Host Species–Microbiome Interactions Contribute to Sphagnum Moss Growth Acclimation to Warming

Tatjana Živković; Alyssa A. Carrell; Gustaf Granath; A. Jonathan Shaw; Dale A. Pelletier; Christopher W. Schadt; Dawn M. Klingeman; Mats B. Nilsson; Manuel Helbig; Denis Warshan; Ingeborg J. Klarenberg; Daniel Gilbert; Joel E. Kostka; David J. Weston

doi:10.1111/gcb.70066

Host Species–Microbiome Interactions Contribute to Sphagnum Moss Growth Acclimation to Warming

Tatjana Živković, Alyssa A. Carrell, Gustaf Granath, A. Jonathan Shaw, Dale A. Pelletier, Christopher W. Schadt, Dawn M. Klingeman, Mats B. Nilsson, Manuel Helbig, Denis Warshan, Ingeborg J. Klarenberg, Daniel Gilbert, Joel E. Kostka, David J. Weston

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

1 Scopus citations

Abstract

Sphagnum moss is the dominant plant genus in northern peatlands responsible for long-term carbon accumulation. Sphagnum hosts diverse microbial communities (microbiomes), and its phytobiome (plant host + constituent microbiome + environment) plays a key role in nutrient acquisition along with carbon cycling. Climate change can modify the Sphagnum-associated microbiome, resulting in enhanced host growth and thermal acclimation as previously shown in warming experiments. However, the extent of microbiome benefits to the host and the influence of host–microbe specificity on Sphagnum thermal acclimation remain unclear. Here, we extracted Sphagnum microbiomes from five donor species of four peatland warming experiments across a latitudinal gradient and applied those microbiomes to three germ-free Sphagnum species grown across a range of temperatures in the laboratory. Using this experimental system, we test if Sphagnum's growth response to warming depends on the donor and/or recipient host species, and we determine how the microbiome's growth conditions in the field affect Sphagnum host growth across a range of temperatures in the laboratory. After 4 weeks, we found that the highest growth rate of recipient Sphagnum was observed in treatments of matched host–microbiome pairs, with rates approximately 50% and 250% higher in comparison to maximum growth rates of non-matched host–microbiome pairs and germ-free Sphagnum, respectively. We also found that the maximum growth rate of host–microbiome pairs was reached when treatment temperatures were close to the microbiome's native temperatures. Our study shows that Sphagnum's growth acclimation to temperature is partially controlled by its constituent microbiome. Strong Sphagnum host–microbiome species specificity indicates the existence of underlying, unknown physiological mechanisms that may drive Sphagnum's ability to acclimatize to elevated temperatures. Together with rapid acclimation of the microbiome to warming, these specific microbiome–plant associations have the potential to enhance peatland resilience in the face of climate change.

Original language	English
Article number	e70066
Journal	Global Change Biology
Volume	31
Issue number	2
DOIs	https://doi.org/10.1111/gcb.70066
State	Published - Feb 2025

Funding

This research was supported by: (1) US Department of Energy's Office of Science, Biological, and Environmental Research (DOE BER) Early Career Research Program ERKP909, SPRUCE project within the Environmental System Science Program DE‐SC0007144 and DE‐SC0012088, and the Genomic Science Program DE‐SC0023297. Oak Ridge National Laboratory is managed by UT‐Battelle LLC, for the US Department of Energy under contract DE‐AC05‐00OR22725; (2) Swedish research council (VR) grant 2018‐04872 and Carl Tryggers Stiftelse to G.G. Funding: Funding: This research was supported by: (1) US Department of Energy's Office of Science, Biological, and Environmental Research (DOE BER) Early Career Research Program ERKP909, SPRUCE project within the Environmental System Science Program DE-SC0007144 and DE-SC0012088, and the Genomic Science Program DE-SC0023297. Oak Ridge National Laboratory is managed by UT-Battelle LLC, for the US Department of Energy under contract DE-AC05-00OR22725; (2) Swedish research council (VR) grant 2018-04872 and Carl Tryggers Stiftelse to G.G. We thank the anonymous reviewers for their insightful comments and constructive feedback, which greatly improved the quality of this manuscript. This research was supported by: (1) U.S. Department of Energy's Office of Science, Biological, and Environmental Research (DOE BER) Early Career Research Program ERKP909, SPRUCE project within the Environmental System Science Program DE-SC0007144 and DE-SC0012088, and the Genomic Science Program DE-SC0023297. Oak Ridge National Laboratory is managed by UT-Battelle LLC, for the U.S. Department of Energy under contract DE-AC05-00OR22725; (2) Swedish research council (VR) grant no. 2018-04872 and Carl Tryggers Stiftelse to G.G. This manuscript has been authored by UT‐Battelle LLC under Contract No. DE‐AC05‐00OR22725 with the U.S. Department of Energy. The United States Government retains and the publisher, by accepting the article for publication, acknowledges that the United States Government retains a non‐exclusive, paid‐up, irrevocable, world‐wide license to publish or reproduce the published form of this manuscript, or allow others to do so, for United States Government purposes. The Department of Energy will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan ( http://energy.gov/downloads/doe‐public‐access‐plan ). We thank the anonymous reviewers for their insightful comments and constructive feedback, which greatly improved the quality of this manuscript. This research was supported by: (1) U.S. Department of Energy's Office of Science, Biological, and Environmental Research (DOE BER) Early Career Research Program ERKP909, SPRUCE project within the Environmental System Science Program DE‐SC0007144 and DE‐SC0012088, and the Genomic Science Program DE‐SC0023297. Oak Ridge National Laboratory is managed by UT‐Battelle LLC, for the U.S. Department of Energy under contract DE‐AC05‐00OR22725; (2) Swedish research council (VR) grant no. 2018‐04872 and Carl Tryggers Stiftelse to G.G.

