tepR encoding a bacterial enhancer-binding protein orchestrates the virulence and interspecies competition of Burkholderia glumae through qsmR and a type VI secretion system

The pathogenesis of the rice pathogenic bacteriumBurkholderia glumaeis under the tight regulation of thetofI/tofRquorum-sensing (QS) system.tepR, encoding a group I bacterial enhancer-binding protein, negatively regulates the production of toxoflavin, the phytotoxin acting as a major virulence factor inB. glumae. In this study, through a transcriptomic analysis, we identified the genes that were modulated bytepRand/or thetofI/tofRQS system. More than half of the differentially expressed genes, including the genes for the biosynthesis and transport of toxoflavin, were significantly more highly expressed in the Delta tepRmutant but less expressed in the Delta tofI-tofR(tofI/tofRQS-defective) mutant. In consonance with the transcriptome data, other virulence-related functions ofB. glumae, extracellular protease activity and flagellum-dependent motility, were also negatively regulated bytepR, and this negative regulatory function oftepRwas dependent on the IclR-type transcriptional regulator geneqsmR. Likewise, the Delta tepRmutant exhibited a higher level of heat tolerance in congruence with the higher transcription levels of heat shock protein genes in the mutant. Interestingly,tepRalso exhibited its positive regulatory function on a previously uncharacterized type VI secretion system (denoted as BgT6SS-1). The survival of the both Delta tepRand Delta tssD(BgT6SS-1-defective) mutants was significantly compromised compared to the wild-type parent strain 336gr-1 in the presence of the natural rice-inhabiting bacterium,Pantoeasp. RSPAM1. Taken together, this study revealed pivotal regulatory roles oftepRin orchestrating multiple biological functions ofB. glumae, including pathogenesis, heat tolerance, and bacterial interspecies competition.