IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41847-w.html
   My bibliography  Save this article

Multi-heme cytochrome-mediated extracellular electron transfer by the anaerobic methanotroph ‘Candidatus Methanoperedens nitroreducens’

Author

Listed:
  • Xueqin Zhang

    (University of Queensland)

  • Georgina H. Joyce

    (Queensland University of Technology (QUT), Translational Research Institute)

  • Andy O. Leu

    (Queensland University of Technology (QUT), Translational Research Institute)

  • Jing Zhao

    (University of Queensland
    The University of Queensland)

  • Hesamoddin Rabiee

    (University of Queensland
    The University of Queensland
    University of Southern Queensland)

  • Bernardino Virdis

    (University of Queensland)

  • Gene W. Tyson

    (Queensland University of Technology (QUT), Translational Research Institute)

  • Zhiguo Yuan

    (University of Queensland
    City University of Hong Kong)

  • Simon J. McIlroy

    (Queensland University of Technology (QUT), Translational Research Institute)

  • Shihu Hu

    (University of Queensland)

Abstract

Anaerobic methanotrophic archaea (ANME) carry out anaerobic oxidation of methane, thus playing a crucial role in the methane cycle. Previous genomic evidence indicates that multi-heme c-type cytochromes (MHCs) may facilitate the extracellular electron transfer (EET) from ANME to different electron sinks. Here, we provide experimental evidence supporting cytochrome-mediated EET for the reduction of metals and electrodes by ‘Candidatus Methanoperedens nitroreducens’, an ANME acclimated to nitrate reduction. Ferrous iron-targeted fluorescent assays, metatranscriptomics, and single-cell imaging suggest that ‘Ca. M. nitroreducens’ uses surface-localized redox-active cytochromes for metal reduction. Electrochemical and Raman spectroscopic analyses also support the involvement of c-type cytochrome-mediated EET for electrode reduction. Furthermore, several genes encoding menaquinone cytochrome type-c oxidoreductases and extracellular MHCs are differentially expressed when different electron acceptors are used.

Suggested Citation

  • Xueqin Zhang & Georgina H. Joyce & Andy O. Leu & Jing Zhao & Hesamoddin Rabiee & Bernardino Virdis & Gene W. Tyson & Zhiguo Yuan & Simon J. McIlroy & Shihu Hu, 2023. "Multi-heme cytochrome-mediated extracellular electron transfer by the anaerobic methanotroph ‘Candidatus Methanoperedens nitroreducens’," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41847-w
    DOI: 10.1038/s41467-023-41847-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41847-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-41847-w?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. Mohamed F. Haroon & Shihu Hu & Ying Shi & Michael Imelfort & Jurg Keller & Philip Hugenholtz & Zhiguo Yuan & Gene W. Tyson, 2013. "Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage," Nature, Nature, vol. 500(7464), pages 567-570, August.
    2. Shawn E. McGlynn & Grayson L. Chadwick & Christopher P. Kempes & Victoria J. Orphan, 2015. "Single cell activity reveals direct electron transfer in methanotrophic consortia," Nature, Nature, vol. 526(7574), pages 531-535, October.
    3. Michael J. McAnulty & Venkata G. Poosarla & Kyoung-Yeol Kim & Ricardo Jasso-Chávez & Bruce E. Logan & Thomas K. Wood, 2017. "Electricity from methane by reversing methanogenesis," Nature Communications, Nature, vol. 8(1), pages 1-8, August.
    4. Mohamed F. Haroon & Shihu Hu & Ying Shi & Michael Imelfort & Jurg Keller & Philip Hugenholtz & Zhiguo Yuan & Gene W. Tyson, 2013. "Erratum: Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage," Nature, Nature, vol. 501(7468), pages 578-578, September.
    5. Antje Boetius & Katrin Ravenschlag & Carsten J. Schubert & Dirk Rickert & Friedrich Widdel & Armin Gieseke & Rudolf Amann & Bo Barker Jørgensen & Ursula Witte & Olaf Pfannkuche, 2000. "A marine microbial consortium apparently mediating anaerobic oxidation of methane," Nature, Nature, vol. 407(6804), pages 623-626, October.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Heleen T. Ouboter & Rob Mesman & Tom Sleutels & Jelle Postma & Martijn Wissink & Mike S. M. Jetten & Annemiek Ter Heijne & Tom Berben & Cornelia U. Welte, 2024. "Mechanisms of extracellular electron transfer in anaerobic methanotrophic archaea," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

