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

• Published in: Journal of Integrative Agriculture 2022-06, Vol.21 (6), p.1673-1682
• Main Authors: Pei-hong, WANG, Sai, WANG, Wen-han, NIE, Yan, WU, AHMAD, Iftikhar, YIMING, Ayizekeranmu, Jin, HUANG, Gong-you, CHEN, Bo, ZHU
• Format: Article
• Language: English
• Subjects: HGT; oxidative stress adaptation and virulence; transcriptional factor; Xanthomonas oryzae pv. oryzicola
• ISSN: 2095-3119
• DOI: 10.1016/S2095-3119(21)63801-7

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.