The microbe-mediated mechanisms affecting topsoil carbon stock in Tibetan grasslands

Yue, Haowei; Wang, Mengmeng; Wang, Shiping; Gilbert, Jack A.; Sun, Xin; Wu, Linwei; Lin, Qiaoyan; Hu, Yigang; Li, Xiangzhen; He, Zhili; Zhou, Jizhong; Yang, Yunfeng

doi:10.1038/ismej.2015.19

The microbe-mediated mechanisms affecting topsoil carbon stock in Tibetan grasslands

Journal Article · Mon Feb 16 23:00:00 EST 2015 · The ISME Journal

DOI:https://doi.org/10.1038/ismej.2015.19· OSTI ID:1225223

Yue, Haowei ^[1]; Wang, Mengmeng ^[1]; Wang, Shiping ^[2]; Gilbert, Jack A. ^[3]; Sun, Xin ^[1]; Wu, Linwei ^[1]; Lin, Qiaoyan ^[4]; Hu, Yigang ^[5]; Li, Xiangzhen ^[6]; He, Zhili ^[7]; Zhou, Jizhong ^[8]; Yang, Yunfeng ^[1]

Tsinghua Univ., Beijing (China)
Chinese Academy of Sciences (CAS), Beijing (China); CAS Center for Excellence in Tibetan Plateau Earth Science, Beijing (China)
Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of Chicago, Chicago, IL (United States); Zhejiang Univ., Hangzhou (China)
Chinese Academy of Sciences (CAS), Xining (China)
Chinese Academy of Sciences (CAS), Xining (China); Chinese Academy of Sciences (CAS), Lanzhou (China)
Chinese Academy of Sciences (CAS), Sichuan (China)
Univ. of Oklahoma, Norman, OK (United States)
Tsinghua Univ., Beijing (China); Univ. of Oklahoma, Norman, OK (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Warming has been shown to cause soil carbon (C) loss in northern grasslands owing to accelerated microbial decomposition that offsets increased grass productivity. Yet, a multi-decadal survey indicated that the surface soil C stock in Tibetan alpine grasslands remained relatively stable. To investigate this inconsistency, we analyzed the feedback responses of soil microbial communities to simulated warming by soil transplant in Tibetan grasslands. Microbial functional diversity decreased in response to warming, whereas microbial community structure did not correlate with changes in temperature. The relative abundance of catabolic genes associated with nitrogen (N) and C cycling decreased with warming, most notably in genes encoding enzymes associated with more recalcitrant C substrates. By contrast, genes associated with C fixation increased in relative abundance. The relative abundance of genes associated with urease, glutamate dehydrogenase and ammonia monoxygenase (ureC, gdh and amoA) were significantly correlated with N₂O efflux. These results suggest that unlike arid/semiarid grasslands, Tibetan grasslands maintain negative feedback mechanisms that preserve terrestrial C and N pools. To examine whether these trends were applicable to the whole plateau, we included these measurements in a model and verified that topsoil C stocks remained relatively stable. Thus, by establishing linkages between microbial metabolic potential and soil biogeochemical processes, we conclude that long-term C loss in Tibetan grasslands is ameliorated by a reduction in microbial decomposition of recalcitrant C substrates.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-06CH11357; SC0004601

OSTI ID:: 1225223

Alternate ID(s):: OSTI ID: 1581098

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 9 Vol. 9; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (47)

