Plant Soil Environ., 2021, 67(5):264-269 | DOI: 10.17221/579/2020-PSE

Different impacts of an electron shuttle on nitrate- and nitrite-dependent anaerobic oxidation of methane in paddy soilOriginal Paper

Yaohong Zhang*,1, Fangyuan Wang1,2
1 Collaborative Innovation Center on Forecast and Evaluation of Meteorological Disasters, Jiangsu Key Laboratory of Agricultural Meteorology, School of Applied Meteorology, Nanjing University of Information Science and Technology, Nanjing, P.R. China
2 State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, P.R. China

Quinones, redox-active functional groups in soil organic matter, can act as electron shuttles for microbial anaerobic transformation. Here, we used 13CH4 to trace 13C conversion (13C-CO2 + 13C-SOC) to investigate the influence of an artificial electron shuttle (anthraquinone-2,6-disulfonate, AQDS) on denitrifying anaerobic methane oxidation (DAMO) in paddy soil. The results showed that AQDS could act as the terminal electron acceptor for the anaerobic oxidation of methane (AOM) in the paddy field. Moreover, AQDS significantly enhanced nitrate-dependent AOM rates and the amount of 13C-CH4 assimilation to soil organic carbon (SOC), whereas it was remarkably reduced nitrite-dependent AOM rates and 13C assimilation. Ultimately, AQDS notably increased the total DAMO rates and 13C assimilation to SOC. However, the electron shuttle did not change the percentage of 13C-SOC in total 13C-CH4 conversion. These results suggest that electron shuttles in the natural organic matter might be able to offset methane emission by facilitating AOM coupled with the denitrification process.

Keywords: global warming; microbial anaerobic metabolism; nitrogen fertilisation; 13CO2 production

