Decreased growth of wild soil microbes after 15 years of transplant‐induced warming in a montane meadow

Purcell, Alicia M.; Hayer, Michaela; Koch, Benjamin J.; Mau, Rebecca L.; Blazewicz, Steven J.; Dijkstra, Paul; Mack, Michelle C.; Marks, Jane C.; Morrissey, Ember M.; Pett‐Ridge, Jennifer; Rubin, Rachel L.; Schwartz, Egbert; van Gestel, Natasja C.; Hungate, Bruce A.

doi:10.1111/gcb.15911

Title: Decreased growth of wild soil microbes after 15 years of transplant‐induced warming in a montane meadow

Journal Article · 15 October 2021 · Global Change Biology

DOI: https://doi.org/10.1111/gcb.15911 · OSTI ID:1826631

^[1]; Hayer, Michaela ^[1]; Koch, Benjamin J. ^[1]; Mau, Rebecca L. ^[1]; Blazewicz, Steven J. ^[2]; Dijkstra, Paul ^[1]; Mack, Michelle C. ^[1]; Marks, Jane C. ^[1];

^[3];

^[4];

^[5]; Schwartz, Egbert ^[1];

^[6]; Hungate, Bruce A. ^[1]

Department of Biological Sciences Center for Ecosystem Science and Society Northern Arizona University Flagstaff Arizona USA
Physical and Life Sciences Directorate Lawrence Livermore National Lab Livermore California USA
Division of Plant and Soil Sciences West Virginia University Morgantown West Virginia USA
Physical and Life Sciences Directorate Lawrence Livermore National Lab Livermore California USA, Life &, Environmental Sciences Department University of California Merced Merced CA USA
Department of Environmental Sciences Mount Holyoke College South Hadley Massachusetts USA
Department of Biological Sciences &, TTU Climate Center Texas Tech University Lubbock Texas USA

Abstract The carbon stored in soil exceeds that of plant biomass and atmospheric carbon and its stability can impact global climate. Growth of decomposer microorganisms mediates both the accrual and loss of soil carbon. Growth is sensitive to temperature and given the vast biological diversity of soil microorganisms, the response of decomposer growth rates to warming may be strongly idiosyncratic, varying among taxa, making ecosystem predictions difficult. Here, we show that 15 years of warming by transplanting plant–soil mesocosms down in elevation, strongly reduced the growth rates of soil microorganisms, measured in the field using undisturbed soil. The magnitude of the response to warming varied among microbial taxa. However, the direction of the response—reduced growth—was universal and warming explained twofold more variation than did the sum of taxonomic identity and its interaction with warming. For this ecosystem, most of the growth responses to warming could be explained without taxon‐specific information, suggesting that in some cases microbial responses measured in aggregate may be adequate for climate modeling. Long‐term experimental warming also reduced soil carbon content, likely a consequence of a warming‐induced increase in decomposition, as warming‐induced changes in plant productivity were negligible. The loss of soil carbon and decreased microbial biomass with warming may explain the reduced growth of the microbial community, more than the direct effects of temperature on growth. These findings show that direct and indirect effects of long‐term warming can reduce growth rates of soil microbes, which may have important feedbacks to global warming.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0016207; AC52-07NA27344

OSTI ID:: 1826631

Journal Information:: Global Change Biology, Journal Name: Global Change Biology Journal Issue: 1 Vol. 28; ISSN 1354-1013

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (61)

