Diverse sediment microbiota shape methane emission temperature sensitivity in Arctic lakes

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

doi:10.1038/s41467-021-25983-9

Diverse sediment microbiota shape methane emission temperature sensitivity in Arctic lakes

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

^*Corresponding author for this work

Research output: Contribution to journal › Journal article › Research › peer-review

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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.

Original language	English
Article number	5815
Journal	Nature Communications
Volume	12
Issue number	1
ISSN	2041-1723
DOIs	https://doi.org/10.1038/s41467-021-25983-9
Publication status	Published - Dec 2021

Bibliographical note

Funding Information:
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; DESC0010338 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 Fah-nestock, 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.

Publisher Copyright:
© 2021, The Author(s).

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Emerson, J. B., Varner, R. K., Wik, M., Parks, D. H., Neumann, R. B., Johnson, J. E., Singleton, C. M., Woodcroft, B. J., Tollerson, R., Owusu-Dommey, A., Binder, M., Freitas, N. L., Crill, P. M., Saleska, S. R., Tyson, G. W., & Rich, V. I. (2021). Diverse sediment microbiota shape methane emission temperature sensitivity in Arctic lakes. Nature Communications, 12(1), Article 5815. https://doi.org/10.1038/s41467-021-25983-9

@article{b85a70ee5a3c4c76b7549603ee06e2d4,

title = "Diverse sediment microbiota shape methane emission temperature sensitivity in Arctic lakes",

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.",

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

note = "Funding Information: 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; DESC0010338 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{\textquoteright}s Abisko Research Station (ANS). Thanks to Kaitlyn Steele, Florencia Fah-nestock, 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. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

month = dec,

doi = "10.1038/s41467-021-25983-9",

language = "English",

volume = "12",

journal = "Nature Communications",

issn = "2041-1723",

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Emerson, JB, Varner, RK, Wik, M, Parks, DH, Neumann, RB, Johnson, JE, Singleton, CM, Woodcroft, BJ, Tollerson, R, Owusu-Dommey, A, Binder, M, Freitas, NL, Crill, PM, Saleska, SR, Tyson, GW & Rich, VI 2021, 'Diverse sediment microbiota shape methane emission temperature sensitivity in Arctic lakes', Nature Communications, vol. 12, no. 1, 5815. https://doi.org/10.1038/s41467-021-25983-9

TY - JOUR

T1 - Diverse sediment microbiota shape methane emission temperature sensitivity in Arctic lakes

AU - Emerson, Joanne B.

AU - Varner, Ruth K.

AU - Wik, Martin

AU - Parks, Donovan H.

AU - Neumann, Rebecca B.

AU - Johnson, Joel E.

AU - Singleton, Caitlin M.

AU - Woodcroft, Ben J.

AU - Tollerson, Rodney

AU - Owusu-Dommey, Akosua

AU - Binder, Morgan

AU - Freitas, Nancy L.

AU - Crill, Patrick M.

AU - Saleska, Scott R.

AU - Tyson, Gene W.

AU - Rich, Virginia I.

N1 - Funding Information: 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; DESC0010338 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 Fah-nestock, 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. Publisher Copyright: © 2021, The Author(s).

PY - 2021/12

Y1 - 2021/12

N2 - 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.

AB - 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.

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U2 - 10.1038/s41467-021-25983-9

DO - 10.1038/s41467-021-25983-9

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SN - 2041-1723

VL - 12

JO - Nature Communications

JF - Nature Communications

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ER -

Diverse sediment microbiota shape methane emission temperature sensitivity in Arctic lakes

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