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Coupled abiotic-biotic cycling of nitrous oxide in tropical peatlands

Nature Ecology & Evolution volume 6, pages 1881–1890 (2022)Cite this article

Subjects

Abstract

Atmospheric nitrous oxide (N2O) is a potent greenhouse gas thought to be mainly derived from microbial metabolism as part of the denitrification pathway. Here we report that in unexplored peat soils of Central and South America, N2O production can be driven by abiotic reactions (≤98%) highly competitive to their enzymatic counterparts. Extracted soil iron positively correlated with in situ abiotic N2O production determined by isotopic tracers. Moreover, we found that microbial N2O reduction accompanied abiotic production, essentially closing a coupled abiotic-biotic N2O cycle. Anaerobic N2O consumption occurred ubiquitously (pH 6.4–3.7), with proportions of diverse clade II N2O reducers increasing with consumption rates. Our findings show that denitrification in tropical peat soils is not a purely biological process but rather a ‘mosaic’ of abiotic and biotic reduction reactions. We predict that hydrological and temperature fluctuations differentially affect abiotic and biotic drivers and further contribute to the high N2O flux variation in the region.

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Fig. 1: Contribution of abiotic and biotic reactions to overall N2O production in tropical peatlands.
Fig. 2: Isotopic enrichment in molecular nitrogen during in situ incubations of (15N)2O with anoxic peat soil.
Fig. 3: Microbial N2O consumption and abiotic N2O production (bars) along with nosZ gene quantities (open and filled circles).
Fig. 4: NosZ phylogeny and taxonomy in tropical peat soils.
Fig. 5: Schematic representation of denitrification pathways in tropical peatlands.

Data availability

All data to evaluate the conclusions of the study are present in the paper and its Supplementary Information and can be found in the Figshare repository (https://doi.org/10.6084/m9.figshare.19552588.v1). Genomic data have been deposited in the GenBank, EMBL, and DDBJ databases under accession: SAMN27959396, SAMN27959397, SAMN27959398, SAMN27959399, SAMN27959400, SAMN27959401, SAMN27959402, SAMN27959403, SAMN27959404, SAMN27959405, SAMN27959406, SAMN27959407, SAMN27959408, SAMN27959409, SAMN27959410, SAMN27959411, SAMN27959412, SAMN27959413, SAMN27959414, SAMN27959415, SAMN27959416, SAMN27959417, SAMN27959418, SAMN27959419, SAMN27959420, SAMN27959421, SAMN27959422, SAMN27959423, SAMN27959424, SAMN27959425, SAMN27959426, SAMN27959427, SAMN27959428, SAMN27959429, SAMN27959430, SAMN27959431, SAMN27959432, SAMN27959433, SAMN27959434, SAMN27959435, SAMN27959436, SAMN27959437, SAMN27959438, SAMN27959439, SAMN27959440, SAMN27959441, SAMN27959442 and SAMN27959443

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Acknowledgements

We acknowledge R. T. Espinoza, T. P. Gomez, D. Reyna, B. Crnobrna, O. Lähteenoja, K. Arbaiza, A. H. Carmona, P. Fonteboa, R. C. Chaves, J. R. Trucios, C. M. Cadillo-Quiroz, the UFSJ Graduate Program in Geography (PPGEOG) and the Office for International Affairs (ASSIN/UFSJ) for assistance and help during stages of field work. We also thank W. Nitschke (CNRS/BIP) for discussions, M. Abdalla for efforts supporting this effort at the USAID-GDR program at ASU, and the USAID missions in Peru and Brazil.

This study was funded by an NSF-DEB award (no. 1355066) and a SOLS -KED ASU award (ECR A548 HC) to H.C-Q, a Global Development Research Scholarship to S.B. and H.C-Q in partnership with the USAID-Global Development Lab and the Peruvian and Brazilian USAID missions. S.B. also received support from the Lewis & Clark Fund for Exploration and Field Research in Astrobiology provided by the American Philosophical Society (APS). N.E.O. was funded in part by the DOE Great Lakes Bioenergy Research Center (DOE BER Office of Science DE-SC0018409).

