Microbial sensitivity to temperature and sulfate deposition modulates greenhouse gas emissions from peat soils
Abstract
Abstract Peatlands are among the largest natural sources of atmospheric methane (CH 4 ) worldwide. Microbial processes play a key role in regulating CH 4 emissions from peatland ecosystems, yet the complex interplay between soil substrates and microbial communities in controlling CH 4 emissions as a function of global change remains unclear. Herein, we performed an integrated analysis of multi‐omics data sets to provide a comprehensive understanding of the molecular processes driving changes in greenhouse gas (GHG) emissions in peatland ecosystems with increasing temperature and sulfate deposition in a laboratory incubation study. We sought to first investigate how increasing temperatures (4, 21, and 35°C) impact soil microbiome–metabolome interactions; then explore the competition between methanogens and sulfate‐reducing bacteria (SRBs) with increasing sulfate concentrations at the optimum temperature for methanogenesis. Our results revealed that peat soil organic matter degradation, mediated by biotic and potentially abiotic processes, is the main driver of the increase in CO 2 production with temperature. In contrast, the decrease in CH 4 production at 35°C was linked to the absence of syntrophic communities and the potential inhibitory effect of phenols on methanogens. Elevated temperatures further induced the microbial communities to develop high growth yield and stress tolerator trait‐basedmore »
- Authors:
-
- Department of Environmental Science The University of Arizona Tucson Arizona USA
- Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory Richland Washington USA
- Department of Chemistry and Biochemistry Lebanese University Beirut Lebanon
- Department of Earth, Ocean and Atmospheric Science Florida State University Tallahassee Florida USA
- Department of Environmental Science The University of Arizona Tucson Arizona USA, Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory Richland Washington USA
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1923556
- Grant/Contract Number:
- DE‐SC0021349
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Global Change Biology
- Additional Journal Information:
- Journal Name: Global Change Biology Journal Volume: 29 Journal Issue: 7; Journal ID: ISSN 1354-1013
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
AminiTabrizi, Roya, Graf‐Grachet, Nathalia, Chu, Rosalie K., Toyoda, Jason G., Hoyt, David W., Hamdan, Rasha, Wilson, Rachel M., and Tfaily, Malak M. Microbial sensitivity to temperature and sulfate deposition modulates greenhouse gas emissions from peat soils. United Kingdom: N. p., 2023.
Web. doi:10.1111/gcb.16614.
AminiTabrizi, Roya, Graf‐Grachet, Nathalia, Chu, Rosalie K., Toyoda, Jason G., Hoyt, David W., Hamdan, Rasha, Wilson, Rachel M., & Tfaily, Malak M. Microbial sensitivity to temperature and sulfate deposition modulates greenhouse gas emissions from peat soils. United Kingdom. https://doi.org/10.1111/gcb.16614
AminiTabrizi, Roya, Graf‐Grachet, Nathalia, Chu, Rosalie K., Toyoda, Jason G., Hoyt, David W., Hamdan, Rasha, Wilson, Rachel M., and Tfaily, Malak M. Sun .
"Microbial sensitivity to temperature and sulfate deposition modulates greenhouse gas emissions from peat soils". United Kingdom. https://doi.org/10.1111/gcb.16614.
