Climate drivers alter nitrogen availability in surface peat and decouple N2 fixation from CH4 oxidation in the Sphagnum moss microbiome

Caitlin Petro; Alyssa A. Carrell; Rachel M. Wilson; Katherine Duchesneau; Sekou Noble-Kuchera; Tianze Song; Colleen M. Iversen; Joanne Childs; Geoff Schwaner; Jeffrey P. Chanton; Richard J. Norby; Paul J. Hanson; Jennifer B. Glass; David J. Weston; Joel E. Kostka

doi:10.1111/gcb.16651

Climate drivers alter nitrogen availability in surface peat and decouple N₂ fixation from CH₄ oxidation in the Sphagnum moss microbiome

Caitlin Petro, Alyssa A. Carrell, Rachel M. Wilson, Katherine Duchesneau, Sekou Noble-Kuchera, Tianze Song, Colleen M. Iversen, Joanne Childs, Geoff Schwaner, Jeffrey P. Chanton, Richard J. Norby, Paul J. Hanson, Jennifer B. Glass, David J. Weston, Joel E. Kostka

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

7 Scopus citations

Abstract

Peat mosses (Sphagnum spp.) are keystone species in boreal peatlands, where they dominate net primary productivity and facilitate the accumulation of carbon in thick peat deposits. Sphagnum mosses harbor a diverse assemblage of microbial partners, including N₂-fixing (diazotrophic) and CH₄-oxidizing (methanotrophic) taxa that support ecosystem function by regulating transformations of carbon and nitrogen. Here, we investigate the response of the Sphagnum phytobiome (plant + constituent microbiome + environment) to a gradient of experimental warming (+0°C to +9°C) and elevated CO₂ (+500 ppm) in an ombrotrophic peatland in northern Minnesota (USA). By tracking changes in carbon (CH₄, CO₂) and nitrogen (NH₄-N) cycling from the belowground environment up to Sphagnum and its associated microbiome, we identified a series of cascading impacts to the Sphagnum phytobiome triggered by warming and elevated CO₂. Under ambient CO₂, warming increased plant-available NH₄-N in surface peat, excess N accumulated in Sphagnum tissue, and N₂ fixation activity decreased. Elevated CO₂ offset the effects of warming, disrupting the accumulation of N in peat and Sphagnum tissue. Methane concentrations in porewater increased with warming irrespective of CO₂ treatment, resulting in a ~10× rise in methanotrophic activity within Sphagnum from the +9°C enclosures. Warming's divergent impacts on diazotrophy and methanotrophy caused these processes to become decoupled at warmer temperatures, as evidenced by declining rates of methane-induced N₂ fixation and significant losses of keystone microbial taxa. In addition to changes in the Sphagnum microbiome, we observed ~94% mortality of Sphagnum between the +0°C and +9°C treatments, possibly due to the interactive effects of warming on N-availability and competition from vascular plant species. Collectively, these results highlight the vulnerability of the Sphagnum phytobiome to rising temperatures and atmospheric CO₂ concentrations, with significant implications for carbon and nitrogen cycling in boreal peatlands.

Original language	English
Pages (from-to)	3159-3176
Number of pages	18
Journal	Global Change Biology
Volume	29
Issue number	11
DOIs	https://doi.org/10.1111/gcb.16651
State	Published - Jun 2023

Funding

This work was supported by the National Science Foundation (DEB grant no. 1754756). The SPRUCE project is supported by the U.S. Department of Energy's Office of Science, Biological, and Environmental Research (DOE BER) and the USDA Forest Service. UT‐Battelle, LLC, manages Oak Ridge National Laboratory for the U.S. Department of Energy under contract DE‐AC05‐00OR22725. We thank Allison Fortner, Deanne Brice, and John Latimer for assistance with the ion‐exchange resins, and Verity Salmon for helpful discussions about the calculation of ecosystem‐scaled rates.

