Versatile nitrate-respiring heterotrophs are previously concealed contributors to sulfur cycle
Abstract Heterotrophic denitrifiers play crucial roles in global carbon and nitrogen cycling. However, their inability to oxidize sulfide renders them vulnerable to this toxic molecule, which inhibits the key enzymatic reaction responsible for reducing nitrous oxide (N2O), thereby raising greenhouse...
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Nature Portfolio
2025-01-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-025-56588-1 |
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| author | Bo Shao Yuan-Guo Xie Long Zhang Yang Ruan Bin Liang Ruochen Zhang Xijun Xu Wei Wang Zhengda Lin Xuanyuan Pei Xueting Wang Lei Zhao Xu Zhou Xiaohui Wu Defeng Xing Aijie Wang Duu-Jong Lee Nanqi Ren Donald E. Canfield Brian P. Hedlund Zheng-Shuang Hua Chuan Chen |
| author_facet | Bo Shao Yuan-Guo Xie Long Zhang Yang Ruan Bin Liang Ruochen Zhang Xijun Xu Wei Wang Zhengda Lin Xuanyuan Pei Xueting Wang Lei Zhao Xu Zhou Xiaohui Wu Defeng Xing Aijie Wang Duu-Jong Lee Nanqi Ren Donald E. Canfield Brian P. Hedlund Zheng-Shuang Hua Chuan Chen |
| author_sort | Bo Shao |
| collection | DOAJ |
| description | Abstract Heterotrophic denitrifiers play crucial roles in global carbon and nitrogen cycling. However, their inability to oxidize sulfide renders them vulnerable to this toxic molecule, which inhibits the key enzymatic reaction responsible for reducing nitrous oxide (N2O), thereby raising greenhouse gas emissions. Here, we applied microcosm incubations, community-isotope-corrected DNA stable-isotope probing, and metagenomics to characterize a cohort of heterotrophic denitrifiers in estuarine sediments that thrive by coupling sulfur oxidation with denitrification through chemolithoheterotrophic metabolism. Remarkably, ecophysiology experiments from enrichments demonstrate that such heterotrophs expedite denitrification with sulfur acting as alternative electron sources and substantially curtail N2O emissions in both organic-rich and organic-limited environments. Their flexible, non-sulfur-dependent physiology may confer competitive advantages over conventional heterotrophic denitrifiers in detoxifying sulfide, adapting to organic matter fluctuations, and mitigating greenhouse gas emissions. Our study provides insights into the ecological role of heterotrophic denitrifiers in microbial communities with implications for sulfur cycling and climate change. |
| format | Article |
| id | doaj-art-a5b860cb81c04c61929069b5cc55b54e |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-a5b860cb81c04c61929069b5cc55b54e2025-02-02T12:32:10ZengNature PortfolioNature Communications2041-17232025-01-0116111510.1038/s41467-025-56588-1Versatile nitrate-respiring heterotrophs are previously concealed contributors to sulfur cycleBo Shao0Yuan-Guo Xie1Long Zhang2Yang Ruan3Bin Liang4Ruochen Zhang5Xijun Xu6Wei Wang7Zhengda Lin8Xuanyuan Pei9Xueting Wang10Lei Zhao11Xu Zhou12Xiaohui Wu13Defeng Xing14Aijie Wang15Duu-Jong Lee16Nanqi Ren17Donald E. Canfield18Brian P. Hedlund19Zheng-Shuang Hua20Chuan Chen21State Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of TechnologyChinese Academy of Sciences Key Laboratory of Urban Pollutant Conversion, Department of Environmental Science and Engineering, University of Science and Technology of ChinaCollege of Life Sciences, Huaibei Normal UniversityJangsu Provincial Key Lab for Solid Organic Waste Utilization, Key Lab of Organic-based Fertilizers of China, Nanjing Agricultural UniversityState Key Laboratory of Urban Water Resource and Environment, School of Civil and Environmental Engineering, Harbin Institute of Technology ShenzhenSchool of Civil and Transportation, Hebei University of TechnologyState Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of TechnologyState Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of TechnologyState Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of TechnologySchool of Environmental Engineering, Wuhan Textile UniversityState Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of TechnologyState Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of TechnologyState Key Laboratory of Urban Water Resource and Environment, School of Civil and Environmental Engineering, Harbin Institute of Technology ShenzhenSchool of Environmental Science and Engineering, Huazhong University of Science and TechnologyState Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of TechnologyState Key Laboratory of Urban Water Resource and Environment, School of Civil and Environmental Engineering, Harbin Institute of Technology ShenzhenDepartment of Mechanical Engineering, City University of Hong KongState Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of TechnologyNordcee, Department of Biology, University of Southern DenmarkSchool of Life Sciences, University of Nevada, Las VegasChinese Academy of Sciences Key Laboratory of Urban Pollutant Conversion, Department of Environmental Science and Engineering, University of Science and Technology of ChinaState Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of TechnologyAbstract Heterotrophic denitrifiers play crucial roles in global carbon and nitrogen cycling. However, their inability to oxidize sulfide renders them vulnerable to this toxic molecule, which inhibits the key enzymatic reaction responsible for reducing nitrous oxide (N2O), thereby raising greenhouse gas emissions. Here, we applied microcosm incubations, community-isotope-corrected DNA stable-isotope probing, and metagenomics to characterize a cohort of heterotrophic denitrifiers in estuarine sediments that thrive by coupling sulfur oxidation with denitrification through chemolithoheterotrophic metabolism. Remarkably, ecophysiology experiments from enrichments demonstrate that such heterotrophs expedite denitrification with sulfur acting as alternative electron sources and substantially curtail N2O emissions in both organic-rich and organic-limited environments. Their flexible, non-sulfur-dependent physiology may confer competitive advantages over conventional heterotrophic denitrifiers in detoxifying sulfide, adapting to organic matter fluctuations, and mitigating greenhouse gas emissions. Our study provides insights into the ecological role of heterotrophic denitrifiers in microbial communities with implications for sulfur cycling and climate change.https://doi.org/10.1038/s41467-025-56588-1 |
| spellingShingle | Bo Shao Yuan-Guo Xie Long Zhang Yang Ruan Bin Liang Ruochen Zhang Xijun Xu Wei Wang Zhengda Lin Xuanyuan Pei Xueting Wang Lei Zhao Xu Zhou Xiaohui Wu Defeng Xing Aijie Wang Duu-Jong Lee Nanqi Ren Donald E. Canfield Brian P. Hedlund Zheng-Shuang Hua Chuan Chen Versatile nitrate-respiring heterotrophs are previously concealed contributors to sulfur cycle Nature Communications |
| title | Versatile nitrate-respiring heterotrophs are previously concealed contributors to sulfur cycle |
| title_full | Versatile nitrate-respiring heterotrophs are previously concealed contributors to sulfur cycle |
| title_fullStr | Versatile nitrate-respiring heterotrophs are previously concealed contributors to sulfur cycle |
| title_full_unstemmed | Versatile nitrate-respiring heterotrophs are previously concealed contributors to sulfur cycle |
| title_short | Versatile nitrate-respiring heterotrophs are previously concealed contributors to sulfur cycle |
| title_sort | versatile nitrate respiring heterotrophs are previously concealed contributors to sulfur cycle |
| url | https://doi.org/10.1038/s41467-025-56588-1 |
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