IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42304-4.html
   My bibliography  Save this article

Methylphosphonate-driven methane formation and its link to primary production in the oligotrophic North Atlantic

Author

Listed:
  • Jan N. Arx

    (Max Planck Institute for Marine Microbiology)

  • Abiel T. Kidane

    (Max Planck Institute for Marine Microbiology)

  • Miriam Philippi

    (Max Planck Institute for Marine Microbiology
    Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research)

  • Wiebke Mohr

    (Max Planck Institute for Marine Microbiology)

  • Gaute Lavik

    (Max Planck Institute for Marine Microbiology)

  • Sina Schorn

    (Max Planck Institute for Marine Microbiology)

  • Marcel M. M. Kuypers

    (Max Planck Institute for Marine Microbiology)

  • Jana Milucka

    (Max Planck Institute for Marine Microbiology)

Abstract

Methylphosphonate is an organic phosphorus compound used by microorganisms when phosphate, a key nutrient limiting growth in most marine surface waters, becomes unavailable. Microbial methylphosphonate use can result in the formation of methane, a potent greenhouse gas, in oxic waters where methane production is traditionally unexpected. The extent and controlling factors of such aerobic methane formation remain underexplored. Here, we show high potential net rates of methylphosphonate-driven methane formation (median 0.4 nmol methane L−1 d−1) in the upper water column of the western tropical North Atlantic. The rates are repressed but still quantifiable in the presence of in-situ or added phosphate, suggesting that some methylphosphonate-driven methane formation persists in phosphate-replete waters. The genetic potential for methylphosphonate utilisation is present in and transcribed by key photo- and heterotrophic microbial taxa, such as Pelagibacterales, SAR116, and Trichodesmium. While the large cyanobacterial nitrogen-fixers dominate in the surface layer, phosphonate utilisation by Alphaproteobacteria appears to become more important in deeper depths. We estimate that at our study site, a substantial part (median 11%) of the measured surface carbon fixation can be sustained by phosphorus liberated from phosphonate utilisation, highlighting the ecological importance of phosphonates in the carbon cycle of the oligotrophic ocean.

