Short-term warming increased soil heterotrophic respiration due to enhanced active microbial community

Xie, Min; He, Liyuan; Guo, Yaoxin; Wang, Jun; Zhou, Sha; Zhao, Fazhu

doi:10.1007/s11104-025-07769-w

Short-term warming increased soil heterotrophic respiration due to enhanced active microbial community

Journal Article · Wed Aug 06 00:00:00 EDT 2025 · Plant and Soil

DOI:https://doi.org/10.1007/s11104-025-07769-w· OSTI ID:2586868

Xie, Min ^[1]; He, Liyuan ^[2]; Guo, Yaoxin ^[3]; Wang, Jun ^[4]; Zhou, Sha ^[5]; ^[1]

Northwest University, Shaanxi (China); Shaanxi Xi’an Urban Ecosystem National Observation and Research Station (China)
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Northwest University, Shaanxi (China)
Northwest University, Shaanxi (China); Shaanxi Xi’an Urban Ecosystem National Observation and Research Station (China); Chinese Academy of Sciences and Ministry of Water Resources, Yangling (China)
Xi’an Botanical Garden of Shaanxi Province (Institute of Botany of Shaanxi Province) (China)

Soil microbes, particularly active microbes, play a crucial role in conserving soil carbon under climate change, especially in forest ecosystems, constituting over 50% of global soil organic carbon. Nevertheless, the response mechanisms of active microbial community to climate warming and their subsequent impacts on soil heterotrophic respiration (Rh) remain insufficiently understood. To resolve this mechanistic uncertainty, we implemented a 3-year soil translocation experiment to investigate soil warming effects on active microbial community and Rh. We used 16S rRNA gene amplicon sequencing, Metatranscriptomics sequencing, coupled with correlation analyses to explore the linkages between warming-induced shifts in Rh and the active microbial community. Our results demonstrated that warming of soil induced a 55% enhancement in Rh. Concurrently, the Shannon index and Richness of active microbial community increased by 20% and 117%, respectively. Warming significantly altered active microbial community composition, inducing a compositional shift characterized by 0.5-to 2-fold increases in the abundances of Proteobacteria, Chloroflexi, and Actinobacteria. Our study also revealed 92–100% increases in the abundance of C-degradation functional genes encoding starch, cellulose, and lignin decomposition pathways within active microbial community under warming. Statistical analyses identified significant positive correlations between Rh and the abundance of Proteobacteria and Actinobacteria, as well as expression levels of functional genes associated with lignin and cellulose decomposition pathways. Furthermore, our results suggested that short-term warming increased Rh through altering diversity, species composition, and C degradation functional genes of active microbial community providing insights into the influence of microbial communities on soil C-climate feedbacks under climate warming.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: National Natural Science Foundation of China; USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 2586868

Journal Information:: Plant and Soil, Journal Name: Plant and Soil Vol. 513; ISSN 1573-5036; ISSN 0032-079X

Publisher:: Springer Science and Business Media LLCCopyright Statement

Country of Publication:: United States

Language:: English

References (67)

