these studies, we examine a swarming-proficient, virulent strain and identify an altered-function allele of the quorum regulator luxO that is demonstrated to produce a constitutively active mimic of LuxOϳP. We find that LuxO* affects the expression of three small regulatory RNAs (Qrrs) and the activity of a translational fusion in opaR, the output regulator. Tests for epistasis showed that luxO* is dominant over luxO and that opaR is dominant over luxO. Thus, information flow through the central elements of the V. parahaemolyticus quorum pathway is proven for the first time. Quorumsensing output was explored using microarray profiling: the OpaR regulon encompasses ϳ5.2% of the genome. OpaR represses the surface-sensing and type III secretion system 1 (T3SS1) regulons. One novel discovery is that OpaR strongly and oppositely regulates two type VI secretion systems (T6SS). New functional consequences of OpaR control were demonstrated: OpaR increases the cellular cyclic di-GMP (c-di-GMP) level, positively controls chitin-induced DNA competency, and profoundly blocks cytotoxicity toward host cells. In expanding the previously known quorum effects beyond the induction of the capsule and the repression of swarming to elucidate the global scope of genes in the OpaR regulon, this study yields many clues to distinguishing traits of this Vibrio species; it underscores the profoundly divergent survival strategies of the quorum On/Off phase variants.Many members of the Vibrionaceae are well known for their capacities to communicate and to control group activities such as biofilm formation, virulence, and luminescence via cell-tocell signaling (reviewed in reference 48). However, quorum sensing has not been intensively investigated in Vibrio parahaemolyticus. This ubiquitous marine organism is the leading worldwide cause of seafood-borne gastroenteritis (43,47,60). Although its pathogenic strategies are not well understood, V. parahaemolyticus possesses a powerful arsenal of potential virulence factors, including proteases, hemolysins, two type VI secretion systems (T6SS1 and T6SS2), and two type III secretion systems (T3SS1 and TSS2) (37). The two T3SS, which are specially designed to inject effector virulence factors into eukaryotic host cells, have garnered much attention recently and have been shown to play distinct and critical roles in the pathogenicity of the organism (9, 27). Another hallmark of the organism is a marked proficiency at surface colonization, which is determined by its vigorous capacity to swarm and form robust biofilms (reviewed in reference 39). Our lack of knowledge about quorum sensing in V. parahaemolyticus stems in part from the fact that the archetypal V. parahaemolyticus strains appear defective in cell density-dependent regulation. S...

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“…T3SS are generally used to breach eukaryotic membranes, whereas T6SS can target both eukaryotic and prokaryotic membranes. In V. harveyi and V. parahaemolyticus, LuxR and OpaR repress expression of the T3SS operons, including those encoding the structural proteins, effector proteins, and the transcription factors in the system (41,49,135). Not only is the expression of T3SS vastly different between LCD and HCD in culture, but these operons are also highly upregulated during infection in a quorum sensing-dependent manner (71).…”

Section: Luxr/hapr Regulation Of Group Behaviors In Vibriosmentioning

confidence: 99%

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

2017

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The coordination of group behaviors in bacteria is accomplished via the cell-cell signaling process called quorum sensing. Vibrios have historically been models for studying bacterial communication due to the diverse and remarkable behaviors controlled by quorum sensing in these bacteria, including bioluminescence, type III and type VI secretion, biofilm formation, and motility. Here, we discuss the Vibrio LuxR/HapR family of proteins, the master global transcription factors that direct downstream gene expression in response to changes in cell density. These proteins are structurally similar to TetR transcription factors but exhibit distinct biochemical and genetic features from TetR that determine their regulatory influence on the quorum sensing gene network. We review here the gene groups regulated by LuxR/ HapR and quorum sensing and explore the targets that are common and unique among Vibrio species.

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Control of the Type 3 Secretion System in Vibrio harveyi by Quorum Sensing through Repression of ExsA

Cited by 40 publications

References 47 publications

Individual and Combined Roles of the Master Regulators AphA and LuxR in Control of the Vibrio harveyi Quorum-Sensing Regulon

Individual and Combined Roles of the Master Regulators AphA and LuxR in Control of the Vibrio harveyi Quorum-Sensing Regulon

Quorum Sensing and Silencing in Vibrio parahaemolyticus

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

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