Structure and function of the soil microbiome underlying N2O emissions from global wetlands

Mohammad Bahram; Mikk Espenberg; Jaan Pärn; Laura Lehtovirta-Morley; Sten Anslan; Kuno Kasak; Urmas Kõljalg; Jaan Liira; Martin Maddison; Mari Moora; Ülo Niinemets; Maarja Öpik; Meelis Pärtel; Kaido Soosaar; Martin Zobel; Falk Hildebrand; Leho Tedersoo; Ülo Mander

doi:10.1038/s41467-022-29161-3

Structure and function of the soil microbiome underlying N₂O emissions from global wetlands

Mohammad Bahram^*, Mikk Espenberg, Jaan Pärn, Laura Lehtovirta-Morley, Sten Anslan, Kuno Kasak, Urmas Kõljalg, Jaan Liira, Martin Maddison, Mari Moora, Ülo Niinemets, Maarja Öpik, Meelis Pärtel, Kaido Soosaar, Martin Zobel, Falk Hildebrand, Leho Tedersoo, Ülo Mander

^*Corresponding author for this work

Aberdeen Centre For Environmental Sustainability

Research output: Contribution to journal › Article › peer-review

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Abstract

Wetland soils are the greatest source of nitrous oxide (N₂O), a critical greenhouse gas and ozone depleter released by microbes. Yet, microbial players and processes underlying the N₂O emissions from wetland soils are poorly understood. Using in situ N₂O measurements and by determining the structure and potential functional of microbial communities in 645 wetland soil samples globally, we examined the potential role of archaea, bacteria, and fungi in nitrogen (N) cycling and N₂O emissions. We show that N₂O emissions are higher in drained and warm wetland soils, and are correlated with functional diversity of microbes. We further provide evidence that despite their much lower abundance compared to bacteria, nitrifying archaeal abundance is a key factor explaining N₂O emissions from wetland soils globally. Our data suggest that ongoing global warming and intensifying environmental change may boost archaeal nitrifiers, collectively transforming wetland soils to a greater source of N₂O.

Original language	English
Article number	1430
Number of pages	10
Journal	Nature Communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-29161-3
Publication status	Published - 17 Mar 2022

Bibliographical note

Funding Information:
We thank O. Botsarova, L. Lopp, K. Kanger, R. Puusepp, E.J. Sova, H. Tamm, I. Varik for assistance in molecular laboratory analyses. We thank Lorenzo Menichetti for useful discussions. We are grateful to S. Egorov, I. Filippov, G. Gabiri, J. Gallagher, I. Gheorghe, W. Hartman, R. Iturraspe, J. Järveoja, A. Kull, F. Laggoun-Défarge, E. Lapshina, A. Lohila, C. Luswata, S. Mander, M. Metspalu, W. Mitsch, R. Moreton, K. Oopkaup, H. Óskarsson, J. Paal, T. Pae, E. Parrodi, S. Pellerin, F. Sabater, J. Salm; F. Sgouridis, D. Silveira Batista, K. Sohar, K. Storey, M. Tenywa; S. Ullah, E. Uuemaa, G. Veber, J. Villa, L. Yang and S.S. Zaw for assistance on study-site selection and field investigation. ME, JP, LT and UM were supported by the Ministry of Education and Science of Estonia (SF0180127s08 grant), the Estonian Research Council (IUT2-16, PUTJD619, PRG-352, PRG-609, and MOBERC20), EU through the European Regional Development Fund (Centres of Excellence ENVIRON, grant number TK-107, EcolChange, grant number TK-131, and the MOBTP101 returning researcher grant by the Mobilitas Pluss program); M.B. was supported by the Swedish Research Council Formas (2020-00807); J.P., K.K., and M.Ma. were supported by the European Social Fund (Doctoral School of Earth Sciences and Ecology); L.L.M. was supported by Royal Society Dorothy Hodgkin Research Fellowship (DH150187); F.H. was supported by European Research Council (ERC) Starting Grant (UNITY 852993), the BBSRC Institute Strategic Program Gut Microbes and Health BB/r012490/1, its constituent project BBS/e/F/000Pr10355, the European Union’s Horizon 2020 research and innovation program (grant agreement no. 948219).