Unaltered soil microbial community composition, but decreased metabolic activity in a semiarid grassland after two years of passive experimental warming Fang, Chao; Ke, Wenbin; Campioli, Matteo Ecology and Evolution, Vol. 10, Issue 21 https://doi.org/10.1002/ece3.6862	journal	October 2020
Soil pH Determines Microbial Diversity and Composition in the Park Grass Experiment Zhalnina, Kateryna; Dias, Raquel; de Quadros, Patricia Dörr Microbial Ecology, Vol. 69, Issue 2 https://doi.org/10.1007/s00248-014-0530-2	journal	November 2014
Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review Blagodatskaya, Е.; Kuzyakov, Y. Biology and Fertility of Soils, Vol. 45, Issue 2 https://doi.org/10.1007/s00374-008-0334-y	journal	October 2008
On maintenance and metabolisms in soil microbial communities Dijkstra, Paul; Martinez, Ayla; Thomas, Scott C. Plant and Soil, Vol. 476, Issue 1-2 https://doi.org/10.1007/s11104-022-05382-9	journal	April 2022
16S rRNA-based bacterial community structure is a sensitive indicator of soil respiration activity Che, Rongxiao; Deng, Yongcui; Wang, Fang Journal of Soils and Sediments, Vol. 15, Issue 9 https://doi.org/10.1007/s11368-015-1152-0	journal	June 2015
Linkages of C: N: P stoichiometry between soil and leaf and their response to climatic factors along altitudinal gradients Zhang, Yu; Li, Chen; Wang, Maolin Journal of Soils and Sediments, Vol. 19, Issue 4 https://doi.org/10.1007/s11368-018-2173-2	journal	November 2018
Temperature effects on soil organic carbon, soil labile organic carbon fractions, and soil enzyme activities under long-term fertilization regimes Qi, Ruimin; Li, Juan; Lin, Zhian Applied Soil Ecology, Vol. 102 https://doi.org/10.1016/j.apsoil.2016.02.004	journal	June 2016
Global pattern of warming effects on microbial respiration is explained by soil microbial biomass carbon and nitrogen Liang, Guopeng CATENA, Vol. 250 https://doi.org/10.1016/j.catena.2025.108728	journal	March 2025
Linkages of C:N:P stoichiometry and bacterial community in soil following afforestation of former farmland Ren, Chengjie; Zhao, Fazhu; Kang, Di Forest Ecology and Management, Vol. 376 https://doi.org/10.1016/j.foreco.2016.06.004	journal	September 2016
Differential soil microbial community responses to the linkage of soil organic carbon fractions with respiration across land-use changes Ren, Chengjie; Wang, Tao; Xu, Yadong Forest Ecology and Management, Vol. 409 https://doi.org/10.1016/j.foreco.2017.11.011	journal	February 2018
Changes of soil microbial and enzyme activities are linked to soil C, N and P stoichiometry in afforested ecosystems Zhao, F. Z.; Ren, C. J.; Han, X. H. Forest Ecology and Management, Vol. 427 https://doi.org/10.1016/j.foreco.2018.06.011	journal	November 2018
Responses of wetland soil bacterial community and edaphic factors to two-year experimental warming and Spartina alterniflora invasion in Chongming Island Song, Shanshan; Zhang, Chao; Gao, Yue Journal of Cleaner Production, Vol. 250, p. 119502 https://doi.org/10.1016/j.jclepro.2019.119502	journal	March 2020
Effects of simulated warming on soil microbial community diversity and composition across diverse ecosystems Zhao, Jiayi; Xie, Xuan; Jiang, Yuying Science of The Total Environment, Vol. 911 https://doi.org/10.1016/j.scitotenv.2023.168793	journal	February 2024
Soil extracellular enzyme stoichiometry reveals the nutrient limitations in soil microbial metabolism under different carbon input manipulations Abay, Peryzat; Gong, Lu; Luo, Yan Science of The Total Environment, Vol. 913 https://doi.org/10.1016/j.scitotenv.2023.169793	journal	February 2024
The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and l-DOPA DeForest, Jared L. Soil Biology and Biochemistry, Vol. 41, Issue 6 https://doi.org/10.1016/j.soilbio.2009.02.029	journal	June 2009
Responses of soil heterotrophic respiration to moisture availability: An exploration of processes and models Moyano, Fernando E.; Manzoni, Stefano; Chenu, Claire Soil Biology and Biochemistry, Vol. 59 https://doi.org/10.1016/j.soilbio.2013.01.002	journal	April 2013
