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Quorum sensing as a potential target for increased production of rhamnolipid biosurfactant in Burkholderia thailandensis E264.

ABSTRACT: Burkholderia thailandensis E264 is a potential non-pathogenic substitute for producing rhamnolipid biosurfactant, replacing the pathogenic Pseudomonas aeruginosa. However, it has low rhamnolipid production and longer fermentation time. We have earlier suggested that media supplementation with exogenous quorum sensing (QS) molecules could lead to early onset of biosynthesis and increased rhamnolipid yield. Here, we assessed the effect of single, double or triple mutations in the various QS systems of B. thailandensis on rhamnolipid production, with the view to see which system(s) have the most impact on rhamnolipid yield and subsequently use the QS molecule to potentially increase yield in the wild-type B. thailandensis. The triple mutant strain had a rhamnolipid yield of 4.46?±?0.345 g/l at 240 h of fermentation which was significantly higher than that of the wild type (0.94?±?0.06 g/l), an unexpected outcome. To gain more insight as to how this might occur, we studied substrate metabolism and energy storage in the form of polyhydroxyalkanoate (PHA) by both the triple mutant and the wild type. We observed increased glycerol metabolism and reduced PHA production in the triple mutant compared with the wild type. Glycerol concentration at 240 h and maximum PHA productivity (g/gDCB) were 8.76 g/l or 16.19 g/l and 21.80% or 31.4% in either the triple mutant or the wild type respectively. Complementation of the triple-mutant cultures with exogenous QS molecules restored rhamnolipid production to similar levels as the wild type. QS therefore is a potential target for increased rhamnolipid production in B. thailandensis.

SUBMITTER: Victor IU

PROVIDER: S-EPMC6667413 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Quorum sensing as a potential target for increased production of rhamnolipid biosurfactant in Burkholderia thailandensis E264.

Victor Irorere U IU Kwiencien Michal M Tripathi Lakshmi L Cobice Diego D McClean Stephen S Marchant Roger R Banat Ibrahim M IM

Applied microbiology and biotechnology 20190621 16

Burkholderia thailandensis E264 is a potential non-pathogenic substitute for producing rhamnolipid biosurfactant, replacing the pathogenic Pseudomonas aeruginosa. However, it has low rhamnolipid production and longer fermentation time. We have earlier suggested that media supplementation with exogenous quorum sensing (QS) molecules could lead to early onset of biosynthesis and increased rhamnolipid yield. Here, we assessed the effect of single, double or triple mutations in the various QS system ...[more]

PMID: 31222386

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Project description:Rhamnolipids are surface-active agents of microbial origin used as alternatives to synthetic surfactants. Burkholderia thailandensis is a non-pathogenic rhamnolipid-producing bacterium that could represent an interesting candidate for use in commercial processes. However, current bioprocesses for rhamnolipid production by this bacterium are not efficient enough, mainly due to low yields. Since regulation of rhamnolipid biosynthesis in B. thailandensis remains poorly understood, identifying new regulatory factors could help increase the production of these valuable metabolites. We performed a random transposon mutagenesis screening to identify genes directing rhamnolipid production in B. thailandensis E264. The most efficient rhamnolipid producer we identified harbored an inactivating transposon insertion in the scmR gene, which was recently described to encode as a secondary metabolite regulator in B. thailandensis. We investigated the impact of scmR loss on rhamnolipid biosynthesis and cell growth. Because biosynthesis of rhamnolipids and polyhydroxyalkanoates (PHAs) could share the same pool of lipid precursors, we also investigate the effect of ScmR on PHA production. We found that production of both rhamnolipids and PHAs are modulated by ScmR during the logarithmic growth phase and demonstrate that ScmR downregulates the production of rhamnolipids by affecting the expression of both rhl biosynthetic operons. Furthermore, our results indicate that PHA biosynthesis is reduced in the scmR- mutant, as ScmR promotes the transcription of the phaC and phaZ genes. By studying the relationship between ScmR and quorum sensing (QS) regulation we reveal that QS acts as an activator of scmR transcription. Finally, we pinpoint the QS-3 system as being involved in the regulation of rhamnolipid and PHA biosynthesis. We conclude that ScmR negatively affects rhamnolipid production, whereas it positively impacts PHAs biosynthesis. This could provide an interesting approach for future strain engineering, leading to improved yields of these valuable metabolites.

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

Quorum sensing as a potential target for increased production of rhamnolipid biosurfactant in Burkholderia thailandensis E264.

Publications

Quorum sensing as a potential target for increased production of rhamnolipid biosurfactant in Burkholderia thailandensis E264.

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