Contrasting soil microbial community functional structures in two major landscapes of the Tibetan alpine meadow Chu, Houjuan; Wang, Shiping; Yue, Haowei MicrobiologyOpen, Vol. 3, Issue 5 https://doi.org/10.1002/mbo3.190	journal	July 2014
Relationships between soil moisture content and nitrous oxide production during nitrification and denitrification Klemedtsson, L.; Svensson, B. H.; Rosswall, T. Biology and Fertility of Soils, Vol. 6, Issue 2 https://doi.org/10.1007/bf00257658	journal	April 1988
Response of Microbial Community Composition and Function to Soil Climate Change Waldrop, M. P.; Firestone, M. K. Microbial Ecology, Vol. 52, Issue 4 https://doi.org/10.1007/s00248-006-9103-3	journal	October 2006
Field Simulation of Global Change: Transplanting Northern Bog Mesocosms Southward Breeuwer, Angela; Heijmans, Monique M. P. D.; Robroek, Bjorn J. M. Ecosystems, Vol. 13, Issue 5 https://doi.org/10.1007/s10021-010-9349-y	journal	June 2010
Linking microbial community composition and soil processes in a California annual grassland and mixed-conifer forest Balser, Teri C.; Firestone, Mary K. Biogeochemistry, Vol. 73, Issue 2 https://doi.org/10.1007/s10533-004-0372-y	journal	April 2005
Differences in yield, Ellenberg N value, tissue chemistry and soil chemistry 15 years after the cessation of nitrogen addition Stevens, Carly J.; Mountford, J. Owen; Gowing, David J. G. Plant and Soil, Vol. 357, Issue 1-2 https://doi.org/10.1007/s11104-012-1160-4	journal	March 2012
Effects of sample preparation on the measurement of organic carbon, hydrogen, nitrogen, sulfur, and oxygen concentrations in marine sediments Ryba, Stephan A.; Burgess, Robert M. Chemosphere, Vol. 48, Issue 1 https://doi.org/10.1016/s0045-6535(02)00027-9	journal	July 2002
Ecological responses to recent climate change Walther, Gian-Reto; Post, Eric; Convey, Peter Nature, Vol. 416, Issue 6879 https://doi.org/10.1038/416389a	journal	March 2002
Long-term experimental warming alters nitrogen-cycling communities but site factors remain the primary drivers of community structure in high arctic tundra soils Walker, Jennifer K. M.; Egger, Keith N.; Henry, Gregory H. R. The ISME Journal, Vol. 2, Issue 9 https://doi.org/10.1038/ismej.2008.52	journal	June 2008
Bacterial gene abundances as indicators of greenhouse gas emission in soils Morales, Sergio E.; Cosart, Theodore; Holben, William E. The ISME Journal, Vol. 4, Issue 6 https://doi.org/10.1038/ismej.2010.8	journal	February 2010
The microbial gene diversity along an elevation gradient of the Tibetan grassland Yang, Yunfeng; Gao, Ying; Wang, Shiping The ISME Journal, Vol. 8, Issue 2 https://doi.org/10.1038/ismej.2013.146	journal	August 2013
Microbial mediation of biogeochemical cycles revealed by simulation of global changes with soil transplant and cropping Zhao, Mengxin; Xue, Kai; Wang, Feng The ISME Journal, Vol. 8, Issue 10 https://doi.org/10.1038/ismej.2014.46	journal	April 2014
High sensitivity of peat decomposition to climate change through water-table feedback Ise, Takeshi; Dunn, Allison L.; Wofsy, Steven C. Nature Geoscience, Vol. 1, Issue 11 https://doi.org/10.1038/ngeo331	journal	October 2008
Characterizing changes in soil bacterial community structure in response to short-term warming Xiong, Jinbo; Sun, Huaibo; Peng, Fei FEMS Microbiology Ecology, Vol. 89, Issue 2 https://doi.org/10.1111/1574-6941.12289	journal	February 2014
Warming increases plant biomass and reduces diversity across continents, latitudes, and species migration scenarios in experimental wetland communities Baldwin, Andrew H.; Jensen, Kai; Schönfeldt, Marisa Global Change Biology, Vol. 20, Issue 3 https://doi.org/10.1111/gcb.12378	journal	December 2013
Soil Warming and Carbon-Cycle Feedbacks to the Climate System Melillo, J. M. Science, Vol. 298, Issue 5601 https://doi.org/10.1126/science.1074153	journal	December 2002