Active microorganisms in soil: Critical review of estimation criteria and approaches Blagodatskaya, Evgenia; Kuzyakov, Yakov Soil Biology and Biochemistry, Vol. 67 https://doi.org/10.1016/j.soilbio.2013.08.024	journal	December 2013
Stoichiometry of soil extracellular enzyme activity along a climatic transect in temperate grasslands of northern China Peng, Xiaoqian; Wang, Wei Soil Biology and Biochemistry, Vol. 98 https://doi.org/10.1016/j.soilbio.2016.04.008	journal	July 2016
Microbial diversity limits soil heterotrophic respiration and mitigates the respiration response to moisture increase Zhang, Fen-Guo; Zhang, Quan-Guo Soil Biology and Biochemistry, Vol. 98 https://doi.org/10.1016/j.soilbio.2016.04.017	journal	July 2016
Growth explains microbial carbon use efficiency across soils differing in land use and geology Zheng, Qing; Hu, Yuntao; Zhang, Shasha Soil Biology and Biochemistry, Vol. 128 https://doi.org/10.1016/j.soilbio.2018.10.006	journal	January 2019
Microbial functional genes driving the positive priming effect in forest soils along an elevation gradient Zhao, Fazhu; Wang, Jieying; Li, Yi Soil Biology and Biochemistry, Vol. 165 https://doi.org/10.1016/j.soilbio.2021.108498	journal	February 2022
Long-term fertilizer postponing promotes soil organic carbon sequestration in paddy soils by accelerating lignin degradation and increasing microbial necromass Zhou, Yan; Zhang, Jianwei; Xu, Lei Soil Biology and Biochemistry, Vol. 175 https://doi.org/10.1016/j.soilbio.2022.108839	journal	December 2022
Shifts in C-degradation genes and microbial metabolic activity with vegetation types affected the surface soil organic carbon pool Huang, Qian; Wang, Baorong; Shen, Jikai Soil Biology and Biochemistry, Vol. 192 https://doi.org/10.1016/j.soilbio.2024.109371	journal	May 2024
Global analysis of soil bacterial genera and diversity in response to pH Zhou, Xuan; Tahvanainen, Teemu; Malard, Lucie Soil Biology and Biochemistry, Vol. 198 https://doi.org/10.1016/j.soilbio.2024.109552	journal	November 2024
Soil respiration related to the molecular composition of soil organic matter in subtropical and temperate forests under soil warming Liu, Yanchun; Wang, Hui; Schindlbacher, Andreas Soil Biology and Biochemistry, Vol. 201 https://doi.org/10.1016/j.soilbio.2024.109661	journal	February 2025
The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil Saiya-Cork, K. R.; Sinsabaugh, R. L.; Zak, D. R. Soil Biology and Biochemistry, Vol. 34, Issue 9 https://doi.org/10.1016/s0038-0717(02)00074-3	journal	September 2002
Temperature effects on the diversity of soil heterotrophs and the δ13C of soil-respired CO2 Andrews, Jeffrey A.; Matamala, Roser; Westover, Kristi M. Soil Biology and Biochemistry, Vol. 32, Issue 5 https://doi.org/10.1016/s0038-0717(99)00206-0	journal	May 2000
Soil bacterial and fungal communities across a pH gradient in an arable soil Rousk, Johannes; Bååth, Erland; Brookes, Philip C. The ISME Journal, Vol. 4, Issue 10 https://doi.org/10.1038/ismej.2010.58	journal	May 2010
Active and total microbial communities in forest soil are largely different and highly stratified during decomposition Baldrian, Petr; Kolařík, Miroslav; Štursová, Martina The ISME Journal, Vol. 6, Issue 2 https://doi.org/10.1038/ismej.2011.95	journal	July 2011
Changing precipitation pattern alters soil microbial community response to wet-up under a Mediterranean-type climate Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K. The ISME Journal, Vol. 9, Issue 4 https://doi.org/10.1038/ismej.2014.192	journal	October 2014
Long-term soil transplant simulating climate change with latitude significantly alters microbial temporal turnover Liang, Yuting; Jiang, Yuji; Wang, Feng The ISME Journal, Vol. 9, Issue 12 https://doi.org/10.1038/ismej.2015.78	journal	May 2015
Microbial diversity drives multifunctionality in terrestrial ecosystems Delgado-Baquerizo, Manuel; Maestre, Fernando T.; Reich, Peter B. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10541	journal	January 2016