Toward more realistic projections of soil carbon dynamics by Earth system models: SOIL CARBON MODELING Luo, Yiqi; Ahlström, Anders; Allison, Steven D. Global Biogeochemical Cycles, Vol. 30, Issue 1 https://doi.org/10.1002/2015GB005239	journal	January 2016
Modeling Global Soil Carbon and Soil Microbial Carbon by Integrating Microbial Processes into the Ecosystem Process Model TRIPLEX-GHG: GLOBAL SOIL CARBON AND MICROBIAL CARBON Wang, Kefeng; Peng, Changhui; Zhu, Qiuan Journal of Advances in Modeling Earth Systems, Vol. 9, Issue 6 https://doi.org/10.1002/2017MS000920	journal	October 2017
Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction Yu, Youngseob; Lee, Changsoo; Kim, Jaai Biotechnology and Bioengineering, Vol. 89, Issue 6 https://doi.org/10.1002/bit.20347	journal	January 2005
Estimating taxon‐specific population dynamics in diverse microbial communities Koch, Benjamin J.; McHugh, Theresa A.; Hayer, Michaela Ecosphere, Vol. 9, Issue 1 https://doi.org/10.1002/ecs2.2090	journal	January 2018
Quantitative stable isotope probing with H ₂ ¹⁸ O to measure taxon‐specific microbial growth Purcell, Alicia M.; Dijkstra, Paul; Finley, Brianna Soil Science Society of America Journal, Vol. 84, Issue 5 https://doi.org/10.1002/saj2.20159	journal	September 2020
Microbial Taxon-Specific Isotope Incorporation with DNA Quantitative Stable Isotope Probing Finley, Brianna K.; Hayer, Michaela; Mau, Rebecca L. Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-9721-3_11	book	January 2019
A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming Rustad, L.; Campbell, J.; Marion, G. Oecologia, Vol. 126, Issue 4 https://doi.org/10.1007/s004420000544	journal	February 2001
Warming induced changes in soil carbon and nitrogen influence priming responses in four ecosystems Mau, Rebecca L.; Dijkstra, Paul; Schwartz, Egbert Applied Soil Ecology, Vol. 124 https://doi.org/10.1016/j.apsoil.2017.10.034	journal	March 2018
Short- and long-term warming alters soil microbial community and relates to soil traits Yu, Hongying; Ma, Quanhui; Liu, Xiaodi Applied Soil Ecology, Vol. 131 https://doi.org/10.1016/j.apsoil.2018.07.006	journal	October 2018
Comparison of temperature effects on soil respiration and bacterial and fungal growth rates PietikÃ¥inen, Janna; Pettersson, Marie; BÃ¥Ã¥th, Erland FEMS Microbiology Ecology, Vol. 52, Issue 1 https://doi.org/10.1016/j.femsec.2004.10.002	journal	March 2005
Long-term warming rather than grazing significantly changed total and active soil procaryotic community structures Che, Rongxiao; Deng, Yongcui; Wang, Weijin Geoderma, Vol. 316 https://doi.org/10.1016/j.geoderma.2017.12.005	journal	April 2018
Diminished soil functions occur under simulated climate change in a sup-alpine pasture, but heterotrophic temperature sensitivity indicates microbial resilience Mills, Robert T. E.; Gavazov, Konstantin S.; Spiegelberger, Thomas Science of The Total Environment, Vol. 473-474 https://doi.org/10.1016/j.scitotenv.2013.12.071	journal	March 2014
Comparison of factors limiting bacterial growth in different soils Demoling, Fredrik; Figueroa, Daniela; Bååth, Erland Soil Biology and Biochemistry, Vol. 39, Issue 10 https://doi.org/10.1016/j.soilbio.2007.05.002	journal	October 2007
Microbial biomass, functional capacity, and community structure after 12 years of soil warming Frey, S. D.; Drijber, R.; Smith, H. Soil Biology and Biochemistry, Vol. 40, Issue 11 https://doi.org/10.1016/j.soilbio.2008.07.020	journal	November 2008
Experimental warming effects on the microbial community of a temperate mountain forest soil Schindlbacher, A.; Rodler, A.; Kuffner, M. Soil Biology and Biochemistry, Vol. 43, Issue 7 https://doi.org/10.1016/j.soilbio.2011.03.005	journal	July 2011
Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain Shen, Congcong; Xiong, Jinbo; Zhang, Huayong Soil Biology and Biochemistry, Vol. 57 https://doi.org/10.1016/j.soilbio.2012.07.013	journal	February 2013
Bacterial and fungal community responses to reciprocal soil transfer along a temperature and soil moisture gradient in a glacier forefield Zumsteg, Anita; Bååth, Erland; Stierli, Beat Soil Biology and Biochemistry, Vol. 61 https://doi.org/10.1016/j.soilbio.2013.02.017	journal	June 2013
Soil microbes and their response to experimental warming over time: A meta-analysis of field studies Romero-Olivares, A. L.; Allison, S. D.; Treseder, K. K. Soil Biology and Biochemistry, Vol. 107 https://doi.org/10.1016/j.soilbio.2016.12.026	journal	April 2017
Metagenomics and stable isotope probing reveal the complementary contribution of fungal and bacterial communities in the recycling of dead biomass in forest soil López-Mondéjar, Rubén; Tláskal, Vojtěch; Větrovský, Tomáš Soil Biology and Biochemistry, Vol. 148 https://doi.org/10.1016/j.soilbio.2020.107875	journal	September 2020
Microbial contributions to climate change through carbon cycle feedbacks Bardgett, Richard D.; Freeman, Chris; Ostle, Nicholas J. The ISME Journal, Vol. 2, Issue 8 https://doi.org/10.1038/ismej.2008.58	journal	July 2008
The microbe-mediated mechanisms affecting topsoil carbon stock in Tibetan grasslands Yue, Haowei; Wang, Mengmeng; Wang, Shiping The ISME Journal, Vol. 9, Issue 9 https://doi.org/10.1038/ismej.2015.19	journal	February 2015
Where less may be more: how the rare biosphere pulls ecosystems strings Jousset, Alexandre; Bienhold, Christina; Chatzinotas, Antonis The ISME Journal, Vol. 11, Issue 4 https://doi.org/10.1038/ismej.2016.174	journal	January 2017
Temperature sensitivity of soil carbon decomposition and feedbacks to climate change Davidson, Eric A.; Janssens, Ivan A. Nature, Vol. 440, Issue 7081 https://doi.org/10.1038/nature04514	journal	March 2006
Microbial mediation of carbon-cycle feedbacks to climate warming Zhou, Jizhong; Xue, Kai; Xie, Jianping Nature Climate Change, Vol. 2, Issue 2 https://doi.org/10.1038/nclimate1331	journal	December 2011
Biogeochemical and ecological feedbacks in grassland responses to warming Wu, Zhuoting; Dijkstra, Paul; Koch, George W. Nature Climate Change, Vol. 2, Issue 6 https://doi.org/10.1038/nclimate1486	journal	April 2012
Global soil carbon projections are improved by modelling microbial processes Wieder, William R.; Bonan, Gordon B.; Allison, Steven D. Nature Climate Change, Vol. 3, Issue 10 https://doi.org/10.1038/nclimate1951	journal	July 2013
Managing uncertainty in soil carbon feedbacks to climate change Bradford, Mark A.; Wieder, William R.; Bonan, Gordon B. Nature Climate Change, Vol. 6, Issue 8 https://doi.org/10.1038/nclimate3071	journal	July 2016
Temperature mediates continental-scale diversity of microbes in forest soils Zhou, Jizhong; Deng, Ye; Shen, Lina Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12083	journal	July 2016
Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls Kallenbach, Cynthia M.; Frey, Serita D.; Grandy, A. Stuart Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13630	journal	November 2016
Soil-carbon response to warming dependent on microbial physiology Allison, Steven D.; Wallenstein, Matthew D.; Bradford, Mark A. Nature Geoscience, Vol. 3, Issue 5 https://doi.org/10.1038/ngeo846	journal	April 2010
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
The importance of anabolism in microbial control over soil carbon storage Liang, Chao; Schimel, Joshua P.; Jastrow, Julie D. Nature Microbiology, Vol. 2, Issue 8 https://doi.org/10.1038/nmicrobiol.2017.105	journal	July 2017