Data Availability Statement

All metabarcoding sequences and associated metadata have been deposited in the European Bioinformatics Institute Sequence Read Archive database: https:// www.ncbi.nlm.nih.gov/bioproject/PRJNA718418; metagenomics sequences and associated metadata have been deposited at The European Nucleotide Archive under accession number https://www.ebi.ac.uk/ena/browser/view/PRJEB44414. Additional data generated in this study are provided in the Supplementary Information/Source Data file. SILVA database is available at https://www.arb-silva.de; UNITE database is available at https://unite.ut.ee/repository.php; Integrated Microbial Genomes is available at https:// img.jgi.doe.gov; eggnog database is available at http://eggnog5.embl.de/download/ eggnog_4.0/ Source data are provided with this paper.
The pipeline to process metabarcoding samples is available under https:// psbweb05.psb.ugent.be/lotus/downloads.html and https://doi.org/10.15156/bio/587450. The pipeline to process shotgun metagenomic samples is available under https:// github.com/hildebra/MATAFILER (https://doi.org/10.5281/zenodo.5831723).

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Cite this

Bahram, M., Espenberg, M., Pärn, J., Lehtovirta-Morley, L., Anslan, S., Kasak, K., Kõljalg, U., Liira, J., Maddison, M., Moora, M., Niinemets, Ü., Öpik, M., Pärtel, M., Soosaar, K., Zobel, M., Hildebrand, F., Tedersoo, L., & Mander, Ü. (2022). Structure and function of the soil microbiome underlying N₂O emissions from global wetlands. Nature Communications, 13(1), Article 1430. https://doi.org/10.1038/s41467-022-29161-3

Bahram, M, Espenberg, M, Pärn, J, Lehtovirta-Morley, L, Anslan, S, Kasak, K, Kõljalg, U, Liira, J, Maddison, M, Moora, M, Niinemets, Ü, Öpik, M, Pärtel, M, Soosaar, K, Zobel, M, Hildebrand, F, Tedersoo, L & Mander, Ü 2022, 'Structure and function of the soil microbiome underlying N₂O emissions from global wetlands', Nature Communications, vol. 13, no. 1, 1430. https://doi.org/10.1038/s41467-022-29161-3

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abstract = "Wetland soils are the greatest source of nitrous oxide (N2O), a critical greenhouse gas and ozone depleter released by microbes. Yet, microbial players and processes underlying the N2O emissions from wetland soils are poorly understood. Using in situ N2O measurements and by determining the structure and potential functional of microbial communities in 645 wetland soil samples globally, we examined the potential role of archaea, bacteria, and fungi in nitrogen (N) cycling and N2O emissions. We show that N2O emissions are higher in drained and warm wetland soils, and are correlated with functional diversity of microbes. We further provide evidence that despite their much lower abundance compared to bacteria, nitrifying archaeal abundance is a key factor explaining N2O emissions from wetland soils globally. Our data suggest that ongoing global warming and intensifying environmental change may boost archaeal nitrifiers, collectively transforming wetland soils to a greater source of N2O.",

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note = "Funding Information: We thank O. Botsarova, L. Lopp, K. Kanger, R. Puusepp, E.J. Sova, H. Tamm, I. Varik for assistance in molecular laboratory analyses. We thank Lorenzo Menichetti for useful discussions. We are grateful to S. Egorov, I. Filippov, G. Gabiri, J. Gallagher, I. Gheorghe, W. Hartman, R. Iturraspe, J. J{\"a}rveoja, A. Kull, F. Laggoun-D{\'e}farge, E. Lapshina, A. Lohila, C. Luswata, S. Mander, M. Metspalu, W. Mitsch, R. Moreton, K. Oopkaup, H. {\'O}skarsson, J. Paal, T. Pae, E. Parrodi, S. Pellerin, F. Sabater, J. Salm; F. Sgouridis, D. Silveira Batista, K. Sohar, K. Storey, M. Tenywa; S. Ullah, E. Uuemaa, G. Veber, J. Villa, L. Yang and S.S. Zaw for assistance on study-site selection and field investigation. ME, JP, LT and UM were supported by the Ministry of Education and Science of Estonia (SF0180127s08 grant), the Estonian Research Council (IUT2-16, PUTJD619, PRG-352, PRG-609, and MOBERC20), EU through the European Regional Development Fund (Centres of Excellence ENVIRON, grant number TK-107, EcolChange, grant number TK-131, and the MOBTP101 returning researcher grant by the Mobilitas Pluss program); M.B. was supported by the Swedish Research Council Formas (2020-00807); J.P., K.K., and M.Ma. were supported by the European Social Fund (Doctoral School of Earth Sciences and Ecology); L.L.M. was supported by Royal Society Dorothy Hodgkin Research Fellowship (DH150187); F.H. was supported by European Research Council (ERC) Starting Grant (UNITY 852993), the BBSRC Institute Strategic Program Gut Microbes and Health BB/r012490/1, its constituent project BBS/e/F/000Pr10355, the European Union{\textquoteright}s Horizon 2020 research and innovation program (grant agreement no. 948219). ",

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