A transferred regulator that contributes to Xanthomonas oryzae pv. oryzicola oxidative stress adaptation and virulence by regulating the expression of cytochrome bd oxidase genes

Abstract

Horizontal gene transfer (HGT) has been well documented as a driving force in the evolution of bacteria. It has been shown that a horizontally acquired gene, xoc_2868, involved in the global response against oxidative stress and pathogenicity of Xanthomonas oryzae pv. oryzicola strain BLS256. However, as a transcriptional factor (TF), the regulatory mechanism of XOC_2868 has not yet been revealed. Here, evolutionary analysis suggested XOC_2868 might be co-transferred with its physically proximate downstream genes from a Burkholderiaceae ancestor. Interestingly, RNA-seq data of wild-type (BLS256) and Δxoc_2868 strains under oxidative stress showed that XOC_2868 did not regulate the expression of its adjacent genes, but remarkably influenced the expression of several genes involved in the extracellular polysaccharide (EPS) production and xanthan biosynthesis. Chromatin immunoprecipitation-sequence (ChIP-seq) combined with transcriptome analysis revealed that XOC_2868 directly regulates a cydAB operon, encoding two subunits of cytochrome bd oxidase and involved in redox balance. Consistent with Δxoc_2868 strain, cydA- and cydAB-knockout mutants also showed a higher sensitivity to H2O2 along with a reduced bacterial virulence compared with the wild-type strain. Overall, our findings raise the possibility of regulatory circuit evolution shaped by HGT and driven by selection and reveal a novel regulatory pathway that regulates the expression of cytochrome bd oxidase and thus contributes to the virulence of BLS256.