Dataset Information

In Silico Analysis of the Quorum Sensing Metagenome in Environmental Biofilm Samples.

ABSTRACT: Quorum sensing (QS) is a sophisticated cell to cell signaling mechanism mediated by small diffusible molecules called "autoinducers." This phenomenon is well studied in bacteria, where different QS systems are described that differ between Gram-negative and Gram-positive bacteria. However, a common system to these groups was discovered, the autoinducer 2. QS has implications in biofilm formation, where the application of metagenomic techniques to study these phenomena may be useful to understand the communication networks established by the different components of the community, and to discover new targets for microbial control. Here we present an in silico screening of QS proteins in all publicly available biofilm metagenomes from the JGI database. We performed sequence, conserved motifs, phylogenetic, and three-dimensional structure analyses of the candidates, resulting in an effective strategy to search QS proteins in metagenomes sequences. The number of QS proteins present in each sample, and its phylogenetic affiliation, was clearly related to the bacterial diversity and the origin of the biofilm. The samples isolated from natural habitats presented clear differences with those from artificial habitats. Interesting findings have been made in the abundance of LuxR-like proteins finding an unbalanced ratio between the synthases and the receptor proteins in Bacteroidetes bacteria, pointing out the existence of "cheaters" in this group. Moreover, we have shown the presence of the LuxI/R QS system in bacteria from the Nitrospira taxonomic group. Finally, some undescribed proteins from the HdtS family have been found in Gamma-proteobacteria.

SUBMITTER: Barriuso J

PROVIDER: S-EPMC6000730 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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In Silico Analysis of the Quorum Sensing Metagenome in Environmental Biofilm Samples.

Barriuso Jorge J Martínez María J MJ

Frontiers in microbiology 20180607

Quorum sensing (QS) is a sophisticated cell to cell signaling mechanism mediated by small diffusible molecules called "autoinducers." This phenomenon is well studied in bacteria, where different QS systems are described that differ between Gram-negative and Gram-positive bacteria. However, a common system to these groups was discovered, the autoinducer 2. QS has implications in biofilm formation, where the application of metagenomic techniques to study these phenomena may be useful to und ...[more]

PMID: 29930547

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Project description:Paracoccus denitrificans is a valuable model organism due to its versatile respiration capability and bioenergetic flexibility, both of which are critical to its survival in different environments. Quorum sensing (QS) plays a crucial role in the regulation of many cell functions; however, whether QS systems play a role in P. denitrificans is unknown. In this study, we demonstrated that iron uptake systems in P. denitrificans were directly regulated by a newly identified QS system. Genes coding for TonB-dependent systems, which transport chelated iron, were transcribed at higher levels in the QS-defective mutants. In contrast, genes coding for the Fbp system, which is TonB independent and transports unchelated ferric iron, were downregulated in the mutants. In brief, QS in P. denitrificans triggers a switch in iron uptake from TonB-dependent to TonB-independent transport during biofilm formation as higher concentrations of iron accumulate in the exopolysaccharide (EPS). Switching from TonB-dependent iron uptake systems to TonB-independent systems not only prevents cells from absorbing excess iron but also conserves energy. Our data suggest that iron uptake strategies are directly regulated by QS in Paracoccus denitrificans to support their survival in available ecological niches.IMPORTANCE As iron is an important trace metal for most organisms, its absorption is highly regulated. Fur has been reported as a prevalent regulator of iron acquisition. In addition, there is a relationship between QS and iron acquisition in pathogenic microbes. However, there have been few studies on the iron uptake strategies of nonpathogenic bacteria. In this study, we demonstrated that iron uptake systems in Paracoccus denitrificans PD1222 were regulated by a newly identified PdeR/PdeI QS system during biofilm formation, and we put forward a hypothesis that QS-dependent iron uptake systems benefit the stability of biofilms. This report elaborates the correlation among QS, iron uptake, and biofilm formation and thus contributes to an understanding of the ecological behavior of environmental bacteria.