@article{osti_1923556,
title = {Microbial sensitivity to temperature and sulfate deposition modulates greenhouse gas emissions from peat soils},
author = {AminiTabrizi, Roya and Graf‐Grachet, Nathalia and Chu, Rosalie K. and Toyoda, Jason G. and Hoyt, David W. and Hamdan, Rasha and Wilson, Rachel M. and Tfaily, Malak M.},
abstractNote = {Abstract Peatlands are among the largest natural sources of atmospheric methane (CH 4 ) worldwide. Microbial processes play a key role in regulating CH 4 emissions from peatland ecosystems, yet the complex interplay between soil substrates and microbial communities in controlling CH 4 emissions as a function of global change remains unclear. Herein, we performed an integrated analysis of multi‐omics data sets to provide a comprehensive understanding of the molecular processes driving changes in greenhouse gas (GHG) emissions in peatland ecosystems with increasing temperature and sulfate deposition in a laboratory incubation study. We sought to first investigate how increasing temperatures (4, 21, and 35°C) impact soil microbiome–metabolome interactions; then explore the competition between methanogens and sulfate‐reducing bacteria (SRBs) with increasing sulfate concentrations at the optimum temperature for methanogenesis. Our results revealed that peat soil organic matter degradation, mediated by biotic and potentially abiotic processes, is the main driver of the increase in CO 2 production with temperature. In contrast, the decrease in CH 4 production at 35°C was linked to the absence of syntrophic communities and the potential inhibitory effect of phenols on methanogens. Elevated temperatures further induced the microbial communities to develop high growth yield and stress tolerator trait‐based strategies leading to a shift in their composition and function. On the other hand, SRBs were able to outcompete methanogens in the presence of non‐limiting sulfate concentrations at 21°C, thereby reducing CH 4 emissions. At higher sulfate concentrations, however, the prevalence of communities capable of producing sufficient low‐molecular‐weight carbon substrates for the coexistence of SRBs and methanogens was translated into elevated CH 4 emissions. The use of omics in this study enhanced our understanding of the structure and interactions among microbes with the abiotic components of the system that can be useful for mitigating GHG emissions from peatland ecosystems in the face of global change.},
doi = {10.1111/gcb.16614},
journal = {Global Change Biology},
number = 7,
volume = 29,
place = {United Kingdom},
year = {Sun Feb 05 00:00:00 EST 2023},
month = {Sun Feb 05 00:00:00 EST 2023}
}
https://doi.org/10.1111/gcb.16614
Works referenced in this record:
Atmospheric sulfur deposition alters pathways of gaseous carbon production in peatlands: S DEPOSITION ALTERS GASEOUS C PRODUCTION IN PEATLANDS
journal, May 2003
- Vile, Melanie A.; Bridgham, Scott D.; Wieder, R. Kelman
- Global Biogeochemical Cycles, Vol. 17, Issue 2
DRAM for distilling microbial metabolism to automate the curation of microbiome function
journal, August 2020
- Shaffer, Michael; Borton, Mikayla A.; McGivern, Bridget B.
- Nucleic Acids Research, Vol. 48, Issue 16
Anaerobic oxidation of methane: an “active” microbial process
journal, December 2014
- Cui, Mengmeng; Ma, Anzhou; Qi, Hongyan
- MicrobiologyOpen, Vol. 4, Issue 1
On r- and K-Selection
journal, November 1970
- Pianka, Eric R.
- The American Naturalist, Vol. 104, Issue 940
Peat-Inhabiting Verrucomicrobia of the Order Methylacidiphilales Do Not Possess Methanotrophic Capabilities
journal, December 2021
- Dedysh, Svetlana N.; Beletsky, Alexey V.; Ivanova, Anastasia A.
- Microorganisms, Vol. 9, Issue 12
Stability of peatland carbon to rising temperatures
journal, December 2016
- Wilson, R. M.; Hopple, A. M.; Tfaily, M. M.
- Nature Communications, Vol. 7, Article No. 13723
Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014
- Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern
- Bioinformatics, Vol. 30, Issue 15
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph
journal, January 2015
- Li, Dinghua; Liu, Chi-Man; Luo, Ruibang
- Bioinformatics, Vol. 31, Issue 10
Sequential Abiotic‐Biotic Processes Drive Organic Carbon Transformation in Peat Bogs
journal, February 2021
- Fudyma, Jane D.; Toyoda, Jason G.; Chu, Rosalie K.
- Journal of Geophysical Research: Biogeosciences, Vol. 126, Issue 2
Geochemical controls on anaerobic organic matter decomposition in a northern peatland
journal, July 2008
- Beer, Julia; Lee, Kern; Whiticar, Michael
- Limnology and Oceanography, Vol. 53, Issue 4
Complexation and reduction of iron by phenolic substances: Implications for transport of dissolved Fe from peatlands to aquatic ecosystems and global iron cycling
journal, October 2018
- Wan, Xiang; Xiang, Wu; Wan, Neng
- Chemical Geology, Vol. 498
Regulation of Organic Matter Decomposition and Nutrient Release in a Wetland Soil
journal, September 1998
- McLatchey, G. P.; Reddy, K. R.
- Journal of Environmental Quality, Vol. 27, Issue 5
Clostridium thailandense sp. nov., a novel CO2-reducing acetogenic bacterium isolated from peatland soil
journal, February 2022
- Chaikitkaew, Srisuda; In-chan, Supattra; Singkhala, Apinya
- International Journal of Systematic and Evolutionary Microbiology, Vol. 72, Issue 2
Microcharacteristic analysis of CH4 emissions under different conditions during coal spontaneous combustion with high-temperature oxidation and in situ FTIR
journal, October 2020
- Zhao, Jingyu; Wang, Tao; Deng, Jun
- Energy, Vol. 209
Methanogenic archaea and sulfate reducing bacteria co-cultured on acetate: teamwork or coexistence?
journal, May 2015
- Ozuolmez, Derya; Na, Hyunsoo; Lever, Mark A.
