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      Editorial: LuxR Solos are Becoming Major Players in Cell–Cell Communication in Bacteria

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          Abstract

          Quorum sensing (QS) is the ability of microbes to sense and respond to their own population density, which typically results in cooperative activity (Fuqua et al., 1994). This form of microbial communication is important to agriculture and human health as they often participate in the regulation of genes important for host interactions. The classic example of QS in bacteria is performed by the symbiotic bioluminescent bacterium Vibrio fischeri (Hastings and Greenberg, 1999). This bacterium colonizes the light organ of a squid and becomes luminescent at high population density. A pheromone of the acylhomoserine lactone class (AHL) is synthesized by the enzyme LuxI, and is a proxy for population density. The AHL is sensed by the transcription factor LuxR, which then activates the transcription of the luxICDABEG luciferase operon. Homologous LuxR-LuxI pairs have been found throughout the Proteobacteria (Fuqua et al., 2001); there is divergence among the structures of AHLs produced and detected by LuxI-LuxR pairs, providing some species specificity to the systems. Several studies and the sequencing of many bacterial genomes has evidenced the presence of many AHL/QS-related luxR-type genes, which are unpaired to a cognate luxI. These LuxRs possess the typical modular structure having an AHL-binding domain and a DNA-binding HTH domain. These upaired luxRs/LuxRs have been called orphans (Fuqua, 2006; Patankar and Gonzalez, 2009) and more recently solos (Subramoni and Venturi, 2009). Several questions arise on the role of LuxR solos in bacteria and recent studies have revealed a number of roles including eavesdropping, intra-species and inter-kingdom signaling. This research topic of Frontiers in Cellular and Infection Microbiology is a collection of 10 articles which highlight these different roles as well as the widespread distribution of LuxR solos. Three articles highlight how widespread LuxR solos are and provide data on their phylogenetic distribution (Gan et al., 2014; Hudaiberdiev et al., 2015; Subramoni et al., 2015). These surveys have shown the presence of one or multiple predicted LuxR solos in many proteobacterial genomes living in different environments, some of them also harboring genes for one or more complete AHL-QS circuits. LuxR solos can be tentatively clustered into meaningful groups or putative orthologs. These LuxR solos subfamilies could respond to different signals and/or having different roles. The functions of solos can thus far be sub-divided in four categories; as detecting endogenous or exogenous signals, of either the classical AHL type, or of a novel type. The AHL-responsive solos can firstly detect exogenous AHLs, i.e., AHLs synthesized by other organisms, and this category is typified by the LuxR solo, SdiA (Sperandio, 2010; Soares and Ahmer, 2011; Swearingen et al., 2013; Sabag-Daigle et al., 2015). Orthologs of sdiA are present in Escherichia, Salmonella, Enterobacter, Citrobacter, Cronobacter, Klebsiella, Pantoea, and Erwinia (Sabag-Daigle and Ahmer, 2012). The Pantoea and Erwinia orthologs are part of luxR-luxI pairs and represent the ancestral state, and the luxI homolog was lost in the remaining genera, giving rise to the sdiA solos (Sabag-Daigle and Ahmer, 2012). In this issue, an sdiA-regulon study is presented showing a number of genes regulated by SdiA in Enterobacter cloacae (Sabag-Daigle et al., 2015). Interestingly some target genes were regulated in the complete absence of AHLs and thus AHLs may not be a “folding-switch” for SdiA, in which SdiA only folds correctly in the presence of AHL (Yao et al., 2006; Nguyen et al., 2015), AHL may alter the DNA binding specificity of SdiA so that there are AHL-dependent and AHL-independent promoters. LuxR solos can also be used to detect endogenous AHLs, i.e., AHLs that are made by the species detecting them. This “third wheel” type of LuxR solo is typified by QscR of Pseudomonas aeruginosa which harbors two complete AHL QS circuits, namely LasI/R and RhlI/R (Chugani and Greenberg, 2014; Martínez et al., 2015). In this issue, a review regarding the function of QscR is presented (Chugani and Greenberg, 2014; Martínez et al., 2015). QscR is involved in virulence and it responds to LasI generated AHLs, however it has a more relaxed specificity and is more promiscuous than LasR and its regulon overlaps with the one of LasR. The article particularly focuses on its biochemistry since QscR has become a model for understanding QS LuxR homologs. LuxR solos can also respond to ligands which are not AHLs of either endogenous or exogenous sources. A large sub-family of LuxR solos has been found that specifically recognizes molecules from plants (González and Venturi, 2012; da Silva et al., 2015; Xu et al., 2015). These solos are only found in both pathogenic and beneficial plant-associated bacteria (PAB) and show changes in one or two highly conserved amino acids of the autoinducer binding domain (González and Venturi, 2012). Another member of this subfamily of PAB LuxR solos is reported in this Frontiers topic (Xu et al., 2015) as well as studies of protein domain switching between these solos and classic AHL responsive motifs (da Silva et al., 2015). A major step forward will be to identify the class of plant molecules that these solos respond to. Some solos respond to an endogenous, non-AHL, ligand. The LuxR-type receptor PluR of Photorhabdus luminescens responds to α-pyrones, while the related organism Photorhabdus asymbiotica responds to dialkylresorcinols using the LuxR homolog PauR (Brachmann et al., 2013; Brameyer et al., 2014, 2015; Brameyer and Heermann, 2015; Chen et al., 2015). The synthases for these molecules were determined to be PpyS and DarABC, respectively. In this instance, the LuxR solos turned out not to be solo at all. Instead, these LuxR homologs are paired with previously unrecognized types of synthases. In this topic, a survey of these LuxRs in Photorhabdus species is reported (Brameyer et al., 2014). In summary, LuxR solos are widespread in Proteobacteria hence they are major players in bacterial communication and require more attention. Articles in this topic highlight the different modes of action of LuxR solos which are responding to endogenous and exogenous AHL or non-AHL signals. Further studies could lead to novel ways of controlling bacterial host colonization. Conflict of interest statement The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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          Most cited references 26