    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. Heleen T. Ouboter & Rob Mesman & Tom Sleutels & Jelle Postma & Martijn Wissink & Mike S. M. Jetten & Annemiek Ter Heijne & Tom Berben & Cornelia U. Welte, 2024. "Mechanisms of extracellular electron transfer in anaerobic methanotrophic archaea," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Scott A. Klasek & Wei-Li Hong & Marta E. Torres & Stella Ross & Katelyn Hostetler & Alexey Portnov & Friederike Gründger & Frederick S. Colwell, 2021. "Distinct methane-dependent biogeochemical states in Arctic seafloor gas hydrate mounds," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    3. Mengxiong Wu & Jie Li & Andy O. Leu & Dirk V. Erler & Terra Stark & Gene W. Tyson & Zhiguo Yuan & Simon J. McIlroy & Jianhua Guo, 2022. "Anaerobic oxidation of propane coupled to nitrate reduction by a lineage within the class Symbiobacteriia," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. Yue Zheng & Huan Wang & Yan Liu & Peiyu Liu & Baoli Zhu & Yanning Zheng & Jinhua Li & Ludmila Chistoserdova & Zhiyong Jason Ren & Feng Zhao, 2024. "Electrochemically coupled CH4 and CO2 consumption driven by microbial processes," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    5. Yaohong Zhang & Fangyuan Wang, 2021. "Different impacts of an electron shuttle on nitrate- and nitrite-dependent anaerobic oxidation of methane in paddy soil," Plant, Soil and Environment, Czech Academy of Agricultural Sciences, vol. 67(5), pages 264-269.
    6. Marie C. Schoelmerich & Lynn Ly & Jacob West-Roberts & Ling-Dong Shi & Cong Shen & Nikhil S. Malvankar & Najwa Taib & Simonetta Gribaldo & Ben J. Woodcroft & Christopher W. Schadt & Basem Al-Shayeb & , 2024. "Borg extrachromosomal elements of methane-oxidizing archaea have conserved and expressed genetic repertoires," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    7. He, Yanying & Li, Yiming & Li, Xuecheng & Liu, Yingrui & Wang, Yufen & Guo, Haixiao & Hou, Jiaqi & Zhu, Tingting & Liu, Yiwen, 2023. "Net-zero greenhouse gas emission from wastewater treatment: Mechanisms, opportunities and perspectives," Renewable and Sustainable Energy Reviews, Elsevier, vol. 184(C).
    8. S. Emil Ruff & Pauline Humez & Isabella Hrabe Angelis & Muhe Diao & Michael Nightingale & Sara Cho & Liam Connors & Olukayode O. Kuloyo & Alan Seltzer & Samuel Bowman & Scott D. Wankel & Cynthia N. Mc, 2023. "Hydrogen and dark oxygen drive microbial productivity in diverse groundwater ecosystems," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. Sina Schorn & Jon S. Graf & Sten Littmann & Philipp F. Hach & Gaute Lavik & Daan R. Speth & Carsten J. Schubert & Marcel M. M. Kuypers & Jana Milucka, 2024. "Persistent activity of aerobic methane-oxidizing bacteria in anoxic lake waters due to metabolic versatility," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    10. Marie C. Schoelmerich & Heleen T. Ouboter & Rohan Sachdeva & Petar I. Penev & Yuki Amano & Jacob West-Roberts & Cornelia U. Welte & Jillian F. Banfield, 2022. "A widespread group of large plasmids in methanotrophic Methanoperedens archaea," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    11. Daniel S. Grégoire & Nikhil A. George & Laura A. Hug, 2023. "Microbial methane cycling in a landfill on a decadal time scale," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    12. Aracely Zambrano-Romero & Dario X. Ramirez-Villacis & Gabriel Trueba & Reyes Sierra-Alvarez & Antonio Leon-Reyes & Paul Cardenas & Valeria Ochoa-Herrera, 2022. "Dynamics of Microbial Communities during the Removal of Copper and Zinc in a Sulfate-Reducing Bioreactor with a Limestone Pre-Column System," IJERPH, MDPI, vol. 19(3), pages 1-18, January.
    13. Daidai Wu & Tiantian Sun & Rui Xie & Mengdi Pan & Xuegang Chen & Ying Ye & Lihua Liu & Nengyou Wu, 2019. "Characteristics of Authigenic Minerals around the Sulfate-Methane Transition Zone in the Methane-Rich Sediments of the Northern South China Sea: Inorganic Geochemical Evidence," IJERPH, MDPI, vol. 16(13), pages 1-18, June.
    14. Richard B. Coffin & Leila J. Hamdan & Joseph P. Smith & Paula S. Rose & Rebecca E. Plummer & Brandon Yoza & Ingo Pecher & Michael T. Montgomery, 2014. "Contribution of Vertical Methane Flux to Shallow Sediment Carbon Pools across Porangahau Ridge, New Zealand," Energies, MDPI, vol. 7(8), pages 1-25, August.
    15. Maria De La Fuente & Sandra Arndt & Héctor Marín-Moreno & Tim A. Minshull, 2022. "Assessing the Benthic Response to Climate-Driven Methane Hydrate Destabilisation: State of the Art and Future Modelling Perspectives," Energies, MDPI, vol. 15(9), pages 1-32, May.
    16. Rousseau, Raphaël & Etcheverry, Luc & Roubaud, Emma & Basséguy, Régine & Délia, Marie-Line & Bergel, Alain, 2020. "Microbial electrolysis cell (MEC): Strengths, weaknesses and research needs from electrochemical engineering standpoint," Applied Energy, Elsevier, vol. 257(C).
    17. Yunru Chen & Liang Dong & Weikang Sui & Mingyang Niu & Xingqian Cui & Kai-Uwe Hinrichs & Fengping Wang, 2024. "Cycling and persistence of iron-bound organic carbon in subseafloor sediments," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    18. Wang, Zixin & Wang, Tengfei & Si, Buchun & Watson, Jamison & Zhang, Yuanhui, 2021. "Accelerating anaerobic digestion for methane production: Potential role of direct interspecies electron transfer," Renewable and Sustainable Energy Reviews, Elsevier, vol. 145(C).
    19. Klaus Wallmann & Elena Pinero & Ewa Burwicz & Matthias Haeckel & Christian Hensen & Andrew Dale & Lars Ruepke, 2012. "The Global Inventory of Methane Hydrate in Marine Sediments: A Theoretical Approach," Energies, MDPI, vol. 5(7), pages 1-50, July.
    20. Jarrod J Scott & John A Breier & George W Luther III & David Emerson, 2015. "Microbial Iron Mats at the Mid-Atlantic Ridge and Evidence that Zetaproteobacteria May Be Restricted to Iron-Oxidizing Marine Systems," PLOS ONE, Public Library of Science, vol. 10(3), pages 1-19, March.

    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_s41467-023-41847-w. 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.