- Frontiers in Microbiology, Vol. 6
Comparative Genomics of Candidate Phylum TM6 Suggests That Parasitism Is Widespread and Ancestral in This Lineage
journal, November 2015
- Yeoh, Yun Kit; Sekiguchi, Yuji; Parks, Donovan H.
- Molecular Biology and Evolution, Vol. 33, Issue 4
Support for an anaerobic sulfur cycle in two Canadian peatland soils
journal, January 2007
- Blodau, Christian; Mayer, Bernhard; Peiffer, Stefan
- Journal of Geophysical Research, Vol. 112, Issue G2
Controls on Soil Organic Matter Degradation and Subsequent Greenhouse Gas Emissions Across a Permafrost Thaw Gradient in Northern Sweden
journal, September 2020
- AminiTabrizi, Roya; Wilson, Rachel M.; Fudyma, Jane D.
- Frontiers in Earth Science, Vol. 8
Long-term effects of atmospheric deposition on British plant species richness
journal, July 2021
- Tipping, Edward; Davies, Jessica A. C.; Henrys, Peter A.
- Environmental Pollution, Vol. 281
Does dissolved organic matter or solid peat fuel anaerobic respiration in peatlands?
journal, September 2019
- Hopple, Anya M.; Pfeifer-Meister, Laurel; Zalman, Cassandra A.
- Geoderma, Vol. 349
Humic-rich peat extracts inhibit sulfate reduction, methanogenesis, and anaerobic respiration but not acetogenesis in peat soils of a temperate bog
journal, December 2010
- Minderlein, Stefanie; Blodau, Christian
- Soil Biology and Biochemistry, Vol. 42, Issue 12
Microbial carbon use and associated changes in microbial community structure in high-Arctic tundra soils under elevated temperature
journal, November 2021
- Frossard, Aline; De Maeyer, Lotte; Adamczyk, Magdalene
- Soil Biology and Biochemistry, Vol. 162
Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change
journal, September 2019
- Malik, Ashish A.; Martiny, Jennifer B. H.; Brodie, Eoin L.
- The ISME Journal, Vol. 14, Issue 1
Rapid Net Carbon Loss From a Whole‐Ecosystem Warmed Peatland
journal, July 2020
- Hanson, Paul J.; Griffiths, Natalie A.; Iversen, Colleen M.
- AGU Advances, Vol. 1, Issue 3
Unraveling the Importance of Polyphenols for Microbial Carbon Mineralization in Rewetted Riparian Peatlands
journal, October 2019
- Zak, Dominik; Roth, Cyril; Unger, Viktoria
- Frontiers in Environmental Science, Vol. 7
Methane fluxes show consistent temperature dependence across microbial to ecosystem scales
journal, March 2014
- Yvon-Durocher, Gabriel; Allen, Andrew P.; Bastviken, David
- Nature, Vol. 507, Issue 7493
Microbial diversity drives multifunctionality in terrestrial ecosystems
journal, January 2016
- Delgado-Baquerizo, Manuel; Maestre, Fernando T.; Reich, Peter B.
- Nature Communications, Vol. 7, Issue 1
Hydrogenation of organic matter as a terminal electron sink sustains high CO2:CH4 production ratios during anaerobic decomposition
journal, October 2017
- Wilson, Rachel M.; Tfaily, Malak M.; Rich, Virginia I.
- Organic Geochemistry, Vol. 112
Potential shift from a carbon sink to a source in Amazonian peatlands under a changing climate
journal, November 2018
- Wang, Sirui; Zhuang, Qianlai; Lähteenoja, Outi
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 49
Fundamentals of methanogenic pathways that are key to the biomethanation of complex biomass
journal, June 2011
- Ferry, James G.