Project description:BACKGROUND: In a previous study, we demonstrated that Vibrio scophthalmi, the most abundant Vibrio species among the marine aerobic or facultatively anaerobic bacteria inhabiting the intestinal tract of healthy cultured turbot (Scophthalmus maximus), contains at least two quorum-sensing circuits involving two types of signal molecules (a 3-hydroxy-dodecanoyl-homoserine lactone and the universal autoinducer 2 encoded by luxS). The purpose of this study was to investigate the functions regulated by these quorum sensing circuits in this vibrio by constructing mutants for the genes involved in these circuits. RESULTS: The presence of a homologue to the Vibrio harveyi luxR gene encoding a main transcriptional regulator, whose expression is modulated by quorum-sensing signal molecules in other vibrios, was detected and sequenced. The V. scophthalmi LuxR protein displayed a maximum amino acid identity of 82% with SmcR, the LuxR homologue found in Vibrio vulnificus. luxR and luxS null mutants were constructed and their phenotype analysed. Both mutants displayed reduced biofilm formation in vitro as well as differences in membrane protein expression by mass-spectrometry analysis. Additionally, a recombinant strain of V. scophthalmi carrying the lactonase AiiA from Bacillus cereus, which causes hydrolysis of acyl homoserine lactones, was included in the study. CONCLUSIONS: V. scophthalmi shares two quorum sensing circuits, including the main transcriptional regulator luxR, with some pathogenic vibrios such as V. harveyi and V. anguillarum. However, contrary to these pathogenic vibrios no virulence factors (such as protease production) were found to be quorum sensing regulated in this bacterium. Noteworthy, biofilm formation was altered in luxS and luxR mutants. In these mutants a different expression profile of membrane proteins were observed with respect to the wild type strain suggesting that quorum sensing could play a role in the regulation of the adhesion mechanisms of this bacterium.

Project description:UnlabelledMembers of the genus Burkholderia are known to be adept at biofilm formation, which presumably assists in the survival of these organisms in the environment and the host. Biofilm formation has been linked to quorum sensing (QS) in several bacterial species. In this study, we characterized Burkholderia thailandensis biofilm development under flow conditions and sought to determine whether QS contributes to this process. B. thailandensis biofilm formation exhibited an unusual pattern: the cells formed small aggregates and then proceeded to produce mature biofilms characterized by "dome" structures filled with biofilm matrix material. We showed that this process was dependent on QS. B. thailandensis has three acyl-homoserine lactone (AHL) QS systems (QS-1, QS-2, and QS-3). An AHL-negative strain produced biofilms consisting of cell aggregates but lacking the matrix-filled dome structures. This phenotype was rescued via exogenous addition of the three AHL signals. Of the three B. thailandensis QS systems, we show that QS-1 is required for proper biofilm development, since a btaR1 mutant, which is defective in QS-1 regulation, forms biofilms without these dome structures. Furthermore, our data show that the wild-type biofilm biomass, as well as the material inside the domes, stains with a fucose-binding lectin. The btaR1 mutant biofilms, however, are negative for fucose staining. This suggests that the QS-1 system regulates the production of a fucose-containing exopolysaccharide in wild-type biofilms. Finally, we present data showing that QS ability during biofilm development produces a biofilm that is resistant to dispersion under stress conditions.ImportanceThe saprophyte Burkholderia thailandensis is a close relative of the pathogenic bacterium Burkholderia pseudomallei, the causative agent of melioidosis, which is contracted from its environmental reservoir. Since most bacteria in the environment reside in biofilms, B. thailandensis is an ideal model organism for investigating questions in Burkholderia physiology. In this study, we characterized B. thailandensis biofilm development and sought to determine if quorum sensing (QS) contributes to this process. Our work shows that B. thailandensis produces biofilms with unusual dome structures under flow conditions. Our findings suggest that these dome structures are filled with a QS-regulated, fucose-containing exopolysaccharide that may be involved in the resilience of B. thailandensis biofilms against changes in the nutritional environment.

Dataset Information

In Silico Analysis of the Quorum Sensing Metagenome in Environmental Biofilm Samples.

Publications

<i>In Silico</i> Analysis of the <i>Quorum Sensing</i> Metagenome in Environmental Biofilm Samples.

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