Soil metabolome response to whole-ecosystem warming at the spruce and peatland responses under changing environments experiment

Rachel M. Wilson, Malak M. Tfaily, Max Kolton, Eric R. Johnston, Caitlin Petro, Cassandra A. Zalman, Paul J. Hanson, Heino M. Heyman, Jennifer E. Kyle, David W. Hoyt, Elizabeth K. Eder, Samuel O. Purvine, Randall K. Kolka, Stephen D. Sebestyen, Natalie A. Griffiths, Christopher W. Schadt, Jason K. Keller, Scott D. Bridgham, Jeffrey P. Chanton, Joel E. Kostka

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Abstract

In this study, a suite of complementary environmental geochemical analyses, including NMR and gas chromatography-mass spectrometry (GC-MS) analyses of central metabolites, Fourier transform ion cyclotron resonance mass spectrometry (FTICR-MS) of secondary metabolites, and lipidomics, was used to investigate the influence of organic matter (OM) quality on the heterotrophic microbial mechanisms controlling peatland CO2, CH4, and CO2:CH4 porewater production ratios in response to climate warming. Our investigations leverage the Spruce and Peatland Responses under Changing Environments (SPRUCE) experiment, where air and peat warming were combined in a whole-ecosystem warming treatment. We hypothesized that warming would enhance the production of plant-derived metabolites, resulting in increased labile OM inputs to the surface peat, thereby enhancing microbial activity and greenhouse gas production. Because shallow peat is most susceptible to enhanced warming, increases in labile OM inputs to the surface, in particular, are likely to result in significant changes to CO2 and CH4 dynamics and methanogenic pathways. In support of this hypothesis, significant correlations were observed between metabolites and temperature consistent with increased availability of labile substrates, which may stimulate more rapid turnover of microbial proteins. An increase in the abundance of methanogenic genes in response to the increase in the abundance of labile substrates was accompanied by a shift toward acetoclastic and methylotrophic methanogenesis. Our results suggest that as peatland vegetation trends toward increasing vascular plant cover with warming, we can expect a concomitant shift toward increasingly methanogenic conditions and amplified climate–peatland feedbacks.

Original languageEnglish
Article numbere2004192118
JournalProceedings of the National Academy of Sciences of the United States of America
Volume118
Issue number25
DOIs
StatePublished - Jun 22 2021

Funding

ACKNOWLEDGMENTS. This study was funded by the Office of Biological and Environmental Research, Terrestrial Ecosystem Science Program, under US Department of Energy (DOE) Contracts DE-SC0007144 and DE-SC0012088. The Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the US DOE under Contract DE-AC05-00OR22725. A portion of this research was performed using Environmental Molecular Sciences Laboratory (EMSL) (grid.436923.9) (proposal: Wilson ID 49279), a DOE Office of Science User Facility sponsored by the Office of Biological and Environmental Research and located at the PNNL. The PNNL is a multiprogram national laboratory operated by Battelle for the DOE under Contract DE-AC05-76RLO 1830. The participation of R.K.K. and S.D.S. was funded by the Northern Research Station of the USDA Forest Service. Measurement of dissolved organic carbon concentration at the Forestry Sciences Laboratory, Grand Rapids, MN, was also funded by the USDA Forest Service. Metagenome sequence data were produced by the US Department of Energy Joint Genome Institute (https:// www.jgi.doe.gov/) in collaboration with the user community. This manuscript has been coauthored by UT-Battelle, LLC, under Contract DE-AC05-00OR22725 with the US DOE. The United States Government and the publisher, by accepting the article for publication, acknowledge that the United States Government retains a nonexclusive, paid-up, irrevocable, worldwide license to publish or reproduce the published form of this manuscript, or allow others to do so, for United States Government purposes. The DOE 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).

FundersFunder number
U.S. Department of EnergyDE-AC05-00OR22725, DE-SC0007144, 49279, DE-SC0012088
Office of Science
Biological and Environmental Research
Oak Ridge National Laboratory
U.S. Forest Service
Pacific Northwest National LaboratoryDE-AC05-76RLO 1830
UT-Battelle

    Keywords

    • Peatland | metabolome | climate change | metagenomics | elevated methane and carbon dioxide

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