Published: May 31, 2021  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Zhang Y, Wang F. Different impacts of an electron shuttle on nitrate- and nitrite-dependent anaerobic oxidation of methane in paddy soil. Plant Soil Environ. 2021;67(5):264-269. doi: 10.17221/579/2020-PSE.
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Aranda-Tamaura C., Estrada-Alvarado M.I., Texier A.-C., Cuervo F., Gómez J., Cervantes F.J. (2007): Effects of different quinoid redox mediators on the removal of sulphide and nitrate via denitrification. Chemosphere, 69: 1722-1727. Go to original source... Go to PubMed...
    2. Bai Y.N., Wang X.N., Wu J., Lu Y.Z., Fu L., Zhang F., Lau T.C., Zeng R.J. (2019): Humic substances as electron acceptors for anaerobic oxidation of methane driven by ANME-2d. Water Research, 164: 114935. Go to original source... Go to PubMed...
    3. Cervantes F.J., van der Velde S., Lettinga G., Field J.A. (2000): Quinones as terminal electron acceptors for anaerobic microbial oxidation of phenolic compounds. Biodegradation, 11: 313-321. Go to original source... Go to PubMed...
    4. Ding J., Fu L., Ding Z.W., Lu Y.Z., Cheng S.H., Zeng R.J. (2016): Environmental evaluation of coexistence of denitrifying anaerobic methane-oxidizing archaea and bacteria in a paddy field. Applied Microbiology and Biotechnology, 100: 439-446. Go to original source... Go to PubMed...
    5. Ettwig K.F., Butler M.K., Le Paslier D., Pelletier E., Mangenot S., Kuypers M.M., Schreiber F., Dutilh B.E., Zedelius J., de Beer D., Gloerich J., Wessels H.J., van Alen T., Luesken F., Wu M.L., van de Pas-Schoonen K.T., Opden Camp H.J., Janssen-Megens E.M., Francoijs K.J., Stunnenberg H., Weissenbach J., Jetten M.S., Strous M. (2010): Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature, 464: 543-548. Go to original source... Go to PubMed...
    6. Fan L.C., Dippold M.A., Ge T.D., Wu J.S., Thiel V., Kuzyakov Y., Dorodnikov M. (2020): Anaerobic oxidation of methane in paddy soil: role of electron acceptors and fertilization in mitigating CH4 fluxes. Soil Biology and Biochemistry, 141: 107685. Go to original source...
    7. Gupta V., Smemo K.A., Yavitt J.B., Fowle D., Branfireun B., Basiliko N. (2013): Stable isotopes reveal widespread anaerobic methane oxidation across latitude and peatland type. Environmental Science and Technology, 47: 8273-8279. Go to original source... Go to PubMed...
    8. Haroon M.F., Hu S.H., Shi Y., Imelfort M., Keller J., Hugenholtz P., Yuan Z.G., Tyson G.W. (2013): Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature, 500: 567-570. Go to original source... Go to PubMed...
    9. He Q.X., Yu L.P., Li J.B., He D., Cai X.X., Zhou S.G. (2019): Electron shuttles enhance anaerobic oxidation of methane coupled to iron(III) reduction. Science of The Total Environment, 688: 664-672. Go to original source... Go to PubMed...
    10. He Z.F., Wang J.Q., Zhang X., Cai C.Y., Geng S., Zheng P., Xu X.H., Hu B.L. (2015): Nitrogen removal from wastewater by anaerobic methane-driven denitrification in a lab-scale reactor: heterotrophic denitrifiers associated with denitrifying methanotrophs. Applied Microbiology and Biotechnology, 99: 10853-10860. Go to original source... Go to PubMed...
    11. Knittel K., Boetius A. (2009): Anaerobic oxidation of methane: progress with an unknown process. Annual Review of Microbiology, 63: 311-334. Go to original source... Go to PubMed...
    12. McGlynn S.E., Chadwick G.L., Kempes C.P., Orphan V.J. (2015): Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature, 526: 531-535. Go to original source... Go to PubMed...
    13. Mujiyo M., Sunarminto B.H., Hanudin E., Widada J., Syamsiyah J. (2017): Methane production potential of soil profile in organic paddy field. Soil and Water Research, 12: 212-219. Go to original source...
    14. Scheller S., Yu H., Chadwick G.L., McGlynn S.E., Orphan V.J. (2016): Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science, 351: 703-707. Go to original source... Go to PubMed...
    15. Shen L.D., Huang Q., He Z.F., Lian X., Liu S.A., He Y.F., Lou L.P., Xu X.Y., Zheng P., Hu B.I. (2015): Vertical distribution of nitrite-dependent anaerobic methane-oxidising bacteria in natural freshwater wetland soils. Applied Microbiology and Biotechnology, 991: 349-357. Go to original source... Go to PubMed...
    16. Smemo K.A., Yavitt J.B. (2011): Anaerobic oxidation of methane: an underappreciated aspect of methane cycling in peatland ecosystems? Biogeosciences, 8: 779-793. Go to original source...
    17. Vaksmaa A., Guerrero-Cruz S., van Alen T.A., Cremers G., Ettwig K.F., Lüke C., Jetten M.S.M. (2017): Enrichment of anaerobic nitrate-dependent methanotrophic 'Candidatus Methanoperedens nitroreducens' archaea from an Italian paddy field soil. Applied Microbiology and Biotechnology, 101: 7075-7084. Go to original source... Go to PubMed...
    18. Valenzuela E.I., Padilla-Loma C., Gómez-Hernández N., LópezLozano N.E., Casas-Flores S., Cervantes F.J. (2020): Humic substances mediate anaerobic methane oxidation linked to nitrous oxide reduction in wetland sediments. Frontiers in Microbiology, 11: 587. Go to original source... Go to PubMed...
    19. Valenzuela E.I., Prieto-Davó A., López-Lozano N.E., HernándezEligio A., Vega-Alvarado L., Juárez K., García-González A.S., López M.G., Cervantes F.J. (2017): Anaerobic methane oxidation driven by microbial reduction of natural organic matter in a tropical wetland. Applied and Environmental Microbiology, 83: AEM.00645-17. Go to original source... Go to PubMed...
    20. Wang J.Q., Cai C.Y., Li Y.F., Hua M.L., Wang J.R., Yang H.R., Zheng P., Hu B.L. (2019): Denitrifying anaerobic methane oxidation: a previously overlooked methane sink in intertidal zone. Environmental Science and Technology, 53: 203-212. Go to original source... Go to PubMed...
    21. Wu Y.D., Liu T.X., Li X.M., Li F.B. (2014): Exogenous electron shuttle-mediated extracellular electron transfer of Shewanella putrefaciens 200: electrochemical parameters and thermodynamics. Environmental Science and Technology, 48: 9306-9314. Go to original source... Go to PubMed...

    This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content