Funders	Funder number
DOE BER
Environmental Research
National Science Foundation
U.S. Department of Energy
Division of Environmental Biology	1754756
U.S. Forest Service	DE‐AC05‐00OR22725

Keywords

Sphagnum moss
boreal peatland
climate change
diazotroph
elevated CO
methane
methanotroph
nitrogen
plant microbiomes
warming

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1111/gcb.16651

Cite this

Petro, C., Carrell, A. A., Wilson, R. M., Duchesneau, K., Noble-Kuchera, S., Song, T., Iversen, C. M., Childs, J., Schwaner, G., Chanton, J. P., Norby, R. J., Hanson, P. J., Glass, J. B., Weston, D. J., & Kostka, J. E. (2023). Climate drivers alter nitrogen availability in surface peat and decouple N₂ fixation from CH₄ oxidation in the Sphagnum moss microbiome. Global Change Biology, 29(11), 3159-3176. https://doi.org/10.1111/gcb.16651

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title = "Climate drivers alter nitrogen availability in surface peat and decouple N2 fixation from CH4 oxidation in the Sphagnum moss microbiome",

abstract = "Peat mosses (Sphagnum spp.) are keystone species in boreal peatlands, where they dominate net primary productivity and facilitate the accumulation of carbon in thick peat deposits. Sphagnum mosses harbor a diverse assemblage of microbial partners, including N2-fixing (diazotrophic) and CH4-oxidizing (methanotrophic) taxa that support ecosystem function by regulating transformations of carbon and nitrogen. Here, we investigate the response of the Sphagnum phytobiome (plant + constituent microbiome + environment) to a gradient of experimental warming (+0°C to +9°C) and elevated CO2 (+500 ppm) in an ombrotrophic peatland in northern Minnesota (USA). By tracking changes in carbon (CH4, CO2) and nitrogen (NH4-N) cycling from the belowground environment up to Sphagnum and its associated microbiome, we identified a series of cascading impacts to the Sphagnum phytobiome triggered by warming and elevated CO2. Under ambient CO2, warming increased plant-available NH4-N in surface peat, excess N accumulated in Sphagnum tissue, and N2 fixation activity decreased. Elevated CO2 offset the effects of warming, disrupting the accumulation of N in peat and Sphagnum tissue. Methane concentrations in porewater increased with warming irrespective of CO2 treatment, resulting in a ~10× rise in methanotrophic activity within Sphagnum from the +9°C enclosures. Warming's divergent impacts on diazotrophy and methanotrophy caused these processes to become decoupled at warmer temperatures, as evidenced by declining rates of methane-induced N2 fixation and significant losses of keystone microbial taxa. In addition to changes in the Sphagnum microbiome, we observed ~94% mortality of Sphagnum between the +0°C and +9°C treatments, possibly due to the interactive effects of warming on N-availability and competition from vascular plant species. Collectively, these results highlight the vulnerability of the Sphagnum phytobiome to rising temperatures and atmospheric CO2 concentrations, with significant implications for carbon and nitrogen cycling in boreal peatlands.",

keywords = "Sphagnum moss, boreal peatland, climate change, diazotroph, elevated CO, methane, methanotroph, nitrogen, plant microbiomes, warming",

author = "Caitlin Petro and Carrell, {Alyssa A.} and Wilson, {Rachel M.} and Katherine Duchesneau and Sekou Noble-Kuchera and Tianze Song and Iversen, {Colleen M.} and Joanne Childs and Geoff Schwaner and Chanton, {Jeffrey P.} and Norby, {Richard J.} and Hanson, {Paul J.} and Glass, {Jennifer B.} and Weston, {David J.} and Kostka, {Joel E.}",

note = "Publisher Copyright: {\textcopyright} 2023 John Wiley & Sons Ltd.",

year = "2023",

month = jun,

doi = "10.1111/gcb.16651",

language = "English",

volume = "29",

pages = "3159--3176",

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Petro, C, Carrell, AA, Wilson, RM, Duchesneau, K, Noble-Kuchera, S, Song, T, Iversen, CM, Childs, J, Schwaner, G, Chanton, JP, Norby, RJ, Hanson, PJ, Glass, JB, Weston, DJ & Kostka, JE 2023, 'Climate drivers alter nitrogen availability in surface peat and decouple N₂ fixation from CH₄ oxidation in the Sphagnum moss microbiome', Global Change Biology, vol. 29, no. 11, pp. 3159-3176. https://doi.org/10.1111/gcb.16651

TY - JOUR

T1 - Climate drivers alter nitrogen availability in surface peat and decouple N2 fixation from CH4 oxidation in the Sphagnum moss microbiome

AU - Petro, Caitlin

AU - Carrell, Alyssa A.

AU - Wilson, Rachel M.

AU - Duchesneau, Katherine

AU - Noble-Kuchera, Sekou

AU - Song, Tianze

AU - Iversen, Colleen M.