Microbial seed banks: the ecological and evolutionary implications of dormancy Lennon, Jay T.; Jones, Stuart E. Nature Reviews Microbiology, Vol. 9, Issue 2 https://doi.org/10.1038/nrmicro2504	journal	January 2011
A moisture function of soil heterotrophic respiration that incorporates microscale processes Yan, Zhifeng; Bond-Lamberty, Ben; Todd-Brown, Katherine E. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04971-6	journal	July 2018
Acidification suppresses the natural capacity of soil microbiome to fight pathogenic Fusarium infections Li, Xiaogang; Chen, Dele; Carrión, Víctor J. Nature Communications, Vol. 14, Issue 1 https://doi.org/10.1038/s41467-023-40810-z	journal	August 2023
Experimental warming accelerates positive soil priming in a temperate grassland ecosystem Tao, Xuanyu; Yang, Zhifeng; Feng, Jiajie Nature Communications, Vol. 15, Issue 1 https://doi.org/10.1038/s41467-024-45277-0	journal	February 2024
Thermal sensitivity of soil microbial carbon use efficiency across forest biomes Ren, Chengjie; Zhou, Zhenghu; Delgado-Baquerizo, Manuel Nature Communications, Vol. 15, Issue 1 https://doi.org/10.1038/s41467-024-50593-6	journal	July 2024
The soil microbiome governs the response of microbial respiration to warming across the globe Sáez-Sandino, Tadeo; García-Palacios, Pablo; Maestre, Fernando T. Nature Climate Change, Vol. 13, Issue 12 https://doi.org/10.1038/s41558-023-01868-1	journal	December 2023
Soil respiration response to decade-long warming modulated by soil moisture in a boreal forest Liang, Guopeng; Stefanski, Artur; Eddy, William C. Nature Geoscience, Vol. 17, Issue 9 https://doi.org/10.1038/s41561-024-01512-3	journal	August 2024
Globally rising soil heterotrophic respiration over recent decades Bond-Lamberty, Ben; Bailey, Vanessa L.; Chen, Min Nature, Vol. 560, Issue 7716 https://doi.org/10.1038/s41586-018-0358-x	journal	August 2018
Soil properties explain tree growth and mortality, but not biomass, across phosphorus-depleted tropical forests Soong, Jennifer L.; Janssens, Ivan A.; Grau, Oriol Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-58913-8	journal	February 2020
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
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
Variability of ecosystem carbon source from microbial respiration is controlled by rainfall dynamics Huang, Heng; Calabrese, Salvatore; Rodriguez-Iturbe, Ignacio Proceedings of the National Academy of Sciences, Vol. 118, Issue 52 https://doi.org/10.1073/pnas.2115283118	journal	December 2021
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
Microbial life under ice: Metagenome diversity and in situ activity of Verrucomicrobia in seasonally ice‐covered Lakes Tran, Patricia; Ramachandran, Arthi; Khawasik, Ola Environmental Microbiology, Vol. 20, Issue 7 https://doi.org/10.1111/1462-2920.14283	journal	July 2018
Change in active microbial community structure, abundance and carbon cycling in an acid rice paddy soil with the addition of biochar: Microbial community affected by biochar in a paddy soil Chen, J.; Sun, X.; Li, L. European Journal of Soil Science, Vol. 67, Issue 6 https://doi.org/10.1111/ejss.12388	journal	November 2016
Microbial responses to warming enhance soil carbon loss following translocation across a tropical forest elevation gradient Nottingham, Andrew T.; Whitaker, Jeanette; Ostle, Nick J. Ecology Letters, Vol. 22, Issue 11 https://doi.org/10.1111/ele.13379	journal	September 2019
Long‐term geothermal warming reduced stocks of carbon but not nitrogen in a subarctic forest soil Peplau, Tino; Schroeder, Julia; Gregorich, Edward Global Change Biology, Vol. 27, Issue 20 https://doi.org/10.1111/gcb.15754	journal	July 2021
Microbial community shifts correspond with suppression of decomposition 25 years after liming of acidic forest soils Sridhar, Bhavya; Wilhelm, Roland C.; Debenport, Spencer J. Global Change Biology, Vol. 28, Issue 18 https://doi.org/10.1111/gcb.16321	journal	July 2022
Substrate availability and not thermal acclimation controls microbial temperature sensitivity response to long‐term warming Domeignoz‐Horta, Luiz A.; Pold, Grace; Erb, Hailey Global Change Biology, Vol. 29, Issue 6 https://doi.org/10.1111/gcb.16544	journal	December 2022
