Genetic Networks and Gene Regulation Mechanisms for Quorum Sensing and Quorum Quenching in Bacteria

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Microbial Genetics and Genomics".

Deadline for manuscript submissions: closed (31 January 2018) | Viewed by 33357

Special Issue Editors

Department of Environmental Protection, Estacion Experimental del Zaidin, CSIC, Profesor Albareda, 1, 18008 Granada, Spain
Interests: biofilms; beneficial plant-bacterial interactions; bacterial signaling; gene regulation; environmental microbiology
Special Issues, Collections and Topics in MDPI journals
Department of Microbiology, Faculty of Pharmacy, Campus Universitario Cartuja s/n, University of Granada, 18071 Granada, Spain
Interests: microbiology; halophiles; quorum sensing; quorum quenching; exopolysaccharides; agriculture
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Many bacterial activities, including the synthesis of secondary metabolites, enzymes and virulence factors, are modulated by quorum sensing (QS), a sophisticated cell-to-cell communication mechanism based on small diffusible molecules that alter the expression of a whole network of genes (up to 25% of the genome in some cases) when population density reaches a critical threshold. The number of chemically different molecules described as QS signals has constantly increased in the past two decades. Molecular mimics and antagonists produced by eukaryotic organisms and examples of quorum quenching activities that interfere with bacterial QS have also been identified, and may be more widespread than initially expected.

There is still much to be learned about the regulatory mechanisms in which these molecules participate and how QS enables bacteria to coordinate activities, an issue that has significant interest from the perspective of social evolution, fitness and the benefits at the population level associated with costly co-operative behaviours. Inhibiting gene expression when population density is low could serve this purpose, for example, by delaying virulence factor production until enough cells amass to produce effective levels. Restrained gene expression may also benefit groups by enabling coordinated “sneak attacks” during infection, and hiding factors that could be recognized as antigens by the immune system until a large force assembles.

In complex environments, the size of the quorum is not fixed but varies according to the relative rates of production and loss of signal molecules, which depend on many naturally fluctuating environmental parameters. Thus, quorum sensing can also be considered in the context of ‘diffusion sensing’ (DS), ‘compartment sensing’ (CS) or ‘efficiency sensing’ (ES), where the signal molecule supplies information with respect to the local environment and spatial distribution of the cells rather than, or as well as, cell population density.

This Special Issue will explore recent advances and future research avenues on quorum sensing and quorum quenching genomics and genetic networks, and molecular mechanisms of gene expression regulation mediated by signalling molecules.

Dr. Manuel Espinosa Urgel
Dr. Inmaculada Llamas
Guest Editors

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Keywords

  • cell–cell signalling
  • gene expression
  • regulatory networks
  • sociomicrobiology

Published Papers (6 papers)