- Current Opinion in Biotechnology, Vol. 22, Issue 3
Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming
journal, April 2015
- Tveit, Alexander Tøsdal; Urich, Tim; Frenzel, Peter
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 19
Integration of sulfate assimilation with carbon and nitrogen metabolism in transition from C3 to C4 photosynthesis
journal, May 2019
- Jobe, Timothy O.; Zenzen, Ivan; Rahimzadeh Karvansara, Parisa
- Journal of Experimental Botany, Vol. 70, Issue 16
Assessing the Effect of Humic Substances and Fe(III) as Potential Electron Acceptors for Anaerobic Methane Oxidation in a Marine Anoxic System
journal, August 2020
- van Grinsven, Sigrid; Sinninghe Damsté, Jaap S.; Villanueva, Laura
- Microorganisms, Vol. 8, Issue 9
Response of Methanogens in Arctic Sediments to Temperature and Methanogenic Substrate Availability
journal, June 2015
- Blake, Lynsay I.; Tveit, Alexander; Øvreås, Lise
- PLOS ONE, Vol. 10, Issue 6
Effect of one step temperature increment from mesophilic to thermophilic anaerobic digestion on the linked pattern between bacterial and methanogenic communities
journal, November 2019
- Lv, Zuopeng; Wu, Xiayuan; Zhou, Bingqian
- Bioresource Technology, Vol. 292
Formularity: Software for Automated Formula Assignment of Natural and Other Organic Matter from Ultrahigh-Resolution Mass Spectra
journal, November 2017
- Tolić, Nikola; Liu, Yina; Liyu, Andrey
- Analytical Chemistry, Vol. 89, Issue 23
Soil protists: a fertile frontier in soil biology research
journal, February 2018
- Geisen, Stefan; Mitchell, Edward A. D.; Adl, Sina
- FEMS Microbiology Reviews, Vol. 42, Issue 3
Molecular hijacking of siroheme for the synthesis of heme and d1 heme
journal, October 2011
- Bali, S.; Lawrence, A. D.; Lobo, S. A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 45
Linking soil organic carbon mineralization with soil microbial and substrate properties under warming in permafrost peatlands of Northeastern China
journal, August 2021
- Song, Yanyu; Liu, Chao; Song, Changchun
- CATENA, Vol. 203
Biofilm and motility in response to environmental and host-related signals in Gram negative opportunistic pathogens
journal, October 2018
- Rossi, E.; Paroni, M.; Landini, P.
- Journal of Applied Microbiology, Vol. 125, Issue 6
Sulfur pollution suppression of the wetland methane source in the 20th and 21st centuries
journal, August 2004
- Gauci, V.; Matthews, E.; Dise, N.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 34
Sulfide as a soil phytotoxin—a review
journal, January 2013
- Lamers, Leon P. M.; Govers, Laura L.; Janssen, Inge C. J. M.
- Frontiers in Plant Science, Vol. 4
Carbon Fluxes and Microbial Activities From Boreal Peatlands Experiencing Permafrost Thaw
journal, March 2021
- Waldrop, M. P.; McFarland, J.; Manies, K. L.
- Journal of Geophysical Research: Biogeosciences, Vol. 126, Issue 3
Effect of water table decline on the abundances of soil mites, springtails, and nematodes in the Zoige peatland of eastern Tibetan Plateau
journal, August 2018
- Wei, Xue; Cao, Rui; Wu, Xinwei
- Applied Soil Ecology, Vol. 129
Untargeted metabolomic profiling of Sphagnum fallax reveals novel antimicrobial metabolites
journal, November 2019
- Fudyma, Jane D.; Lyon, Jamee; AminiTabrizi, Roya
- Plant Direct, Vol. 3, Issue 11
Decoupling function and taxonomy in the global ocean microbiome
journal, September 2016
- Louca, S.; Parfrey, L. W.; Doebeli, M.
- Science, Vol. 353, Issue 6305
Environmental and stoichiometric controls on microbial carbon‐use efficiency in soils
journal, July 2012
- Manzoni, Stefano; Taylor, Philip; Richter, Andreas
- New Phytologist, Vol. 196, Issue 1
KBase: The United States Department of Energy Systems Biology Knowledgebase
journal, July 2018
- Arkin, Adam P.; Cottingham, Robert W.; Henry, Christopher S.
- Nature Biotechnology, Vol. 36, Issue 7
Cytotoxicity, antimicrobial and antioxidant activities of mosses obtained from open habitats
journal, September 2021
- Wolski, Grzegorz J.; Sadowska, Beata; Fol, Marek
- PLOS ONE, Vol. 16, Issue 9
Compositional stability of peat in ecosystem-scale warming mesocosms
journal, March 2022
- Baysinger, Mackenzie R.; Wilson, Rachel M.; Hanson, Paul J.
- PLOS ONE, Vol. 17, Issue 3
Organic matter transformation in the peat column at Marcell Experimental Forest: Humification and vertical stratification: Organic matter dynamics
journal, April 2014
- Tfaily, Malak M.; Cooper, William T.; Kostka, Joel E.
- Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 4
Elevated temperatures drive abiotic and biotic degradation of organic matter in a peat bog under oxic conditions
journal, January 2022
- AminiTabrizi, Roya; Dontsova, Katerina; Graf Grachet, Nathalia
- Science of The Total Environment, Vol. 804
Anaerobic Methane Oxidation in High-Arctic Alaskan Peatlands as a Significant Control on Net CH4 Fluxes
journal, January 2019
- Miller, Kimberley; Lai, Chun-Ta; Dahlgren, Randy
- Soil Systems, Vol. 3, Issue 1
Impact of Warming on Greenhouse Gas Production and Microbial Diversity in Anoxic Peat From a Sphagnum-Dominated Bog (Grand Rapids, Minnesota, United States)
journal, April 2019
- Kolton, Max; Marks, Ansley; Wilson, Rachel M.
- Frontiers in Microbiology, Vol. 10
The contribution of Fe(III) and humic acid reduction to ecosystem respiration in drained thaw lake basins of the Arctic Coastal Plain: Fe(III) AND HA REDUCTION IN THE ARCTIC
journal, May 2013
- Lipson, David A.; Raab, Theodore K.; Goria, Dominic
- Global Biogeochemical Cycles, Vol. 27, Issue 2
Consortia of low-abundance bacteria drive sulfate reduction-dependent degradation of fermentation products in peat soil microcosms
journal, March 2016
- Hausmann, Bela; Knorr, Klaus-Holger; Schreck, Katharina
- The ISME Journal, Vol. 10, Issue 10
Soil metabolome response to whole-ecosystem warming at the Spruce and Peatland Responses under Changing Environments experiment
journal, June 2021
- Wilson, Rachel M.; Tfaily, Malak M.; Kolton, Max
- Proceedings of the National Academy of Sciences, Vol. 118, Issue 25
Effect of Temperature Pre-Exposure on the Locomotion and Chemotaxis of C. elegans
journal, October 2014
- Parida, Lipika; Neogi, Sudarsan; Padmanabhan, Venkat
- PLoS ONE, Vol. 9, Issue 10
RASTtk: A modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes
journal, February 2015
- Brettin, Thomas; Davis, James J.; Disz, Terry
- Scientific Reports, Vol. 5, Issue 1
Methanogenic archaea: ecologically relevant differences in energy conservation
journal, June 2008
- Thauer, Rudolf K.; Kaster, Anne-Kristin; Seedorf, Henning
- Nature Reviews Microbiology, Vol. 6, Issue 8
Homoacetogenesis competes with hydrogenotrophic methanogenesis for substrates in a peatland experiencing ecosystem warming
journal, September 2022
- LeeWays, Cory; McCullough, Laura L.; Hopple, Anya M.
- Soil Biology and Biochemistry, Vol. 172
Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales
journal, February 2013
- Bridgham, Scott D.; Cadillo-Quiroz, Hinsby; Keller, Jason K.
- Global Change Biology, Vol. 19, Issue 5
Thermodynamic Control of the Carbon Budget of a Peatland
journal, June 2018
- Worrall, Fred; Moody, Catherine S.; Clay, Gareth D.
- Journal of Geophysical Research: Biogeosciences, Vol. 123, Issue 6
Anaerobic respiration pathways and response to increased substrate availability of Arctic wetland soils
journal, January 2020
- Philben, Michael; Zhang, Lijie; Yang, Ziming
- Environmental Science: Processes & Impacts, Vol. 22, Issue 10
Transformations from specialists to generalists cause bacterial communities are more stable than micro-eukaryotic communities under anthropogenic activity disturbance
journal, October 2021
- Liu, Lemian; Wang, Shanshan; Chen, Jianfeng
- Science of The Total Environment, Vol. 790
Effects of decadal deposition of nitrogen and sulfur, and increased temperature, on methane emissions from a boreal peatland
journal, December 2010
- Eriksson, Tobias; Öquist, Mats G.; Nilsson, Mats B.
- Journal of Geophysical Research, Vol. 115, Issue G4
Plant organic matter inputs exert a strong control on soil organic matter decomposition in a thawing permafrost peatland
journal, May 2022
- Wilson, Rachel M.; Hough, Moira A.; Verbeke, Brittany A.
- Science of The Total Environment, Vol. 820
Microbial communities in natural and disturbed peatlands: A review
journal, February 2013
- Andersen, R.; Chapman, S. J.; Artz, R. R. E.
- Soil Biology and Biochemistry, Vol. 57
Sulfate-reducing microorganisms in wetlands – fameless actors in carbon cycling and climate change
journal, January 2012
- Pester, Michael
- Frontiers in Microbiology, Vol. 3