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Author notes

  1. Steffen Buessecker

    Present address: Department of Earth System Science, Stanford University, Stanford, CA, USA

Authors and Affiliations

  1. School of Life Sciences, Arizona State University, Tempe, AZ, USA

    Steffen Buessecker, Analissa F. Sarno, Mark C. Reynolds, Marc Fontánez Ortiz, Sharon J. Hall & Hinsby Cadillo-Quiroz

  2. Biodesign Institute, Arizona State University, Tempe, AZ, USA

    Ramani Chavan, Jin Park & Hinsby Cadillo-Quiroz

  3. Environmental Pollution Research Center (CICA), University of Costa Rica, Montes de Oca, Costa Rica

    Ana G. Pérez-Castillo

  4. School of Forestry and Environmental Sciences, Ucayali National University, Ucayali, Peru

    Grober Panduro Pisco

  5. Laboratory of Soil Research, Research Institute of Amazonia’s Natural Resources, National University of the Peruvian Amazon, Iquitos, Loreto, Peru

    José David Urquiza-Muñoz

  6. School of Forestry, National University of the Peruvian Amazon, Iquitos, Loreto, Peru

    José David Urquiza-Muñoz

  7. Department for Biogeochemical Processes, Max Planck Institute for Biogeochemistry, Jena, Germany

    José David Urquiza-Muñoz

  8. Mamiraua Institute for Sustainable Development, Amazonia, Brazil

    Leonardo P. Reis & Jefferson Ferreira-Ferreira

  9. Normal Superior School, Amazonas State University, Manaus, Amazonia, Brazil

    Jair M. Furtunato Maia

  10. National Institute of Amazonian Research, Manaus, Amazonia, Brazil

    Jair M. Furtunato Maia

  11. School of Electrical, Computer and Energy Engineering, Arizona State University, Tempe, AZ, USA

    Keith E. Holbert

  12. College of Integrative Sciences and Arts, Arizona State University, Mesa, AZ, USA

    C. Ryan Penton

  13. Department of Integrative Biology, Michigan State University, East Lansing, MI, USA

    Hasand Gandhi & Nathaniel E. Ostrom

  14. DOE Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, USA

    Hasand Gandhi & Nathaniel E. Ostrom

  15. Applied Limnology Laboratory, Department of Geosciences, Federal University of São João del-Rei, São João del-Rei, Brazil

    Iola G. Boëchat & Björn Gücker

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  1. Steffen Buessecker
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  2. Analissa F. Sarno
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  19. Nathaniel E. Ostrom
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S.B., N.E.O. and H.C.-Q. designed the study; S.B. conducted the field work with essential contributions from A.G.P-C, G.P.P., J.D.U.-M., L.P.R., J.F.-F., J.M.F.M., I.G.B. and B.G.; S.B., M.F.O., A.F.S., M.C.R., R.C. and J.P. performed laboratory experiments and molecular analyses; S.J.H. supported the NO analysis; K.E.H. conducted soil gamma sterilization; C.R.P. supported qPCR analysis. H.G. analysed isotopic abundances of gas samples; S.B., I.G.B., B.G., N.E.O. and H.C.-Q. performed the data analysis. S.B. and H.C.-Q. wrote the manuscript, and all co-authors contributed to the final version of the paper.

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Correspondence to Hinsby Cadillo-Quiroz.

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Nature Ecology & Evolution thanks Luiz Domeignoz, Maija Marushchak and Yit Arn Teh for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Overall workflow of incubations in the field and lab.

This workflow was applied for each peatland. Derived data sets are in circles. At the end of the incubations, microcosms were opened, and soil dry mass was determined for each replicate in order to normalize rates. Headspace of lab incubations was sporadically tested for CO2 accumulation to verify absence of biological activity.

Supplementary information

Supplementary Information

Supplementary Text (activation energy and N2O flux and carbon mineralization calculations), Figs. 1–6, Tables 1–6 and References.

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Buessecker, S., Sarno, A.F., Reynolds, M.C. et al. Coupled abiotic-biotic cycling of nitrous oxide in tropical peatlands. Nat Ecol Evol 6, 1881–1890 (2022). https://doi.org/10.1038/s41559-022-01892-y

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