The Microbial Engines That Drive Earth's Biogeochemical Cycles Falkowski, P. G.; Fenchel, T.; Delong, E. F. Science, Vol. 320, Issue 5879 https://doi.org/10.1126/science.1153213	journal	May 2008
Field-Scale Transplantation Experiment To Investigate Structures of Soil Bacterial Communities at Pioneering Sites Lazzaro, Anna; Gauer, Andreas; Zeyer, Josef Applied and Environmental Microbiology, Vol. 77, Issue 23 https://doi.org/10.1128/aem.05778-11	journal	September 2011
Experimental Warming, not Grazing, Decreases Rangeland Quality on the Tibetan Plateau Klein, Julia A.; Harte, John; Zhao, Xin-Quan Ecological Applications, Vol. 17, Issue 2 https://doi.org/10.1890/05-0685	journal	March 2007
Changes in Soil Microbial Community Structure and Function in an Alpine Dry Meadow Following Spring Snow Melt Lipson, D. A.; Schadt, C. W.; Schmidt, S. K. Microbial Ecology, Vol. 43, Issue 3 https://doi.org/10.1007/s00248-001-1057-x	journal	May 2002
Symbiotic nitrogen fixation by legumes in two Chinese grasslands estimated with the 15N dilution technique Yang, Baijie; Qiao, Na; Xu, Xingliang Nutrient Cycling in Agroecosystems, Vol. 91, Issue 1 https://doi.org/10.1007/s10705-011-9448-y	journal	July 2011
Effects of sample preparation on the measurement of organic carbon, hydrogen, nitrogen, sulfur, and oxygen concentrations in marine sediments Ryba, Stephan A.; Burgess, Robert M. Chemosphere, Vol. 48, Issue 1 https://doi.org/10.1016/S0045-6535(02)00027-9	journal	July 2002
GeoChip as a metagenomics tool to analyze the microbial gene diversity along an elevation gradient Gao, Ying; Wang, Shiping; Xu, Depeng Genomics Data, Vol. 2 https://doi.org/10.1016/j.gdata.2014.06.003	journal	December 2014
Fluxes of CO2, CH4, and N2O in an alpine meadow affected by yak excreta on the Qinghai-Tibetan plateau during summer grazing periods Lin, Xingwu; Wang, Shiping; Ma, Xiuzhi Soil Biology and Biochemistry, Vol. 41, Issue 4 https://doi.org/10.1016/j.soilbio.2009.01.007	journal	April 2009
Pathways of nitrogen utilization by soil microorganisms – A review Geisseler, Daniel; Horwath, William R.; Joergensen, Rainer Georg Soil Biology and Biochemistry, Vol. 42, Issue 12 https://doi.org/10.1016/j.soilbio.2010.08.021	journal	December 2010
Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils He, Ji-Zheng; Hu, Hang-Wei; Zhang, Li-Mei Soil Biology and Biochemistry, Vol. 55 https://doi.org/10.1016/j.soilbio.2012.06.006	journal	December 2012
How soil moisture, rain pulses, and growth alter the response of ecosystem respiration to temperature: RAIN, GROWTH, AND RESPIRATION Xu, Liukang; Baldocchi, Dennis D.; Tang, Jianwu Global Biogeochemical Cycles, Vol. 18, Issue 4 https://doi.org/10.1029/2004GB002281	journal	October 2004
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
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
Increased cuticular carbon sequestration and lignin oxidation in response to soil warming Feng, Xiaojuan; Simpson, André J.; Wilson, Kevin P. Nature Geoscience, Vol. 1, Issue 12 https://doi.org/10.1038/ngeo361	journal	November 2008
Atmospheric nitrogen deposition promotes carbon loss from peat bogs Bragazza, L.; Freeman, C.; Jones, T. Proceedings of the National Academy of Sciences, Vol. 103, Issue 51 https://doi.org/10.1073/pnas.0606629104	journal	December 2006
The interactive effects of soil transplant into colder regions and cropping on soil microbiology and biogeochemistry: Effects of northward soil transplant and cropping Liu, Shanshan; Wang, Feng; Xue, Kai Environmental Microbiology, Vol. 17, Issue 3 https://doi.org/10.1111/1462-2920.12398	journal	February 2014
Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland Yang, Yunfeng; Wu, Linwei; Lin, Qiaoyan Global Change Biology, Vol. 19, Issue 2 https://doi.org/10.1111/gcb.12065	journal	November 2012