Altered activities of extracellular soil enzymes by the interacting global environmental changes Zuccarini, Paolo; Sardans, Jordi; Asensio, Loles Global Change Biology, Vol. 29, Issue 8 https://doi.org/10.1111/gcb.16604	journal	February 2023
Soil organic matter priming: The pH effects Wang, Chaoqun; Kuzyakov, Yakov Global Change Biology, Vol. 30, Issue 6 https://doi.org/10.1111/gcb.17349	journal	June 2024
Intrinsic microbial temperature sensitivity and soil organic carbon decomposition in response to climate change Li, Sen; Delgado‐Baquerizo, Manuel; Ding, Jixian Global Change Biology, Vol. 30, Issue 6 https://doi.org/10.1111/gcb.17395	journal	June 2024
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
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
Soil warming increases the number of growing bacterial taxa but not their growth rates Metze, Dennis; Schnecker, Jörg; de Carlan, Coline Le Noir Science Advances, Vol. 10, Issue 8 https://doi.org/10.1126/sciadv.adk6295	journal	February 2024
Microbial change in warming soils Metcalfe, Daniel B. Science, Vol. 358, Issue 6359 https://doi.org/10.1126/science.aap7325	journal	October 2017
Variation in pH Optima of Hydrolytic Enzyme Activities in Tropical Rain Forest Soils Turner, Benjamin L. Applied and Environmental Microbiology, Vol. 76, Issue 19 https://doi.org/10.1128/aem.00560-10	journal	August 2010
High Microbial Diversity Promotes Soil Ecosystem Functioning Maron, Pierre-Alain; Sarr, Amadou; Kaisermann, Aurore Applied and Environmental Microbiology, Vol. 84, Issue 9 https://doi.org/10.1128/aem.02738-17	journal	February 2018
Contrasting Soil pH Effects on Fungal and Bacterial Growth Suggest Functional Redundancy in Carbon Mineralization Rousk, J.; Brookes, P. C.; Baath, E. Applied and Environmental Microbiology, Vol. 75, Issue 6 https://doi.org/10.1128/aem.02775-08	journal	January 2009
The Role of Microbial Community Composition in Controlling Soil Respiration Responses to Temperature Auffret, Marc D.; Karhu, Kristiina; Khachane, Amit PLOS ONE, Vol. 11, Issue 10 https://doi.org/10.1371/journal.pone.0165448	journal	October 2016
Temperature Dependence of Net Nitrogen and Sulfur Mineralization Ellert, B. H.; Bettany, J. R. Soil Science Society of America Journal, Vol. 56, Issue 4 https://doi.org/10.2136/sssaj1992.03615995005600040021x	journal	July 1992
Resuscitation of the rare biosphere contributes to pulses of ecosystem activity Aanderud, Zachary T.; Jones, Stuart E.; Fierer, Noah Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00024	journal	January 2015
Changes in the Size of the Active Microbial Pool Explain Short-Term Soil Respiratory Responses to Temperature and Moisture Salazar-Villegas, Alejandro; Blagodatskaya, Evgenia; Dukes, Jeffrey S. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00524	journal	April 2016
Survival and Energy Producing Strategies of Alkane Degraders Under Extreme Conditions and Their Biotechnological Potential Park, Chulwoo; Park, Woojun Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01081	journal	May 2018
Global spatiotemporal distribution of soil respiration modeled using a global database Hashimoto, S.; Carvalhais, N.; Ito, A. Biogeosciences Discussions, Vol. 12, Issue 5 https://doi.org/10.5194/bgd-12-4331-2015	journal	January 2015

Similar Records

Microbial responses to long-term warming differ across soil microenvironments

Journal Article · Fri Apr 05 20:00:00 EDT 2024 · ISME Communications · OSTI ID:2396863

Winter warming in Alaska accelerates lignin decomposition contributed by Proteobacteria

Journal Article · Thu Jun 04 20:00:00 EDT 2020 · Microbiome · OSTI ID:1632050

Related Subjects

Active microbial community
Climate Change
Environmental Microbiology
Forest soil
Palaeoclimate
Short-term warming
Soil Chemistry
Soil Microbiology
Soil Science
Soil heterotrophic respiration

Short-term warming increased soil heterotrophic respiration due to enhanced active microbial community

Citation Formats

References (67)

Similar Records

Related Subjects