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Quorum Sensing in Vibrio and Its Relevance to Bacterial Virulence iolog ter y & c P a a B r f a o s i l Journal of Bacteriology and t o Liu et al., J Bacteriol Parasitol 2013, 4:3 a l n o r g u DOI: 10.4172/2155-9597.1000172 y o J Parasitology ISSN: 2155-9597 Review Article Open Access Quorum Sensing in Vibrio and its Relevance to Bacterial Virulence Huan Liu1, Swaminath Srinivas2, Xiaoxian He1, Guoli Gong1, Chunji Dai1, Youjun Feng3,4,5#, Xuefeng Chen1# and Shihua Wang3#* 1College of Life Science & Engineering, Shaanxi University of Science & Technology, Xi’an 710021, China 2Department of Biochemistry, University of Illinois at Urbana-Champaign, IL61801, USA 3College of Life Sciences, Fujian Agriculture & Forestry University, Fuzhou 350002, China 4Institute of Microbiology, College of Life Science, Zhejiang University, Hangzhou 310058, China 5School of Molecular & Cellular Biology, University of Illinois, Urbana, IL 61801, USA #Equally contributed Abstract Quorum sensing is a widespread system of cell to cell communication in bacteria that is stimulated in response to population density and relies on hormone-like chemical molecules to control gene expression. In mutualistic marine organisms like Vibrio, this system enables them to express certain processes, like virulence, only when its impact as a group would be maximized. An N-acylhomoserine lactone-dependent LuxI/R quorum sensing system has first been exemplified inVibrio fischeri in the 1970s, regulating core bioluminescence genes. Since then, quorum sensing in Vibrio has been shown to influence a wide variety of process ranging from virulence factor formation to sporulation and motility. Most quorum sensing pathways produce and detect an autoinducer in a population dependent manner and transmit this information via a phospho-relay system to a core regulator that controls gene expression using certain pivotal elements. With several members of the genus Vibrio being known to cause severe foodborne infections, this review aims to present an overview of the quorum sensing systems present in four major Vibrio pathogens, V. fischeri, V. harveyi, V. cholerae and V. vulnificus and their roles in regulating the virulence of these organisms. Keywords: Quorum sensing; Vibrio; Pathogenicity; Autoinducer based on cell-density, including those for biofilm formation, motility, bioluminescence and virulence [7-10]. It is particularly interesting Introduction to see that quorum sensing plays an important role in controlling The genusVibrio is made up of some of the most ubiquitous bacteria the virulence of many Vibrio pathogens, implying that this pathway found in the marine ecosystem. Containing 91 different species, these could potentially be a target for compounds aimed at preventing and short rod shaped Gram-negative bacteria are found all over the world, managing vibriosis in the mariculture industry. in temperate to warm aquatic environments, ranging from off-shore In this short review, we concentrated on the different types of areas and estuaries to coastal waters. Some Vibrio species are found quorum sensing in several Vibrio species and also discussed their roles as a part of the normal marine flora or on the surface and/or in the in modulating the production of bacterial virulence factors. gastrointestinal tract of marine organisms like fish, shellfish, coral, sea grass, shrimp, and zooplankton while others are symbionts in light Quorum Sensing in V. fi scher i organs or even pathogens causing disease and death [1,2]. The epizootic Acyl-homoserine lactone (AHL) based quorum sensing was first bacterial disease caused by the genus Vibrio, termed vibriosis, brings observed to induce bioluminescence in a cell-population dependent about grievous economic loss to the worldwide aquaculture industry. fashion in the association between the marine bacterium V. fischeri It is, thus, essential to understand the virulence mechanisms and the and its symbiotic host, the Hawaiian bobtail squid [3]. The AHL underlying regulatory systems in these pathogens as part of an effort to responsible for this was found to be a species-specific metabolite, prevent and control vibriosis. N-(3-oxohexanoyl) homoserine lactone (N-3-oxo-HSL), termed as Bacteria were traditionally considered to be isolated microorganisms AI-1 [11]. AI-1 molecules are synthesized using S-adenosylmethionine living in a complex environment, a notion that has been squashed (SAM) and acyl carrier proteins (ACP) as substrates by the LuxI protein with the discovery of quorum sensing. Quorum sensing utilizes small [12]. This AI is detected by a transcriptional regulator, LuxR. At low cell “hormone-like” organic compounds referred to as autoinducers (AIs) densities and hence low AI concentrations, the N-terminal of LuxR folds to control gene expression in a population density-dependent manner. back onto its HTH domain and thus blocks DNA binding. However, This ensures that energetically expensive processes are not performed as the bacterial density increases with growth, these