A transferred regulator that contributes to Xanthomonas oryzae pv. oryzicola oxidative stress adaptation and virulence by regulating the expression of cytochrome bd oxidase genes
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. Howeve...
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KeAi Communications Co., Ltd.
2022-06-01
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| Series: | Journal of Integrative Agriculture |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2095311921638017 |
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| author | Pei-hong WANG Sai WANG Wen-han NIE Yan WU AHMAD Iftikhar YIMING Ayizekeranmu Jin HUANG Gong-you CHEN Bo ZHU |
| author_facet | Pei-hong WANG Sai WANG Wen-han NIE Yan WU AHMAD Iftikhar YIMING Ayizekeranmu Jin HUANG Gong-you CHEN Bo ZHU |
| author_sort | Pei-hong WANG |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-ece267c3c36b4f49b09cf6216e5b71f8 |
| institution | Matheson Library |
| issn | 2095-3119 |
| language | English |
| publishDate | 2022-06-01 |
| publisher | KeAi Communications Co., Ltd. |
| record_format | Article |
| series | Journal of Integrative Agriculture |
| spelling | doaj-art-ece267c3c36b4f49b09cf6216e5b71f82025-08-02T22:43:56ZengKeAi Communications Co., Ltd.Journal of Integrative Agriculture2095-31192022-06-0121616731682A transferred regulator that contributes to Xanthomonas oryzae pv. oryzicola oxidative stress adaptation and virulence by regulating the expression of cytochrome bd oxidase genesPei-hong WANG0Sai WANG1Wen-han NIE2Yan WU3AHMAD Iftikhar4YIMING Ayizekeranmu5Jin HUANG6Gong-you CHEN7Bo ZHU8Shanghai Yangtze River Delta Eco-Environmental Change and Management Observation and Research Station/Shanghai Cooperative Innovation Center of Agri-Seeds, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, P.R.China; Correspondence ZHU Bo, Tel: +86-21-34205873Shanghai Yangtze River Delta Eco-Environmental Change and Management Observation and Research Station/Shanghai Cooperative Innovation Center of Agri-Seeds, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, P.R.ChinaShanghai Yangtze River Delta Eco-Environmental Change and Management Observation and Research Station/Shanghai Cooperative Innovation Center of Agri-Seeds, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, P.R.ChinaShanghai Yangtze River Delta Eco-Environmental Change and Management Observation and Research Station/Shanghai Cooperative Innovation Center of Agri-Seeds, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, P.R.ChinaShanghai Yangtze River Delta Eco-Environmental Change and Management Observation and Research Station/Shanghai Cooperative Innovation Center of Agri-Seeds, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, P.R.China; Department of Environmental Sciences, COMSATS University Islamabad, Vehari-Campus, Vehari 61100, PakistanShanghai Yangtze River Delta Eco-Environmental Change and Management Observation and Research Station/Shanghai Cooperative Innovation Center of Agri-Seeds, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, P.R.ChinaShanghai Yangtze River Delta Eco-Environmental Change and Management Observation and Research Station/Shanghai Cooperative Innovation Center of Agri-Seeds, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, P.R.ChinaShanghai Yangtze River Delta Eco-Environmental Change and Management Observation and Research Station/Shanghai Cooperative Innovation Center of Agri-Seeds, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, P.R.ChinaShanghai Yangtze River Delta Eco-Environmental Change and Management Observation and Research Station/Shanghai Cooperative Innovation Center of Agri-Seeds, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, P.R.China; Correspondence ZHU Bo, Tel: +86-21-34205873Horizontal 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.http://www.sciencedirect.com/science/article/pii/S2095311921638017HGTtranscriptional factorXanthomonas oryzae pv. oryzicolaoxidative stress adaptation and virulence |
| spellingShingle | Pei-hong WANG Sai WANG Wen-han NIE Yan WU AHMAD Iftikhar YIMING Ayizekeranmu Jin HUANG Gong-you CHEN Bo ZHU 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 HGT transcriptional factor Xanthomonas oryzae pv. oryzicola oxidative stress adaptation and virulence |
| title | A transferred regulator that contributes to Xanthomonas oryzae pv. oryzicola oxidative stress adaptation and virulence by regulating the expression of cytochrome bd oxidase genes |
| title_full | A transferred regulator that contributes to Xanthomonas oryzae pv. oryzicola oxidative stress adaptation and virulence by regulating the expression of cytochrome bd oxidase genes |
| title_fullStr | A transferred regulator that contributes to Xanthomonas oryzae pv. oryzicola oxidative stress adaptation and virulence by regulating the expression of cytochrome bd oxidase genes |
| title_full_unstemmed | A transferred regulator that contributes to Xanthomonas oryzae pv. oryzicola oxidative stress adaptation and virulence by regulating the expression of cytochrome bd oxidase genes |
| title_short | A transferred regulator that contributes to Xanthomonas oryzae pv. oryzicola oxidative stress adaptation and virulence by regulating the expression of cytochrome bd oxidase genes |
| title_sort | transferred regulator that contributes to xanthomonas oryzae pv oryzicola oxidative stress adaptation and virulence by regulating the expression of cytochrome bd oxidase genes |
| topic | HGT transcriptional factor Xanthomonas oryzae pv. oryzicola oxidative stress adaptation and virulence |
| url | http://www.sciencedirect.com/science/article/pii/S2095311921638017 |
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