AU - Childs, Joanne

AU - Schwaner, Geoff

AU - Chanton, Jeffrey P.

AU - Norby, Richard J.

AU - Hanson, Paul J.

AU - Glass, Jennifer B.

AU - Weston, David J.

AU - Kostka, Joel E.

PY - 2023/6

Y1 - 2023/6

N2 - Peat mosses (Sphagnum spp.) are keystone species in boreal peatlands, where they dominate net primary productivity and facilitate the accumulation of carbon in thick peat deposits. Sphagnum mosses harbor a diverse assemblage of microbial partners, including N2-fixing (diazotrophic) and CH4-oxidizing (methanotrophic) taxa that support ecosystem function by regulating transformations of carbon and nitrogen. Here, we investigate the response of the Sphagnum phytobiome (plant + constituent microbiome + environment) to a gradient of experimental warming (+0°C to +9°C) and elevated CO2 (+500 ppm) in an ombrotrophic peatland in northern Minnesota (USA). By tracking changes in carbon (CH4, CO2) and nitrogen (NH4-N) cycling from the belowground environment up to Sphagnum and its associated microbiome, we identified a series of cascading impacts to the Sphagnum phytobiome triggered by warming and elevated CO2. Under ambient CO2, warming increased plant-available NH4-N in surface peat, excess N accumulated in Sphagnum tissue, and N2 fixation activity decreased. Elevated CO2 offset the effects of warming, disrupting the accumulation of N in peat and Sphagnum tissue. Methane concentrations in porewater increased with warming irrespective of CO2 treatment, resulting in a ~10× rise in methanotrophic activity within Sphagnum from the +9°C enclosures. Warming's divergent impacts on diazotrophy and methanotrophy caused these processes to become decoupled at warmer temperatures, as evidenced by declining rates of methane-induced N2 fixation and significant losses of keystone microbial taxa. In addition to changes in the Sphagnum microbiome, we observed ~94% mortality of Sphagnum between the +0°C and +9°C treatments, possibly due to the interactive effects of warming on N-availability and competition from vascular plant species. Collectively, these results highlight the vulnerability of the Sphagnum phytobiome to rising temperatures and atmospheric CO2 concentrations, with significant implications for carbon and nitrogen cycling in boreal peatlands.

AB - Peat mosses (Sphagnum spp.) are keystone species in boreal peatlands, where they dominate net primary productivity and facilitate the accumulation of carbon in thick peat deposits. Sphagnum mosses harbor a diverse assemblage of microbial partners, including N2-fixing (diazotrophic) and CH4-oxidizing (methanotrophic) taxa that support ecosystem function by regulating transformations of carbon and nitrogen. Here, we investigate the response of the Sphagnum phytobiome (plant + constituent microbiome + environment) to a gradient of experimental warming (+0°C to +9°C) and elevated CO2 (+500 ppm) in an ombrotrophic peatland in northern Minnesota (USA). By tracking changes in carbon (CH4, CO2) and nitrogen (NH4-N) cycling from the belowground environment up to Sphagnum and its associated microbiome, we identified a series of cascading impacts to the Sphagnum phytobiome triggered by warming and elevated CO2. Under ambient CO2, warming increased plant-available NH4-N in surface peat, excess N accumulated in Sphagnum tissue, and N2 fixation activity decreased. Elevated CO2 offset the effects of warming, disrupting the accumulation of N in peat and Sphagnum tissue. Methane concentrations in porewater increased with warming irrespective of CO2 treatment, resulting in a ~10× rise in methanotrophic activity within Sphagnum from the +9°C enclosures. Warming's divergent impacts on diazotrophy and methanotrophy caused these processes to become decoupled at warmer temperatures, as evidenced by declining rates of methane-induced N2 fixation and significant losses of keystone microbial taxa. In addition to changes in the Sphagnum microbiome, we observed ~94% mortality of Sphagnum between the +0°C and +9°C treatments, possibly due to the interactive effects of warming on N-availability and competition from vascular plant species. Collectively, these results highlight the vulnerability of the Sphagnum phytobiome to rising temperatures and atmospheric CO2 concentrations, with significant implications for carbon and nitrogen cycling in boreal peatlands.

KW - Sphagnum moss

KW - boreal peatland

KW - climate change

KW - diazotroph

KW - elevated CO

KW - methane

KW - methanotroph

KW - nitrogen

KW - plant microbiomes

KW - warming

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DO - 10.1111/gcb.16651

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