A transferred regulator that contributes to Xanthomonas oryzae pv. oryzicola oxidative stress adaptation and virulence by regulating the expression of cytochrome bd oxidase genes
WANG Pei-hong1*, WANG Sai1*, NIE Wen-han1, WU Yan1, Iftikhar AHMAD1, 2, Ayizekeranmu YIMING1, HUANG Jin1, CHEN Gong-you1, ZHU Bo1
1 Shanghai Yangtze River Delta Eco-Environmental Change and Management Observation and Research Station, Ministry of Science and Technology, Ministry of Education/Shanghai Urban Forest Ecosystem Research Station, National Forestry and Grassland Administration, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, P.R.China 2 Department of Environmental Sciences, COMSATS University Islamabad, Vehari-Campus, Vehari 61100, Pakistan
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.
Fund: This work was supported by the National Key R&D Program of China (2018YFD0201202 and 2017YFD0201108), the Agri-X Interdisciplinary Fund of Shanghai Jiao Tong University, China (Agri-X2017010), the Shanghai Committee of Science and Technology, China (19390743300), and the National Natural Science Foundation of China (31200003).
About author: WANG Pei-hong, E-mail: wangpeihong@sjtu.edu.cn; Correspondence ZHU Bo, Tel: +86-21-34205873, E-mail: bzhu1981@sjtu.edu.cn
* These authors contributed equally to this study.
WANG Pei-hong, WANG Sai, NIE Wen-han, WU Yan, Iftikhar AHMAD, Ayizekeranmu YIMING, HUANG Jin, CHEN Gong-you, ZHU Bo.
2022.
A transferred regulator that contributes to Xanthomonas oryzae pv. oryzicola oxidative stress adaptation and virulence by regulating the expression of cytochrome bd oxidase genes. Journal of Integrative Agriculture, 21(6): 1673-1682.
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