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Research

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14 pages, 1371 KiB  
Article
The Quorum Sensing System of Yersinia enterocolitica 8081 Regulates Swimming Motility, Host Cell Attachment, and Virulence Plasmid Maintenance
by Yen-Kuan Ng, Marco Grasso, Victoria Wright, Vanina Garcia, Paul Williams and Steve Atkinson
Genes 2018, 9(6), 307; https://doi.org/10.3390/genes9060307 - 20 Jun 2018
Cited by 18 | Viewed by 4135
Abstract
Although Yersinia enterocolitica genomes are highly heterogeneous, they contain a conserved N-acylhomoserine lactone-dependent (AHL) quorum sensing (QS) system consisting of the luxR and luxI orthologs yenR and yenI respectively. Certain hypervirulent strains also contain a putative orphan luxR gene, ycoR, that [...] Read more.
Although Yersinia enterocolitica genomes are highly heterogeneous, they contain a conserved N-acylhomoserine lactone-dependent (AHL) quorum sensing (QS) system consisting of the luxR and luxI orthologs yenR and yenI respectively. Certain hypervirulent strains also contain a putative orphan luxR gene, ycoR, that is not linked to an AHL synthase. To explore the contribution of yenR/yenI/ycoR to QS-dependent phenotypes in Yersinia enterocolitica strain 8081, single and multiple mutants were constructed. AHL profiling identified N-(3-oxohexanoyl) homoserine lactone, N-hexanoylhomoserine lactone, and N-(3-oxoseptanoyl) homoserine lactone as the most abundant. The AHL profiles of the yenR, ycoR and yenR/ycoR mutants were similar to the parent suggesting that the two LuxR homologues do not regulate AHL production while the yenI mutants were AHL-negative. A role for QS in swimming motility and cell attachment was demonstrated. Down-regulation of the virulence plasmid partition gene, spyA, in yenI and yenI/yenR/ycoR mutants is consistent with the greater loss of the Y. enterocolitica pYVe virulence plasmid in the yenI mutant during serial passage at 37 °C but not at 22 °C. A role for QS-regulated spyA in virulence plasmid maintenance is suggested. Full article
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17 pages, 11322 KiB  
Article
Role of SdiA on Biofilm Formation by Atypical Enteropathogenic Escherichia coli
by Hebert F. Culler, Samuel C. F. Couto, Juliana S. Higa, Renato M. Ruiz, Min J. Yang, Vanessa Bueris, Marcia R. Franzolin and Marcelo P. Sircili
Genes 2018, 9(5), 253; https://doi.org/10.3390/genes9050253 - 15 May 2018
Cited by 32 | Viewed by 5137
Abstract
Atypical enteropathogenic Escherichia coli are capable to form biofilm on biotic and abiotic surfaces, regardless of the adherence pattern displayed. Several E. coli mechanisms are regulated by Quorum sensing (QS), including virulence factors and biofilm formation. Quorum sensing is a signaling system that [...] Read more.
Atypical enteropathogenic Escherichia coli are capable to form biofilm on biotic and abiotic surfaces, regardless of the adherence pattern displayed. Several E. coli mechanisms are regulated by Quorum sensing (QS), including virulence factors and biofilm formation. Quorum sensing is a signaling system that confers bacteria with the ability to respond to chemical molecules known as autoinducers. Suppressor of division inhibitor (SdiA) is a QS receptor present in atypical enteropathogenic E. coli (aEPEC) that detects acyl homoserine lactone (AHL) type autoinducers. However, these bacteria do not encode an AHL synthase, but they are capable of sensing AHL molecules produced by other species, establishing an inter-species bacterial communication. In this study, we performed experiments to evaluate pellicle, ring-like structure and biofilm formation on wild type, sdiA mutants and complemented strains. We also evaluated the transcription of genes involved in different stages of biofilm formation, such as bcsA, csgA, csgD, fliC and fimA. The sdiA mutants were capable of forming thicker biofilm structures and showed increased motility when compared to wild type and complemented strains. Moreover, they also showed denser pellicles and ring-like structures. Quantitative real-time PCR (qRT-PCR) analysis demonstrated increased csgA, csgD and fliC transcription on mutant strains. Biofilm formation, as well as csgD, csgA and fimA transcription decreased on wild type strains by the addition of AHL. These results indicate that SdiA participates on the regulation of these phenotypes in aEPEC and that AHL addition enhances the repressor effect of this receptor on the transcription of biofilm and motility related genes. Full article
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17 pages, 917 KiB  
Article
Transcriptome Profiling Reveals the EanI/R Quorum Sensing Regulon in Pantoea Ananatis LMG 2665T
by Siphathele Sibanda, Stanford Kwenda, Collins K. Tanui, Divine Y. Shyntum, Teresa A. Coutinho and Lucy N. Moleleki
Genes 2018, 9(3), 148; https://doi.org/10.3390/genes9030148 - 07 Mar 2018
Cited by 6 | Viewed by 4815
Abstract
Pantoea ananatis LMG 2665T synthesizes and utilizes acyl homoserine lactones (AHLs) for signalling. The complete set of genes regulated by the EanI/R quorum sensing (QS) system in this strain is still not fully known. In this study, RNA-sequencing (RNA-seq) was used to [...] Read more.
Pantoea ananatis LMG 2665T synthesizes and utilizes acyl homoserine lactones (AHLs) for signalling. The complete set of genes regulated by the EanI/R quorum sensing (QS) system in this strain is still not fully known. In this study, RNA-sequencing (RNA-seq) was used to identify the EanI/R regulon in LMG 2665T. Pairwise comparisons of LMG 2665T in the absence of AHLs (Optical density (OD)600 = 0.2) and in the presence of AHLs (OD600 = 0.5) were performed. Additionally, pairwise comparisons of LMG 2665T and its QS mutant at OD600 = 0.5 were undertaken. In total, 608 genes were differentially expressed between LMG 2665T at OD600 = 0.5 versus the same strain at OD600 = 0.2 and 701 genes were differentially expressed between LMG 2665T versus its QS mutant at OD600 = 0.5. A total of 196 genes were commonly differentially expressed between the two approaches. These constituted approximately 4.5% of the whole transcriptome under the experimental conditions used in this study. The RNA-seq data was validated by reverse transcriptase quantitative polymerase chain reaction (RT-qPCR). Genes found to be regulated by EanI/R QS were those coding for redox sensing, metabolism, flagella formation, flagella dependent motility, cell adhesion, biofilm formation, regulators, transport, chemotaxis, methyl accepting proteins, membrane proteins, cell wall synthesis, stress response and a large number of hypothetical proteins. The results of this study give insight into the genes that are regulated by the EanI/R system in LMG 2665T. Functional characterization of the QS regulated genes in LMG 2665T could assist in the formulation of control strategies for this plant pathogen. Full article
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20 pages, 1238 KiB  
Article
High Prevalence of Quorum-Sensing and Quorum-Quenching Activity among Cultivable Bacteria and Metagenomic Sequences in the Mediterranean Sea
by Andrea Muras, Mario López-Pérez, Celia Mayer, Ana Parga, Jaime Amaro-Blanco and Ana Otero
Genes 2018, 9(2), 100; https://doi.org/10.3390/genes9020100 - 16 Feb 2018
Cited by 36 | Viewed by 5476
Abstract
There is increasing evidence being accumulated regarding the importance of N-acyl homoserine lactones (AHL)-mediated quorum-sensing (QS) and quorum-quenching (QQ) processes in the marine environment, but in most cases, data has been obtained from specific microhabitats, and subsequently little is known regarding these [...] Read more.
There is increasing evidence being accumulated regarding the importance of N-acyl homoserine lactones (AHL)-mediated quorum-sensing (QS) and quorum-quenching (QQ) processes in the marine environment, but in most cases, data has been obtained from specific microhabitats, and subsequently little is known regarding these activities in free-living marine bacteria. The QS and QQ activities among 605 bacterial isolates obtained at 90 and 2000 m depths in the Mediterranean Sea were analyzed. Additionally, putative QS and QQ sequences were searched in metagenomic data obtained at different depths (15–2000 m) at the same sampling site. The number of AHL producers was higher in the 90 m sample (37.66%) than in the 2000 m sample (4.01%). However, the presence of QQ enzymatic activity was 1.63-fold higher in the 2000 m sample. The analysis of putative QQ enzymes in the metagenomes supports the relevance of QQ processes in the deepest samples, found in cultivable bacteria. Despite the unavoidable biases in the cultivation methods and biosensor assays and the possible promiscuous activity of the QQ enzymes retrieved in the metagenomic analysis, the results indicate that AHL-related QS and QQ processes could be common activity in the marine environment. Full article
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Review

