Diverse sediment microbiota shape methane emission temperature sensitivity in Arctic lakes

Creators: Emerson, Joanne B.; Varner, Ruth K.; Wik, Martin; Parks, Donovan H.; Neumann, Rebecca B.; Johnson, Joel E.; Singleton, Caitlin M.; Woodcroft, Ben J.; Tollerson, Rodney; Owusu-Dommey, Akosua; Binder, Morgan; Freitas, Nancy L.; Crill, Patrick M.; Saleska, Scott R.; Tyson, Gene W.; Rich, Virginia I.

Abstract

Northern post-glacial lakes are significant, increasing sources of atmospheric carbon through ebullition (bubbling) of microbially-produced methane (CH₄) from sediments. Ebullitive CH₄ flux correlates strongly with temperature, reflecting that solar radiation drives emissions. However, here we show that the slope of the temperature-CH₄ flux relationship differs spatially across two post-glacial lakes in Sweden. We compared these CH₄ emission patterns with sediment microbial (metagenomic and amplicon), isotopic, and geochemical data. The temperature-associated increase in CH₄ emissions was greater in lake middles—where methanogens were more abundant—than edges, and sediment communities were distinct between edges and middles. Microbial abundances, including those of CH₄-cycling microorganisms and syntrophs, were predictive of porewater CH₄ concentrations. Results suggest that deeper lake regions, which currently emit less CH₄ than shallower edges, could add substantially to CH₄ emissions in a warmer Arctic and that CH₄ emission predictions may be improved by accounting for spatial variations in sediment microbiota.

Additional Information

© The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 03 March 2020; Accepted 07 July 2021; Published 05 October 2021. We would like to acknowledge the following funding in support of this project: U.S. Department of Energy grants (DE-SC0010580 and DE-SC0016440, Co-lead PI Rich; DE-SC0010338 and DE-SC0019063, PI Neumann; DE-SC0020163, Co-PI Emerson), U.S. National Science Foundation grants (the Northern Ecosystems Research for Undergraduates program (NERU) EAR-1063037, PI Varner, MacroSystems Biology grant EF #1241037, PI Varner, and the EMERGE Biology Integration Institute grant #2022070, PI Rich), the Swedish Research Council grants to P. Crill (2007-4547 and 2013-5562), and the UC Davis College of Agricultural and Environmental Sciences and Department of Plant Pathology (laboratory start-up funds to JBE). Thanks to staff at the Polar Research Secretariat's Abisko Research Station (ANS). Thanks to Kaitlyn Steele, Florencia Fahnestock, Kiley Remiszewski, Carmody McCalley, and NERU participants Sophia Burke, Joel DeStasio, Lance Erickson, and Madison Halloran for assistance in sample collection and analysis, Jacob Setera and Steve Phillips (UNH) for assistance with the CHNS elemental analysis, Peter Sternes for assistance with data upload to NCBI, Joachim Jansen for helping us to think critically about the ebullition results, and the IsoGenie Project Team for discussion of results. Data availability: Sequencing data are available at NCBI under BioProject PRJNA667178 and also here: https://isogenie-db.asc.ohio-state.edu/datasources#lake_data (from the IsoGenie link, note that the two folders with MAGs are based on initial taxonomy; some MAGs subsequently determined to be archaea are in the bacteria folder and vice versa). NCBI accession numbers are as follows: raw 16S rRNA gene amplicon sequences SRX10114484–SRX10114504, raw metagenomic sequences SRX10063754–SRX10063756, and MAGs JAFNEO000000000–JAFNIC000000000. Other raw data and relevant processed data are provided in supplementary tables and/or associated with prior publications, as cited in the paper. Data underlying Figs. 1–4 can be found as follows: Fig. 1A–C (Supplementary Table 2), Fig. 2C, D (Supplementary Table 5), Fig. 3 (Supplementary Table 10), and Fig. 4A–C (raw data in Supplementary Tables 4–5, relevant processed data in Supplementary Tables 13 and 16). Author Contributions: J.B.E., R.K.V., and V.I.R. designed the study, J.B.E. wrote and R.K.V. and V.I.R. substantially revised the paper. R.K.V., M.W., and N.L.F. collected the samples and J.B.E., R.K.V., M.W., J.E.J., A.O.D., M.B., and N.L.F. performed laboratory sample processing. M.W., R.K.V., and P.M.C. generated and analyzed ebullitive CH4 flux data, R.K.V. and J.E.J. generated and analyzed geochemical data, R.K.V. and N.L.F. performed and analyzed ex situ incubations, R.B.N. performed the isotopic and mass balance calculations, J.B.E., D.H.P., C.M.S., and B.J.W. processed and J.B.E. and R.T. II analyzed microbial community sequencing data, J.B.E. reconstructed microbial metabolic pathways with guidance from D.H.P., C.M.S., B.J.W., and G.W.T., and J.B.E. performed the statistical modeling with guidance from S.R.S. J.B.E., R.K.V., M.W., D.H.P., R.B.N., J.E.J., C.M.S., B.J.W., R.T. II, N.L.F., A.O.D., M.B., and V.I.R. performed the data analysis. All authors contributed to project discussions, edited the paper, and approved the final version of the paper. The authors declare no competing interests. Peer review information: Nature Communications thanks Stephanie Carr, Florence Schubotz, and Cornelia Welte for their contributions to the peer review of this work.

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