Soil microbial responses to experimental warming and clipping in a tallgrass prairie Zhang, W.; Parker, K. M.; Luo, Y. Global Change Biology, Vol. 11, Issue 2 https://doi.org/10.1111/j.1365-2486.2005.00902.x	journal	February 2005
Diurnal, seasonal and annual variation in net ecosystem CO ₂ exchange of an alpine shrubland on Qinghai-Tibetan plateau Zhao, Liang; Li, Yingnian; Xu, Shixiao Global Change Biology, Vol. 12, Issue 10 https://doi.org/10.1111/j.1365-2486.2006.01197.x	journal	October 2006
Changes in topsoil carbon stock in the Tibetan grasslands between the 1980s and 2004: SOC CHANGES IN TIBETAN GRASSLANDS Yang, Yuanhe; Fang, Jingyun; Smith, Pete Global Change Biology, Vol. 15, Issue 11 https://doi.org/10.1111/j.1365-2486.2009.01924.x	journal	November 2009
Transplantation of organic surface horizons of boreal soils into warmer regions alters microbiology but not the temperature sensitivity of decomposition: WARMING, SOIL BIOLOGY AND DECOMPOSITION Vanhala, Pekka; Karhu, Kristiina; Tuomi, Mikko Global Change Biology, Vol. 17, Issue 1 https://doi.org/10.1111/j.1365-2486.2009.02154.x	journal	December 2010
Temperature effects on forest herbs assessed by warming and transplant experiments along a latitudinal gradient: FOREST HERBS AND CLIMATE WARMING De FRENNE, Pieter; Brunet, JÖRg; Shevtsova, Anna Global Change Biology, Vol. 17, Issue 10 https://doi.org/10.1111/j.1365-2486.2011.02449.x	journal	May 2011
Increased plant productivity in Alaskan tundra as a result of experimental warming of soil and permafrost: Increased plant productivity in Alaskan tundra Natali, Susan M.; Schuur, Edward A. G.; Rubin, Rachel L. Journal of Ecology, Vol. 100, Issue 2 https://doi.org/10.1111/j.1365-2745.2011.01925.x	journal	November 2011
Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time: Warming effects on tundra vegetation Elmendorf, Sarah C.; Henry, Gregory H. R.; Hollister, Robert D. Ecology Letters, Vol. 15, Issue 2 https://doi.org/10.1111/j.1461-0248.2011.01716.x	journal	December 2011
Carbon dynamics of terrestrial ecosystems on the Tibetan Plateau during the 20th century: an analysis with a process-based biogeochemical model: Carbon dynamics on the Tibetan Plateau Zhuang, Q.; He, J.; Lu, Y. Global Ecology and Biogeography https://doi.org/10.1111/j.1466-8238.2010.00559.x	journal	June 2010
Terrestrial carbon-cycle feedback to climate warming: experimental evidence on plant regulation and impacts of biofuel feedstock harvest Luo, Yiqi; Sherry, Rebecca; Zhou, Xuhui GCB Bioenergy, Vol. 1, Issue 1 https://doi.org/10.1111/j.1757-1707.2008.01005.x	journal	February 2009
Field-Scale Transplantation Experiment To Investigate Structures of Soil Bacterial Communities at Pioneering Sites Lazzaro, Anna; Gauer, Andreas; Zeyer, Josef Applied and Environmental Microbiology, Vol. 77, Issue 23 https://doi.org/10.1128/AEM.05778-11	journal	September 2011
Responses of Grassland Production to Single and Multiple Global Environmental Changes Dukes, Jeffrey S.; Chiariello, Nona R.; Cleland, Elsa E. PLoS Biology, Vol. 3, Issue 10 https://doi.org/10.1371/journal.pbio.0030319	journal	August 2005
Integrating Experimental and Gradient Methods in Ecological Climate Change Research Dunne, Jennifer A.; Saleska, Scott R.; Fischer, Marc L. Ecology, Vol. 85, Issue 4 https://doi.org/10.1890/03-8003	journal	April 2004
Long-term experimental warming and nutrient additions increase productivity in tall deciduous shrub tundra DeMarco, Jennie; Mack, Michelle C.; Bret-Harte, M. Syndonia Ecosphere, Vol. 5, Issue 6 https://doi.org/10.1890/ES13-00281.1	journal	June 2014
Experimental Warming, not Grazing, Decreases Rangeland Quality on the Tibetan Plateau Klein, Julia A.; Harte, John; Zhao, Xin-Quan Figshare https://doi.org/10.6084/m9.figshare.c.3293654.v1	collection	January 2016