Keywords

Sphagnum
acclimation
climate change
microbiome
peatland
plant–microbe interaction
resilience
thermotolerance

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10.1111/gcb.70066

Cite this

Živković, T., Carrell, A. A., Granath, G., Shaw, A. J., Pelletier, D. A., Schadt, C. W., Klingeman, D. M., Nilsson, M. B., Helbig, M., Warshan, D., Klarenberg, I. J., Gilbert, D., Kostka, J. E., & Weston, D. J. (2025). Host Species–Microbiome Interactions Contribute to Sphagnum Moss Growth Acclimation to Warming. Global Change Biology, 31(2), Article e70066. https://doi.org/10.1111/gcb.70066

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title = "Host Species–Microbiome Interactions Contribute to Sphagnum Moss Growth Acclimation to Warming",

abstract = "Sphagnum moss is the dominant plant genus in northern peatlands responsible for long-term carbon accumulation. Sphagnum hosts diverse microbial communities (microbiomes), and its phytobiome (plant host + constituent microbiome + environment) plays a key role in nutrient acquisition along with carbon cycling. Climate change can modify the Sphagnum-associated microbiome, resulting in enhanced host growth and thermal acclimation as previously shown in warming experiments. However, the extent of microbiome benefits to the host and the influence of host–microbe specificity on Sphagnum thermal acclimation remain unclear. Here, we extracted Sphagnum microbiomes from five donor species of four peatland warming experiments across a latitudinal gradient and applied those microbiomes to three germ-free Sphagnum species grown across a range of temperatures in the laboratory. Using this experimental system, we test if Sphagnum's growth response to warming depends on the donor and/or recipient host species, and we determine how the microbiome's growth conditions in the field affect Sphagnum host growth across a range of temperatures in the laboratory. After 4 weeks, we found that the highest growth rate of recipient Sphagnum was observed in treatments of matched host–microbiome pairs, with rates approximately 50\% and 250\% higher in comparison to maximum growth rates of non-matched host–microbiome pairs and germ-free Sphagnum, respectively. We also found that the maximum growth rate of host–microbiome pairs was reached when treatment temperatures were close to the microbiome's native temperatures. Our study shows that Sphagnum's growth acclimation to temperature is partially controlled by its constituent microbiome. Strong Sphagnum host–microbiome species specificity indicates the existence of underlying, unknown physiological mechanisms that may drive Sphagnum's ability to acclimatize to elevated temperatures. Together with rapid acclimation of the microbiome to warming, these specific microbiome–plant associations have the potential to enhance peatland resilience in the face of climate change.",

keywords = "Sphagnum, acclimation, climate change, microbiome, peatland, plant–microbe interaction, resilience, thermotolerance",

author = "Tatjana {\v Z}ivkovi{\'c} and Carrell, \{Alyssa A.\} and Gustaf Granath and Shaw, \{A. Jonathan\} and Pelletier, \{Dale A.\} and Schadt, \{Christopher W.\} and Klingeman, \{Dawn M.\} and Nilsson, \{Mats B.\} and Manuel Helbig and Denis Warshan and Klarenberg, \{Ingeborg J.\} and Daniel Gilbert and Kostka, \{Joel E.\} and Weston, \{David J.\}",

note = "Publisher Copyright: {\textcopyright} 2025 Oak Ridge National Laboratory and The Author(s). Global Change Biology published by John Wiley \& Sons Ltd.",

year = "2025",

month = feb,

doi = "10.1111/gcb.70066",

language = "English",

volume = "31",

journal = "Global Change Biology",

issn = "1354-1013",

publisher = "wiley",

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TY - JOUR

T1 - Host Species–Microbiome Interactions Contribute to Sphagnum Moss Growth Acclimation to Warming

AU - Živković, Tatjana

AU - Carrell, Alyssa A.