High proportions of bacteria and archaea across most biomes remain uncultured Steen, Andrew D.; Crits-Christoph, Alexander; Carini, Paul The ISME Journal, Vol. 13, Issue 12 https://doi.org/10.1038/s41396‐019‐0484‐y	journal	August 2019
Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change Malik, Ashish A.; Martiny, Jennifer B. H.; Brodie, Eoin L. The ISME Journal, Vol. 14, Issue 1 https://doi.org/10.1038/s41396‐019‐0510‐0	journal	September 2019
The diversity and biogeography of soil bacterial communities Fierer, N.; Jackson, R. B. Proceedings of the National Academy of Sciences, Vol. 103, Issue 3 https://doi.org/10.1073/pnas.0507535103	journal	January 2006
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample Caporaso, J. G.; Lauber, C. L.; Walters, W. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1000080107	journal	June 2010
Soil warming, carbon-nitrogen interactions, and forest carbon budgets Melillo, J. M.; Butler, S.; Johnson, J. Proceedings of the National Academy of Sciences, Vol. 108, Issue 23 https://doi.org/10.1073/pnas.1018189108	journal	May 2011
Temperature response of soil respiration largely unaltered with experimental warming Carey, Joanna C.; Tang, Jianwu; Templer, Pamela H. Proceedings of the National Academy of Sciences, Vol. 113, Issue 48 https://doi.org/10.1073/pnas.1605365113	journal	November 2016
Revisiting life strategy concepts in environmental microbial ecology Ho, Adrian; Lonardo, D. Paolo Di; Bodelier, Paul L. E. FEMS Microbiology Ecology https://doi.org/10.1093/femsec/fix006	journal	January 2017
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Community and ecosystem responses to recent climate change Walther, Gian-Reto Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, Issue 1549 https://doi.org/10.1098/rstb.2010.0021	journal	July 2010
Phylogenetic conservation of soil bacterial responses to simulated global changes Isobe, Kazuo; Bouskill, Nicholas J.; Brodie, Eoin L. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 375, Issue 1798 https://doi.org/10.1098/rstb.2019.0242	journal	March 2020
Lysobacter capsici sp. nov., with antimicrobial activity, isolated from the rhizosphere of pepper, and emended description of the genus Lysobacter Park, J. H.; Kim, R.; Aslam, Z. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 58, Issue 2 https://doi.org/10.1099/ijs.0.65290-0	journal	February 2008
Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling Sinsabaugh, Robert L.; Manzoni, Stefano; Moorhead, Daryl L. Ecology Letters, Vol. 16, Issue 7 https://doi.org/10.1111/ele.12113	journal	April 2013
Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming? Tucker, Colin L.; Bell, Jennifer; Pendall, Elise Global Change Biology, Vol. 19, Issue 1 https://doi.org/10.1111/gcb.12036	journal	October 2012
Investigating the long-term legacy of drought and warming on the soil microbial community across five European shrubland ecosystems Rousk, Johannes; Smith, Andrew R.; Jones, Davey L. Global Change Biology, Vol. 19, Issue 12 https://doi.org/10.1111/gcb.12338	journal	October 2013
Identifying the microbial taxa that consistently respond to soil warming across time and space Oliverio, Angela M.; Bradford, Mark A.; Fierer, Noah Global Change Biology, Vol. 23, Issue 5 https://doi.org/10.1111/gcb.13557	journal	November 2016
On the variability of respiration in terrestrial ecosystems: moving beyond Q10 Davidson, Eric A.; Janssens, Ivan A.; Luo, Yiqi Global Change Biology, Vol. 12, Issue 2 https://doi.org/10.1111/j.1365-2486.2005.01065.x	journal	February 2006