Cited By (19)

Microbial responses to southward and northward Cambisol soil transplant Wang, Mengmeng; Liu, Shanshan; Wang, Feng MicrobiologyOpen, Vol. 4, Issue 6 https://doi.org/10.1002/mbo3.302	journal	October 2015
Soil bacterial and fungal diversity differently correlated with soil biochemistry in alpine grassland ecosystems in response to environmental changes Zhang, Yong; Dong, Shikui; Gao, Qingzhu Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep43077	journal	March 2017
Long-Term Warming in Alaska Enlarges the Diazotrophic Community in Deep Soils Feng, Jiajie; Penton, C. Ryan; He, Zhili mBio, Vol. 10, Issue 1 https://doi.org/10.1128/mbio.02521-18	journal	February 2019
Zonal Soil Type Determines Soil Microbial Responses to Maize Cropping and Fertilization Zhao, Mengxin; Sun, Bo; Wu, Linwei mSystems, Vol. 1, Issue 4 https://doi.org/10.1128/msystems.00075-16	journal	July 2016
Progressive Microbial Community Networks with Incremental Organic Loading Rates Underlie Higher Anaerobic Digestion Performance Wu, Linwei; Shan, Xiaoyu; Chen, Si mSystems, Vol. 5, Issue 1 https://doi.org/10.1128/msystems.00357-19	journal	January 2020
Bacteriophage–prokaryote dynamics and interaction within anaerobic digestion processes across time and space Zhang, Junyu; Gao, Qun; Zhang, Qiuting Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0272-8	journal	May 2017
Effects of Short-Term Warming and Altered Precipitation on Soil Microbial Communities in Alpine Grassland of the Tibetan Plateau Zhang, Kaoping; Shi, Yu; Jing, Xin Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01032	journal	June 2016
Variations of Soil Microbial Community Structures Beneath Broadleaved Forest Trees in Temperate and Subtropical Climate Zones Yang, Sihang; Zhang, Yuguang; Cong, Jing Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00200	journal	February 2017
The Biogeographic Pattern of Microbial Functional Genes along an Altitudinal Gradient of the Tibetan Pasture Qi, Qi; Zhao, Mengxin; Wang, Shiping Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00976	journal	June 2017
Microbial Community and Functional Gene Changes in Arctic Tundra Soils in a Microcosm Warming Experiment Yang, Ziming; Yang, Sihang; Van Nostrand, Joy D. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01741	journal	September 2017
Taxonomic and Functional Responses of Soil Microbial Communities to Annual Removal of Aboveground Plant Biomass Guo, Xue; Zhou, Xishu; Hale, Lauren Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00954	journal	May 2018
Microbial functional diversity: From concepts to applications Escalas, Arthur; Hale, Lauren; Voordeckers, James W. Ecology and Evolution, Vol. 9, Issue 20 https://doi.org/10.1002/ece3.5670	journal	September 2019
Alpine soil carbon is vulnerable to rapid microbial decomposition under climate cooling Wu, Linwei; Yang, Yunfeng; Wang, Shiping The ISME Journal, Vol. 11, Issue 9 https://doi.org/10.1038/ismej.2017.75	journal	May 2017
Autogenic succession and deterministic recovery following disturbance in soil bacterial communities Jurburg, Stephanie D.; Nunes, Inês; Stegen, James C. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep45691	journal	April 2017
Alpine soil microbial ecology in a changing world Donhauser, Johanna; Frey, Beat FEMS Microbiology Ecology, Vol. 94, Issue 9 https://doi.org/10.1093/femsec/fiy099	journal	May 2018
Molecular mechanisms of water table lowering and nitrogen deposition in affecting greenhouse gas emissions from a Tibetan alpine wetland Wang, Hao; Yu, Lingfei; Zhang, Zhenhua Global Change Biology, Vol. 23, Issue 2 https://doi.org/10.1111/gcb.13467	journal	September 2016
Potential feedback mediated by soil microbiome response to warming in a glacier forefield Wang, Yuwan; Ma, Anzhou; Liu, Guohua Global Change Biology, Vol. 26, Issue 2 https://doi.org/10.1111/gcb.14936	journal	December 2019
Soil organic matter quantity and quality shape microbial community compositions of subtropical broadleaved forests Ding, Junjun; Zhang, Yuguang; Wang, Mengmeng Molecular Ecology, Vol. 24, Issue 20 https://doi.org/10.1111/mec.13384	journal	October 2015
Dissimilar responses of fungal and bacterial communities to soil transplantation simulating abrupt climate changes Zhao, Mengxin; Sun, Bo; Wu, Linwei Molecular Ecology, Vol. 28, Issue 7 https://doi.org/10.1111/mec.15053	journal	April 2019

Similar Records

Evaluating the lingering effect of livestock grazing on functional potentials of microbial communities in Tibetan grassland soils

Journal Article · Tue Apr 19 00:00:00 EDT 2016 · Plant and Soil · OSTI ID:1567066

Related Subjects

54 ENVIRONMENTAL SCIENCES

The microbe-mediated mechanisms affecting topsoil carbon stock in Tibetan grasslands

Citation Formats

References (47)

Cited By (19)

Similar Records

Related Subjects