IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-63601-0.html
   My bibliography  Save this article

Electron shuttling promotes denitrification and mitigates nitrous oxide emissions in lakes

Author

Listed:
  • Kang Song

    (Chinese Academy of Sciences
    Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou)
    Guangdong Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yanlin Xiao

    (Chinese Academy of Sciences
    China University of Geosciences)

  • Yuren Wang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Min Deng

    (Chinese Academy of Sciences
    Guangdong Academy of Sciences)

  • Shuni Zhou

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yongxia Huang

    (Chinese Academy of Sciences)

  • Senbati Yeerken

    (Xinjiang University)

  • Lu Li

    (Chinese Academy of Sciences
    Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou))

  • Fengchang Wu

    (Chinese Research Academy of Environmental Sciences)

Abstract

Eutrophication is an emerging global issue that is becoming increasingly severe due to the rising nutrient inputs and limited availability of electron donors for nitrogen removal. In sediments where redox conditions fluctuate dramatically, extracellular electron transfer (EET) critically supports microbial metabolism. However, the biogeochemical significance of EET-coupled denitrification and its EET mechanisms remain unclear. Here, through field investigations and laboratory 15N isotope experiments, we reveal that humic substance (HS)-mediated electron shuttling significantly enhances denitrification primarily by stimulating bacterial outer membrane c-type cytochrome. Specifically, EET mitigates the emission of greenhouse gas nitrous oxide by enriching nosZII-type reducers. Notably, the efficacy of exogenous HS amendment attenuates in sediment with high native HS concentration. Metagenomic binning further reveals multiple cytochromes forming a complete EET-coupled denitrification electron transport chain. Our findings elucidate the microbial mechanisms underlying electron shuttling-driven denitrification in lakes, thereby expanding the understanding of biogeochemical cycles.