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          Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators.

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            Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing.

            Quorum sensing is an example of community behavior prevalent among diverse bacterial species. The term "quorum sensing" describes the ability of a microorganism to perceive and respond to microbial population density, usually relying on the production and subsequent response to diffusible signal molecules. A significant number of gram-negative bacteria produce acylated homoserine lactones (acyl-HSLs) as signal molecules that function in quorum sensing. Bacteria that produce acyl-HSLs can respond to the local concentration of the signaling molecules, and high population densities foster the accumulation of inducing levels of acyl-HSLs. Depending upon the bacterial species, the physiological processes regulated by quorum sensing are extremely diverse, ranging from bioluminescence to swarming motility. Acyl-HSL quorum sensing has become a paradigm for intercellular signaling mechanisms. A flurry of research over the past decade has led to significant understanding of many aspects of quorum sensing including the synthesis of acyl-HSLs, the receptors that recognize the acyl-HSL signal and transduce this information to the level of gene expression, and the interaction of these receptors with the transcriptional machinery. Recent studies have begun to integrate acyl-HSL quorum sensing into global regulatory networks and establish its role in developing and maintaining the structure of bacterial communities.
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              LuxR-family 'solos': bachelor sensors/regulators of signalling molecules.

              N-Acylhomoserine lactone (AHL) quorum-sensing (QS) signalling is the best-understood chemical language in proteobacteria. In the last 15 years a large amount of research in several bacterial species has revealed in detail the genetic, molecular and biochemical mechanisms underlying AHL signalling. These studies have revealed the role played by protein pairs of the AHL synthase belonging to the LuxI family and cognate LuxR-family AHL sensor-regulator. Proteobacteria however commonly possess a QS LuxR-family protein for which there is no obvious cognate LuxI synthase; these proteins are found in bacteria which possess a complete AHL QS system(s) as well as in bacteria that do not. Scientists are beginning to address the roles played by these proteins and it is emerging that they could allow bacteria to respond to endogenous and exogenous signals produced by their neighbours. AHL QS research thus far has mainly focused on a cell-density response involving laboratory monoculture studies. Recent findings on the role played by the unpaired LuxR-family proteins highlight the need to address bacterial behaviour and response to signals in mixed communities. Here we review recent progress with respect to these LuxR proteins, which we propose to call LuxR 'solos' since they act on their own without the need for a cognate signal generator. Initial investigations have revealed that LuxR solos have diverse roles in bacterial interspecies and interkingdom communication.
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                Author and article information

                Contributors
                Journal
                Front Cell Infect Microbiol
                Front Cell Infect Microbiol
                Front. Cell. Infect. Microbiol.
                Frontiers in Cellular and Infection Microbiology
                Frontiers Media S.A.
                2235-2988
                01 December 2015
                2015
                : 5
                Affiliations
                1International Centre for Genetic and Biotechnology Trieste, Italy
                2Department of Microbial Infection and Immunity, The Ohio State University Columbus, OH, USA
                3Center for Microbial Interface Biology, The Ohio State University Columbus, OH, USA
                4Department of Microbiology, The Ohio State University Columbus, OH, USA
                Author notes

                Edited and reviewed by: Yousef Abu Kwaik, University of Louisville School of Medicine, USA

                *Correspondence: Vittorio Venturi venturi@ 123456icgeb.org

                †These authors have contributed equally to this work.

                Article
                10.3389/fcimb.2015.00089
                4664662
                Copyright © 2015 Venturi and Ahmer.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 0, Tables: 0, Equations: 0, References: 26, Pages: 3, Words: 1954
                Funding
                Funded by: International Centre for Genetic Engineering and Biotechnology 10.13039/501100001688
                Funded by: National Institutes of Health 10.13039/100000002
                Categories
                Microbiology
                Editorial

                Infectious disease & Microbiology

                ahl, luxr solos, quorum sensing, signaling, bacteria

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