Dataset Information

Cell-Cell Signaling Proteobacterial LuxR Solos: a Treasure Trove of Subgroups Having Different Origins, Ligands, and Ecological Roles.

ABSTRACT: Many proteobacteria possess LuxR solos which are quorum sensing LuxR-type regulators that are not paired with a cognate LuxI-type synthase. LuxR solos have been implicated in intraspecies, interspecies, and interkingdom communication by sensing endogenous and exogenous acyl-homoserine lactones (AHLs) as well as non-AHL signals. LuxR solos are likely to play a major role in microbiome formation, shaping, and maintenance through many different cell-cell signaling mechanisms. This review intends to assess the different types and discuss the possible functional roles of the widespread family of LuxR solo regulators. In addition, an analysis of LuxR solo types and variability among the totality of publicly available proteobacterial genomes is presented. This highlights the importance of these proteins and will encourage scientists to mobilize and study them in order to increase our knowledge of novel cell-cell mechanisms that drive bacterial interactions in the context of complex bacterial communities.

SUBMITTER: Bez C

PROVIDER: S-EPMC10134790 | biostudies-literature | 2023 Apr

REPOSITORIES: biostudies-literature

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Cell-Cell Signaling Proteobacterial LuxR Solos: a Treasure Trove of Subgroups Having Different Origins, Ligands, and Ecological Roles.

Bez Cristina C Geller Alexander Martin AM Levy Asaf A Venturi Vittorio V

mSystems 20230221 2

Many proteobacteria possess LuxR solos which are quorum sensing LuxR-type regulators that are not paired with a cognate LuxI-type synthase. LuxR solos have been implicated in intraspecies, interspecies, and interkingdom communication by sensing endogenous and exogenous acyl-homoserine lactones (AHLs) as well as non-AHL signals. LuxR solos are likely to play a major role in microbiome formation, shaping, and maintenance through many different cell-cell signaling mechanisms. This review intends to ...[more]

PMID: 36802056

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Project description:Bacteria communicate via small diffusible molecules to mediate group-coordinated behavior, a process designated as quorum sensing. The basic molecular quorum sensing system of Gram-negative bacteria consists of a LuxI-type autoinducer synthase producing acyl-homoserine lactones (AHLs) as signaling molecules, and a LuxR-type receptor detecting the AHLs to control expression of specific genes. However, many proteobacteria possess one or more unpaired LuxR-type receptors that lack a cognate LuxI-like synthase, referred to as LuxR solos. The enteric and insect pathogenic bacteria of the genus Photorhabdus harbor an extraordinarily high number of LuxR solos, more than any other known bacteria, and all lack a LuxI-like synthase. Here, we focus on the presence and the different types of LuxR solos in the three known Photorhabdus species using bioinformatics analyses. Generally, the N-terminal signal-binding domain (SBD) of LuxR-type receptors sensing AHLs have a motif of six conserved amino acids that is important for binding and specificity of the signaling molecule. However, this motif is altered in the majority of the Photorhabdus-specific LuxR solos, suggesting the use of other signaling molecules than AHLs. Furthermore, all Photorhabdus species contain at least one LuxR solo with an intact AHL-binding motif, which might allow the ability to sense AHLs of other bacteria. Moreover, all three species have high AHL-degrading activity caused by the presence of different AHL-lactonases and AHL-acylases, revealing a high quorum quenching activity against other bacteria. However, the majority of the other LuxR solos in Photorhabdus have a N-terminal so-called PAS4-domain instead of an AHL-binding domain, containing different amino acid motifs than the AHL-sensors, which potentially allows the recognition of a highly variable range of signaling molecules that can be sensed apart from AHLs. These PAS4-LuxR solos are proposed to be involved in host sensing, and therefore in inter-kingdom signaling. Overall, Photorhabdus species are perfect model organisms to study bacterial communication via LuxR solos and their role for a symbiotic and pathogenic life style.

Project description:LuxR solos are related to quorum sensing (QS) LuxR family regulators; however, they lack a cognate LuxI family protein. LuxR solos are widespread and almost exclusively found in proteobacteria. In this study, we investigated the distribution and conservation of LuxR solos in the fluorescent pseudomonads group. Our analysis of more than 600 genomes revealed that the majority of fluorescent Pseudomonas spp. carry one or more LuxR solos, occurring considerably more frequently than complete LuxI/LuxR archetypical QS systems. Based on the adjacent gene context and conservation of the primary structure, nine subgroups of LuxR solos have been identified that are likely to be involved in the establishment of communication networks. Modeling analysis revealed that the majority of subgroups shows some substitutions at the invariant amino acids of the ligand-binding pocket of QS LuxRs, raising the possibility of binding to non-acyl-homoserine lactone (AHL) ligands. Several mutants and gene expression studies on some LuxR solos belonging to different subgroups were performed in order to shed light on their response. The commonality of LuxR solos among fluorescent pseudomonads is an indication of their important role in cell-cell signaling.IMPORTANCE Cell-cell communication in bacteria is being extensively studied in simple settings and uses chemical signals and cognate regulators/receptors. Many Gram-negative proteobacteria use acyl-homoserine lactones (AHLs) synthesized by LuxI family proteins and cognate LuxR-type receptors to regulate their quorum sensing (QS) target loci. AHL-QS circuits are the best studied QS systems; however, many proteobacterial genomes also contain one or more LuxR solos, which are QS-related LuxR proteins which are unpaired to a cognate LuxI. A few LuxR solos have been implicated in intraspecies, interspecies, and interkingdom signaling. Here, we report that LuxR solo homologs occur considerably more frequently than complete LuxI/LuxR QS systems within the Pseudomonas fluorescens group of species and that they are characterized by different genomic organizations and primary structures and can be subdivided into several subgroups. The P. fluorescens group consists of more than 50 species, many of which are found in plant-associated environments. The role of LuxR solos in cell-cell signaling in fluorescent pseudomonads is discussed.

Dataset Information

Cell-Cell Signaling Proteobacterial LuxR Solos: a Treasure Trove of Subgroups Having Different Origins, Ligands, and Ecological Roles.

Publications

Cell-Cell Signaling Proteobacterial LuxR Solos: a Treasure Trove of Subgroups Having Different Origins, Ligands, and Ecological Roles.

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