Suggested Citation

  • Kang Song & Yanlin Xiao & Yuren Wang & Min Deng & Shuni Zhou & Yongxia Huang & Senbati Yeerken & Lu Li & Fengchang Wu, 2025. "Electron shuttling promotes denitrification and mitigates nitrous oxide emissions in lakes," Nature Communications, Nature, vol. 16(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-63601-0
    DOI: 10.1038/s41467-025-63601-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-63601-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-025-63601-0?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Elígio de Raús Maúre & Genki Terauchi & Joji Ishizaka & Nicholas Clinton & Michael DeWitt, 2021. "Globally consistent assessment of coastal eutrophication," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    2. Christian Pfeffer & Steffen Larsen & Jie Song & Mingdong Dong & Flemming Besenbacher & Rikke Louise Meyer & Kasper Urup Kjeldsen & Lars Schreiber & Yuri A. Gorby & Mohamed Y. El-Naggar & Kar Man Leung, 2012. "Filamentous bacteria transport electrons over centimetre distances," Nature, Nature, vol. 491(7423), pages 218-221, November.
    3. Jens Neu & Catharine C. Shipps & Matthew J. Guberman-Pfeffer & Cong Shen & Vishok Srikanth & Jacob A. Spies & Nathan D. Kirchhofer & Sibel Ebru Yalcin & Gary W. Brudvig & Victor S. Batista & Nikhil S., 2022. "Microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome OmcS nanowires," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. Patrick J. Mulholland & Ashley M. Helton & Geoffrey C. Poole & Robert O. Hall & Stephen K. Hamilton & Bruce J. Peterson & Jennifer L. Tank & Linda R. Ashkenas & Lee W. Cooper & Clifford N. Dahm & Walt, 2008. "Stream denitrification across biomes and its response to anthropogenic nitrate loading," Nature, Nature, vol. 452(7184), pages 202-205, March.
    5. Pilar C. Portela & Catharine C. Shipps & Cong Shen & Vishok Srikanth & Carlos A. Salgueiro & Nikhil S. Malvankar, 2024. "Widespread extracellular electron transfer pathways for charging microbial cytochrome OmcS nanowires via periplasmic cytochromes PpcABCDE," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    6. Lars Peter Nielsen & Nils Risgaard-Petersen & Henrik Fossing & Peter Bondo Christensen & Mikio Sayama, 2010. "Electric currents couple spatially separated biogeochemical processes in marine sediment," Nature, Nature, vol. 463(7284), pages 1071-1074, February.
    7. Yanting Zhang & Man Tong & Yuxi Lu & Fengyi Zhao & Peng Zhang & Zhenchen Wan & Ping Li & Songhu Yuan & Yanxin Wang & Andreas Kappler, 2024. "Directional long-distance electron transfer from reduced to oxidized zones in the subsurface," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    8. Louise B. Sennett & Constance A. Roco & Natalie Y. N. Lim & Joseph B. Yavitt & Peter Dörsch & Lars R. Bakken & James P. Shapleigh & Åsa Frostegård, 2024. "Determining how oxygen legacy affects trajectories of soil denitrifier community dynamics and N2O emissions," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Jesper J. Bjerg & Jamie J. M. Lustermans & Ian P. G. Marshall & Anna J. Mueller & Signe Brokjær & Casper A. Thorup & Paula Tataru & Markus Schmid & Michael Wagner & Lars Peter Nielsen & Andreas Schram, 2023. "Cable bacteria with electric connection to oxygen attract flocks of diverse bacteria," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    2. Md Tabish Noori & Dayakar Thatikayala & Booki Min, 2022. "Bioelectrochemical Remediation for the Removal of Petroleum Hydrocarbon Contaminants in Soil," Energies, MDPI, vol. 15(22), pages 1-22, November.
    3. Jamie J. M. Lustermans & Naja Basu & Leonid Digel & Kartik Aiyer, 2025. "Iron reduction under oxic conditions by Microbacterium deferre sp. nov. A1-JKT," Nature Communications, Nature, vol. 16(1), pages 1-12, December.
    4. Cleuren, Bart & Proesmans, Karel, 2020. "Stochastic impedance," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 552(C).
    5. Beaulieu, Jake & Kopits, Elizabeth & Moore, Chris C. & Parthum, Bryan M., 2024. "The Climate Benefits of Improving Water Quality," National Center for Environmental Economics-NCEE Working Papers 348911, United States Environmental Protection Agency (EPA).
    6. Ruikang Sun & Jiawei Dong & Yi Li & Panwen Li & Yaning Liu & Ying Liu & Jinghong Feng, 2022. "The Influence Research on Nitrogen Transport and Reaction in the Hyporheic Zone with an In-Stream Structure," IJERPH, MDPI, vol. 19(19), pages 1-21, October.
    7. Yanting Zhang & Man Tong & Yuxi Lu & Fengyi Zhao & Peng Zhang & Zhenchen Wan & Ping Li & Songhu Yuan & Yanxin Wang & Andreas Kappler, 2024. "Directional long-distance electron transfer from reduced to oxidized zones in the subsurface," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    8. Beiying Li & Conghe Liu & Jingjing Bai & Yikun Huang & Run Su & Yan Wei & Bin Ma, 2024. "Strategy to mitigate substrate inhibition in wastewater treatment systems," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    9. Karki, Seema & Webb, J Angus & Stewardson, Michael J. & Fowler, Keirnan & Kattel, Giri Raj, 2023. "Basin-scale riverine ecosystem services vary with network geometry," Ecosystem Services, Elsevier, vol. 63(C).
    10. Jinhui Zhou & Laura Scherer & Peter M. van Bodegom & Arthur Beusen & José M. Mogollón, 2022. "Regionalized nitrogen fate in freshwater systems on a global scale," Journal of Industrial Ecology, Yale University, vol. 26(3), pages 907-922, June.
    11. repec:plo:pone00:0132256 is not listed on IDEAS
    12. Jing Yang & Lei Gao & Qi Liu & Zhaoxia Guo, 2024. "Assessing environmental impacts of response strategies for sustainable food system transformation," Sustainable Development, John Wiley & Sons, Ltd., vol. 32(3), pages 2435-2453, June.
    13. Awais Mahmood & Ahsan Farooq & Haseeb Akbar & Hafiz Usman Ghani & Shabbir H. Gheewala, 2023. "An Integrated Approach to Analyze the Progress of Developing Economies in Asia toward the Sustainable Development Goals," Sustainability, MDPI, vol. 15(18), pages 1-33, September.
    14. Pilar C. Portela & Catharine C. Shipps & Cong Shen & Vishok Srikanth & Carlos A. Salgueiro & Nikhil S. Malvankar, 2024. "Widespread extracellular electron transfer pathways for charging microbial cytochrome OmcS nanowires via periplasmic cytochromes PpcABCDE," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    15. Kataki, S. & Chatterjee, S. & Vairale, M.G. & Sharma, S. & Dwivedi, S.K. & Gupta, D.K., 2021. "Constructed wetland, an eco-technology for wastewater treatment: A review on various aspects of microbial fuel cell integration, low temperature strategies and life cycle impact of the technology," Renewable and Sustainable Energy Reviews, Elsevier, vol. 148(C).
    16. James, Anina & Li, Mengtong & Mazarji, Mahmoud & Li, Aohua & Li, Yeqing & Pan, Junting, 2025. "Coupling electron bifurcation and interspecies electron transfer to mitigate ammonia and acids inhibition," Renewable and Sustainable Energy Reviews, Elsevier, vol. 210(C).
    17. Lin, Laurence & Davis, Lisa & Cohen, Sagy & Chapman, Elise & Edmonds, Jennifer W., 2016. "The influence of geomorphic unit spatial distribution on nitrogen retention and removal in a large river," Ecological Modelling, Elsevier, vol. 336(C), pages 26-35.
    18. Tranmer, Andrew W. & Marti, Clelia L. & Tonina, Daniele & Benjankar, Rohan & Weigel, Dana & Vilhena, Leticia & McGrath, Claire & Goodwin, Peter & Tiedemann, Matthew & Mckean, Jim & Imberger, Jörg, 2018. "A hierarchical modelling framework for assessing physical and biochemical characteristics of a regulated river," Ecological Modelling, Elsevier, vol. 368(C), pages 78-93.
    19. Minjin Lee & Charles A. Stock & Elena Shevliakova & Sergey Malyshev & Maureen Beaudor & Nicolas Vuichard, 2024. "Uneven consequences of global climate mitigation pathways on regional water quality in the 21st century," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    20. Wilfred M. Wollheim & Tamara K. Harms & Andrew L. Robison & Lauren E. Koenig & Ashley M. Helton & Chao Song & William B. Bowden & Jacques C. Finlay, 2022. "Superlinear scaling of riverine biogeochemical function with watershed size," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    21. Irfan, Muhammad & Zhou, Lei & Ji, Jia-Heng & Chen, Jing & Yuan, Shan & Liang, Tian-Tian & Liu, Jin-Feng & Yang, Shi-Zhong & Gu, Ji-Dong & Mu, Bo-Zhong, 2020. "Enhanced energy generation and altered biochemical pathways in an enrichment microbial consortium amended with natural iron minerals," Renewable Energy, Elsevier, vol. 159(C), pages 585-594.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-63601-0. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.