Suggested Citation

  • Jan N. Arx & Abiel T. Kidane & Miriam Philippi & Wiebke Mohr & Gaute Lavik & Sina Schorn & Marcel M. M. Kuypers & Jana Milucka, 2023. "Methylphosphonate-driven methane formation and its link to primary production in the oligotrophic North Atlantic," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42304-4
    DOI: 10.1038/s41467-023-42304-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42304-4
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-42304-4?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. Elisabet Perez-Coronel & J. Michael Beman, 2022. "Multiple sources of aerobic methane production in aquatic ecosystems include bacterial photosynthesis," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. S. T. Dyhrman & P. D. Chappell & S. T. Haley & J. W. Moffett & E. D. Orchard & J. B. Waterbury & E. A. Webb, 2006. "Phosphonate utilization by the globally important marine diazotroph Trichodesmium," Nature, Nature, vol. 439(7072), pages 68-71, January.
    3. Siddhesh S. Kamat & Howard J. Williams & Frank M. Raushel, 2011. "Intermediates in the transformation of phosphonates to phosphate by bacteria," Nature, Nature, vol. 480(7378), pages 570-573, December.
    4. Thomas Weber & Nicola A. Wiseman & Annette Kock, 2019. "Global ocean methane emissions dominated by shallow coastal waters," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    5. Paul Carini & Angelicque E. White & Emily O. Campbell & Stephen J. Giovannoni, 2014. "Methane production by phosphate-starved SAR11 chemoheterotrophic marine bacteria," Nature Communications, Nature, vol. 5(1), pages 1-7, September.
    6. Leonard Ernst & Benedikt Steinfeld & Uladzimir Barayeu & Thomas Klintzsch & Markus Kurth & Dirk Grimm & Tobias P. Dick & Johannes G. Rebelein & Ilka B. Bischofs & Frank Keppler, 2022. "Methane formation driven by reactive oxygen species across all living organisms," Nature, Nature, vol. 603(7901), pages 482-487, March.
    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. Shi-Hai Mao & Hong-Hai Zhang & Guang-Chao Zhuang & Xiao-Jun Li & Qiao Liu & Zhen Zhou & Wei-Lei Wang & Chun-Yang Li & Ke-Yu Lu & Xi-Ting Liu & Andrew Montgomery & Samantha B. Joye & Yu-Zhong Zhang & G, 2022. "Aerobic oxidation of methane significantly reduces global diffusive methane emissions from shallow marine waters," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    2. Chin-Hsien Cheng & Simon A. T. Redfern, 2022. "Impact of interannual and multidecadal trends on methane-climate feedbacks and sensitivity," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. César Ordóñez & Tonya DelSontro & Timon Langenegger & Daphne Donis & Ena L. Suarez & Daniel F. McGinnis, 2023. "Evaluation of the methane paradox in four adjacent pre-alpine lakes across a trophic gradient," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Leonard Ernst & Uladzimir Barayeu & Jonas Hädeler & Tobias P. Dick & Judith M. Klatt & Frank Keppler & Johannes G. Rebelein, 2023. "Methane formation driven by light and heat prior to the origin of life and beyond," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    5. Søren K. Amstrup & Sui Ching Ong & Nicholas Sofos & Jesper L. Karlsen & Ragnhild B. Skjerning & Thomas Boesen & Jan J. Enghild & Bjarne Hove-Jensen & Ditlev E. Brodersen, 2023. "Structural remodelling of the carbon–phosphorus lyase machinery by a dual ABC ATPase," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    6. Jie Ye & Minghan Zhuang & Mingqiu Hong & Dong Zhang & Guoping Ren & Andong Hu & Chaohui Yang & Zhen He & Shungui Zhou, 2024. "Methanogenesis in the presence of oxygenic photosynthetic bacteria may contribute to global methane cycle," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    7. Stefanie Duller & Simone Vrbancic & Łukasz Szydłowski & Alexander Mahnert & Marcus Blohs & Michael Predl & Christina Kumpitsch & Verena Zrim & Christoph Högenauer & Tomasz Kosciolek & Ruth A. Schmitz , 2024. "Targeted isolation of Methanobrevibacter strains from fecal samples expands the cultivated human archaeome," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Kandasamy Senthilraja & Subramanian Venkatesan & Dhandayuthapani Udhaya Nandhini & Manickam Dhasarathan & Balasubramaniam Prabha & Kovilpillai Boomiraj & Shanmugam Mohan Kumar & Kulanthaivel Bhuvanesw, 2023. "Mitigating Methane Emission from the Rice Ecosystem through Organic Amendments," Agriculture, MDPI, vol. 13(5), pages 1-17, May.
    9. Qi Zhang & Lu Jia & Yuchen Chen & Hanlu Yan & Qiuwen Chen & Jianmin Zhang & Hao Sun, 2024. "Molecular Mechanisms of the Cyanobacterial Response to Different Phosphorus Sources," Sustainability, MDPI, vol. 16(13), pages 1-14, July.
    10. Carlos Y. Sousa & Annabel Fernandes & Albertina Amaro & Maria José Pacheco & Lurdes Ciríaco & Ana Lopes, 2023. "Electrochemical Recovery of Phosphorus from Simulated and Real Wastewater: Effect of Investigational Conditions on the Process Efficiency," Sustainability, MDPI, vol. 15(24), pages 1-15, December.
    11. Florian Roth & Elias Broman & Xiaole Sun & Stefano Bonaglia & Francisco Nascimento & John Prytherch & Volker Brüchert & Maysoon Lundevall Zara & Märta Brunberg & Marc C. Geibel & Christoph Humborg & A, 2023. "Methane emissions offset atmospheric carbon dioxide uptake in coastal macroalgae, mixed vegetation and sediment ecosystems," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

    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:14:y:2023:i:1:d:10.1038_s41467-023-42304-4. 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.