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21 pages, 1012 KiB  
Review
Regulation Mediated by N-Acyl Homoserine Lactone Quorum Sensing Signals in the Rhizobium-Legume Symbiosis
by Nieves Calatrava-Morales, Matthew McIntosh and María J. Soto
Genes 2018, 9(5), 263; https://doi.org/10.3390/genes9050263 - 18 May 2018
Cited by 52 | Viewed by 6436
Abstract
Soil-dwelling bacteria collectively referred to as rhizobia synthesize and perceive N-acyl-homoserine lactone (AHL) signals to regulate gene expression in a population density-dependent manner. AHL-mediated signaling in these bacteria regulates several functions which are important for the establishment of nitrogen-fixing symbiosis with legume [...] Read more.
Soil-dwelling bacteria collectively referred to as rhizobia synthesize and perceive N-acyl-homoserine lactone (AHL) signals to regulate gene expression in a population density-dependent manner. AHL-mediated signaling in these bacteria regulates several functions which are important for the establishment of nitrogen-fixing symbiosis with legume plants. Moreover, rhizobial AHL act as interkingdom signals triggering plant responses that impact the plant-bacteria interaction. Both the regulatory mechanisms that control AHL synthesis in rhizobia and the set of bacterial genes and associated traits under quorum sensing (QS) control vary greatly among the rhizobial species. In this article, we focus on the well-known QS system of the alfalfa symbiont Sinorhizobium (Ensifer) meliloti. Bacterial genes, environmental factors and transcriptional and posttranscriptional regulatory mechanisms that control AHL production in this Rhizobium, as well as the effects of the signaling molecule on bacterial phenotypes and plant responses will be reviewed. Current knowledge of S. meliloti QS will be compared with that of other rhizobia. Finally, participation of the legume host in QS by interfering with rhizobial AHL perception through the production of molecular mimics will also be addressed. Full article
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11 pages, 3930 KiB  
Review
Quorum Sensing and Quorum Quenching in Agrobacterium: A “Go/No Go System”?
by Yves Dessaux and Denis Faure
Genes 2018, 9(4), 210; https://doi.org/10.3390/genes9040210 - 16 Apr 2018
Cited by 27 | Viewed by 6642
Abstract
The pathogen Agrobacterium induces gall formation on a wide range of dicotyledonous plants. In this bacteria, most pathogenicity determinants are borne on the tumour inducing (Ti) plasmid. The conjugative transfer of this plasmid between agrobacteria is regulated by quorum sensing (QS). However, processes [...] Read more.
The pathogen Agrobacterium induces gall formation on a wide range of dicotyledonous plants. In this bacteria, most pathogenicity determinants are borne on the tumour inducing (Ti) plasmid. The conjugative transfer of this plasmid between agrobacteria is regulated by quorum sensing (QS). However, processes involved in the disturbance of QS also occur in this bacteria under the molecular form of a protein, TraM, inhibiting the sensing of the QS signals, and two lactonases BlcC (AttM) and AiiB that degrade the acylhomoserine lactone (AHL) QS signal. In the model Agrobacterium fabrum strain C58, several data, once integrated, strongly suggest that the QS regulation may not be reacting only to cell concentration. Rather, these QS elements in association with the quorum quenching (QQ) activities may constitute an integrated and complex “go/no go system” that finely controls the biologically costly transfer of the Ti plasmid in response to multiple environmental cues. This decision mechanism permits the bacteria to sense whether it is in a gall or not, in a living or decaying tumor, in stressed plant tissues, etc. In this scheme, the role of the lactonases selected and maintained in the course of Ti plasmid and agrobacterial evolution appears to be pivotal. Full article
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