AIs accumulate in till their effect as a collective is maximized. The first example of such the growth medium via diffusion from inside the cell. The N-terminal a cell to cell communication system was elucidated in the marine region of LuxR can then specifically bind the AIs with a high affinity, bacterium Vibrio fischeri [3] controlling genes for bioluminescence. making its HTH domain available for DNA binding and consequently A typical quorum sensing system in Gram-negative bacteria has two types of AIs: acylated homoserine lactones (AI-1) and furanosyl borate diester (AI-2). AI-1 is considered to be an intra-species communication *Corresponding author: Shihua Wang, College of Life Sciences, Fujian Agriculture & signal molecule due to its distinct structure in various species while, Forestry University, Fuzhou 350002, China, E-mail: [email protected] in contrast, AI-2 produced by LuxS is believed to be an inter-species communication autoinducer [4,5]. In addition, there is a unique AI, Received July 18, 2013; Accepted August 06, 2013; Published August 12, 2013 3-hydroxytridecan-4-one (CAI-1), found only in Vibrio which is Citation: Liu H, Srinivas S, He X, Gong G, Dai C, et al. (2013) Quorum Sensing supposedly responsible for communication amongst Vibrio species in Vibrio and its Relevance to Bacterial Virulence. J Bacteriol Parasitol 4: 172. doi:10.4172/2155-9597.1000172 [6]. Following intensive investigation of the quorum sensing system in Vibrio, it has subsequently been demonstrated that quorum sensing Copyright: © 2013 Liu H, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted is present universally in both Gram-negative and Gram-positive use, distribution, and reproduction in any medium, provided the original author and bacteria and is used to regulate the expression of a vast range of genes source are credited. J Bacteriol Parasitol ISSN:2155-9597 JBP an open access journal Volume 4 • Issue 3 • 1000172 Citation: Liu H, Srinivas S, He X, Gong G, Dai C, et al. (2013) Quorum Sensing in Vibrio and its Relevance to Bacterial Virulence. J Bacteriol Parasitol 4: 172. doi:10.4172/2155-9597.1000172 Page 2 of 6 activating transcription of the bioluminescence genes, luxICDABE [13]. AI-I AI-2 CAI-I The LuxI-LuxR system is found widely and is the paradigm of quorum sensing in many Gram-negative bacteria. OM LuxN LuxP CqsS Subsequent research has demonstrated that there are two other IM quorum sensing systems in V. fischeri, AinS-AinR and LuxS-LuxPQ. LuxM LuxS LuxQ CqsA AinS synthesizes a novel AHL autoinducer, N-octanoyl-L-homoserine (C8-HSL) which then interacts with its cognate receptor kinase AinR [14,15]. LuxS synthesizes the furanosyl borate diester (AI-2) LuxU that is responsible for interspecies information dissemination [16]. AI-2 can bind to the periplasmic protein LuxP to form a LuxP-AI-2 LuxO σ54 complex, which is then sensed by the hybrid sensor kinase LuxQ. At a low cell density, in the absence of the corresponding autoinducers, Qrr1-5 both AinR and LuxQ function as kinases and first autophosphorylate. Hfq The phosphoryl group then transfers in sequence to the shared histine phosphotransferase protein LuxU and then to LuxO. The LuxR 54 phosphorylated LuxO cooperates with σ to activate transcription Bioluminescence Target genes of the small regulatory RNA, Qrr1, which subsequently silences LitR Other genes (homologue to LuxR in V. har vey i) expression in the presence of the Figure 2: Quorum sensing in V. harveyi. chaperone protein Hfq. As growth occurs and the cell density increases, There are three parallel quorum sensing systems, including AI-1/LuxM, AI-2/ the autoinducers accumulate in the cell culture and then bind to their LuxS, and CAI-1/CqsA. At low cell populations, no signal molecules are detected. cognate sensor proteins. This converts the sensor proteins into a While at a high cell population, these three AIs are produced and accumulated to reach a critical concentration to be sensed by their receptors. All the three signal phosphatase which drains the phosphate group in the reverse direction transfer pathways are achieved by a series of hierarchical phosphorylation and leaving LuxO in a dephosphorylated state, which is then inactive, dephosphorylation by the same components. resulting in the stable expression of LitR. LitR also positively regulates the transcription of LuxR, causing a modulation of the expression of AinS in V. fischeri, which is then accumulated and detected only at a downstream luminescent genes (Figure 1) [17-19]. high cell density by the inner membrane hybrid sensor, LuxN [4,20]. AI-2 is produced by LuxS, bound by the periplasmic protein LuxP to Quorum Sensing in V. har ve y i form an AI-2-LuxP complex. This is subsequently sensed by the two- Totally, three parallel signal transduction circuits are present in V. component sensor kinase, LuxQ, whose periplasmic region is associated harveyi that correlate separately to three different autoinducers (Figure with the AI-2-LuxP complex while having a histidine kinase and a 2).
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