AU - Granath, Gustaf

AU - Shaw, A. Jonathan

AU - Pelletier, Dale A.

AU - Schadt, Christopher W.

AU - Klingeman, Dawn M.

AU - Nilsson, Mats B.

AU - Helbig, Manuel

AU - Warshan, Denis

AU - Klarenberg, Ingeborg J.

AU - Gilbert, Daniel

AU - Kostka, Joel E.

AU - Weston, David J.

PY - 2025/2

Y1 - 2025/2

N2 - Sphagnum moss is the dominant plant genus in northern peatlands responsible for long-term carbon accumulation. Sphagnum hosts diverse microbial communities (microbiomes), and its phytobiome (plant host + constituent microbiome + environment) plays a key role in nutrient acquisition along with carbon cycling. Climate change can modify the Sphagnum-associated microbiome, resulting in enhanced host growth and thermal acclimation as previously shown in warming experiments. However, the extent of microbiome benefits to the host and the influence of host–microbe specificity on Sphagnum thermal acclimation remain unclear. Here, we extracted Sphagnum microbiomes from five donor species of four peatland warming experiments across a latitudinal gradient and applied those microbiomes to three germ-free Sphagnum species grown across a range of temperatures in the laboratory. Using this experimental system, we test if Sphagnum's growth response to warming depends on the donor and/or recipient host species, and we determine how the microbiome's growth conditions in the field affect Sphagnum host growth across a range of temperatures in the laboratory. After 4 weeks, we found that the highest growth rate of recipient Sphagnum was observed in treatments of matched host–microbiome pairs, with rates approximately 50% and 250% higher in comparison to maximum growth rates of non-matched host–microbiome pairs and germ-free Sphagnum, respectively. We also found that the maximum growth rate of host–microbiome pairs was reached when treatment temperatures were close to the microbiome's native temperatures. Our study shows that Sphagnum's growth acclimation to temperature is partially controlled by its constituent microbiome. Strong Sphagnum host–microbiome species specificity indicates the existence of underlying, unknown physiological mechanisms that may drive Sphagnum's ability to acclimatize to elevated temperatures. Together with rapid acclimation of the microbiome to warming, these specific microbiome–plant associations have the potential to enhance peatland resilience in the face of climate change.

AB - Sphagnum moss is the dominant plant genus in northern peatlands responsible for long-term carbon accumulation. Sphagnum hosts diverse microbial communities (microbiomes), and its phytobiome (plant host + constituent microbiome + environment) plays a key role in nutrient acquisition along with carbon cycling. Climate change can modify the Sphagnum-associated microbiome, resulting in enhanced host growth and thermal acclimation as previously shown in warming experiments. However, the extent of microbiome benefits to the host and the influence of host–microbe specificity on Sphagnum thermal acclimation remain unclear. Here, we extracted Sphagnum microbiomes from five donor species of four peatland warming experiments across a latitudinal gradient and applied those microbiomes to three germ-free Sphagnum species grown across a range of temperatures in the laboratory. Using this experimental system, we test if Sphagnum's growth response to warming depends on the donor and/or recipient host species, and we determine how the microbiome's growth conditions in the field affect Sphagnum host growth across a range of temperatures in the laboratory. After 4 weeks, we found that the highest growth rate of recipient Sphagnum was observed in treatments of matched host–microbiome pairs, with rates approximately 50% and 250% higher in comparison to maximum growth rates of non-matched host–microbiome pairs and germ-free Sphagnum, respectively. We also found that the maximum growth rate of host–microbiome pairs was reached when treatment temperatures were close to the microbiome's native temperatures. Our study shows that Sphagnum's growth acclimation to temperature is partially controlled by its constituent microbiome. Strong Sphagnum host–microbiome species specificity indicates the existence of underlying, unknown physiological mechanisms that may drive Sphagnum's ability to acclimatize to elevated temperatures. Together with rapid acclimation of the microbiome to warming, these specific microbiome–plant associations have the potential to enhance peatland resilience in the face of climate change.

KW - Sphagnum

KW - acclimation

KW - climate change

KW - microbiome

KW - peatland

KW - plant–microbe interaction

KW - resilience

KW - thermotolerance

UR - https://www.scopus.com/pages/publications/85218917298

U2 - 10.1111/gcb.70066

DO - 10.1111/gcb.70066

M3 - Article

C2 - 39968863

AN - SCOPUS:85218917298

SN - 1354-1013

VL - 31

JO - Global Change Biology

JF - Global Change Biology

IS - 2

M1 - e70066

ER -

Host Species–Microbiome Interactions Contribute to Sphagnum Moss Growth Acclimation to Warming

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