Temperature and soil organic matter decomposition rates - synthesis of current knowledge and a way forward Conant, Richard T.; Ryan, Michael G.; Ågren, Göran I. Global Change Biology, Vol. 17, Issue 11 https://doi.org/10.1111/j.1365‐2486.2011.02496.x	journal	August 2011
Thermal adaptation of soil microbial respiration to elevated temperature Bradford, Mark A.; Davies, Christian A.; Frey, Serita D. Ecology Letters, Vol. 11, Issue 12 https://doi.org/10.1111/j.1461‐0248.2008.01251.x	journal	December 2008
A meta-analysis of experimental warming effects on terrestrial nitrogen pools and dynamics Bai, Edith; Li, Shanlong; Xu, Wenhua New Phytologist, Vol. 199, Issue 2 https://doi.org/10.1111/nph.12252	journal	April 2013
Microbiomes in light of traits: A phylogenetic perspective Martiny, J. B. H.; Jones, S. E.; Lennon, J. T. Science, Vol. 350, Issue 6261 https://doi.org/10.1126/science.aac9323	journal	November 2015
Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world Melillo, J. M.; Frey, S. D.; DeAngelis, K. M. Science, Vol. 358, Issue 6359 https://doi.org/10.1126/science.aan2874	journal	October 2017
A global atlas of the dominant bacteria found in soil Delgado-Baquerizo, Manuel; Oliverio, Angela M.; Brewer, Tess E. Science, Vol. 359, Issue 6373 https://doi.org/10.1126/science.aap9516	journal	January 2018
Characterization of Growing Microorganisms in Soil by Stable Isotope Probing with H218O Schwartz, E. Applied and Environmental Microbiology, Vol. 73, Issue 8 https://doi.org/10.1128/AEM.02021-06	journal	February 2007
Microbial rRNA Synthesis and Growth Compared through Quantitative Stable Isotope Probing with H ₂ ¹⁸ O Papp, Katerina; Hungate, Bruce A.; Schwartz, Egbert Applied and Environmental Microbiology, Vol. 84, Issue 8 https://doi.org/10.1128/AEM.02441-17	journal	February 2018
Seasonal Responses of Extracellular Enzyme Activity and Microbial Biomass to Warming and Nitrogen Addition Bell, Terrence H.; Klironomos, John N.; Henry, Hugh A. L. Soil Science Society of America Journal, Vol. 74, Issue 3 https://doi.org/10.2136/sssaj2009.0036	journal	January 2010
Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton Apprill, A.; McNally, S.; Parsons, R. Aquatic Microbial Ecology, Vol. 75, Issue 2 https://doi.org/10.3354/ame01753	journal	June 2015
Microbial control over carbon cycling in soil Schimel, Joshua P.; Schaeffer, Sean M. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00348	journal	January 2012
Long-term forest soil warming alters microbial communities in temperate forest soils DeAngelis, Kristen M.; Pold, Grace; TopÃ§uoÄŸlu, BegÃ¼m D. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00104	journal	February 2015
The complex relationship between microbial growth rate and yield and its implications for ecosystem processes Lipson, David A. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00615	journal	June 2015

Similar Records

The effect of experimental ecosystem warming on CO2 fluxes in a montane meadow

Journal Article · 1997 · Global Change Biology · OSTI ID:841890

Saleska, Scott R; Harte, John; Torn, Margaret S

Microbial responses to inorganic nutrient amendment overridden by warming: Consequences on soil carbon stability

Journal Article · 2018 · Environmental Microbiology · OSTI ID:1567126

Wang, Mengmeng; Ding, Junjun; Sun, Bo; +9 more

The temperature sensitivity of soil: microbial biodiversity, growth, and carbon mineralization

Journal Article · 2021 · The ISME Journal · OSTI ID:1813712

Wang, Chao; Morrissey, Ember M.; Mau, Rebecca L.; +15 more

Title: Decreased growth of wild soil microbes after 15 years of transplant‐induced warming in a montane meadow

Citation Formats

References (61)

Similar Records

Related Subjects