Versatile nitrate-respiring heterotrophs are previously concealed contributors to sulfur cycle

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 () and Chuan Chen ()
Additional contact information
Bo Shao: Harbin Institute of Technology
Yuan-Guo Xie: University of Science and Technology of China
Long Zhang: Huaibei Normal University
Yang Ruan: Nanjing Agricultural University
Bin Liang: Harbin Institute of Technology Shenzhen
Ruochen Zhang: Hebei University of Technology
Xijun Xu: Harbin Institute of Technology
Wei Wang: Harbin Institute of Technology
Zhengda Lin: Harbin Institute of Technology
Xuanyuan Pei: Wuhan Textile University
Xueting Wang: Harbin Institute of Technology
Lei Zhao: Harbin Institute of Technology
Xu Zhou: Harbin Institute of Technology Shenzhen
Xiaohui Wu: Huazhong University of Science and Technology
Defeng Xing: Harbin Institute of Technology
Aijie Wang: Harbin Institute of Technology Shenzhen
Duu-Jong Lee: City University of Hong Kong
Nanqi Ren: Harbin Institute of Technology
Donald E. Canfield: University of Southern Denmark
Brian P. Hedlund: University of Nevada, Las Vegas
Zheng-Shuang Hua: University of Science and Technology of China
Chuan Chen: Harbin Institute of Technology

Nature Communications, 2025, vol. 16, issue 1, 1-15

Abstract: 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.

Date: 2025
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DOI: 10.1038/s41467-025-56588-1

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