Microorganisms exert overriding impacts on the temperature sensitivity of soil C decomposition than substrate quality

Abstract

Understanding the temperature sensitivity (Q₁₀) of soil carbon (C) decomposition and the driving forces is vital for projecting soil C dynamics under climate warming. However, it is unclear of the geographic patterns in Q₁₀ and its driving forces in water-limited regions. We measured Q₁₀ of C decomposition and multiple facets of both C quality and microbial properties, including microbial diversity, abundance, composition, activity, and trophic strategy from two soil depths (0−10 cm, 30−50 cm) collected at 38 sites along a 2000-km transect in northern China’s deserts. Q₁₀ ranged in 1.56−4.80 and was significantly higher in the top (3.21) than deep soil (2.61). The large variation in Q₁₀ is directly determined by microorganisms, rather than C quality which is the ratio of microbial C decomposition rate over soil organic C content. Microbial diversity, the ratio of fungi to bacterial abundance (F:B), and mass-specific respiration (qCO₂) were driving forces for spatial variation in Q₁₀. Microbial diversity negatively impacted Q₁₀, while higher F:B and qCO₂ stimulated Q₁₀. Higher C quality indirectly inhibited Q₁₀ by improving microbial diversity, and decreasing F:B and qCO₂. Our study demonstrates that microorganisms drive the geographic variations in Q₁₀.

Graphical abstract

Keywords

climate warming / C quality-temperature theory / microbial diversity / F:B / temperate desert.

Highlight

	● Q10 ranged from 1.56−4.80 and was higher in the top than deep soil.
	● The total effect of microorganisms was higher than C quality on Q10 of C decomposition.
	● Microbial diversity, F:B, and qCO2 were driving forces over the variation in Q10.
	● Q10 was negatively associated with microbial diversity, positively with F:B and qCO2.
	● C quality changed microorganisms to indirectly mediate Q10.

References

[1] Adingo, S., Yu, J.R., Liu, X.L., Li, X.D., Jing, S., Zhang, X., 2021. Variation of soil microbial carbon use efficiency (CUE) and its influence mechanism in the context of global environmental change: a review. PeerJ9, e12131.

[2] Adingo, S., Yu, J.R., L iu X.L., Li, X.D., Jing, S., Zhang, X., 2021. Land-use change influence soil quality parameters at an ecologically fragile area of YongDeng County of Gansu Province, China. PeerJ9, e12246.

[3] Allison, S.D., Treseder, K.K., 2008. Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Global Change Biology14, 2898–2909.

[4] Alster, C.J., Baas, P., Wallenstein, M.D., Johnson, N.G., von Fischer, J.C., 2016. Temperature sensitivity as a microbial trait using parameters from macromolecular rate theory. Frontiers in Microbiology7, 1821.

[5] Alster, C.J., Weller, Z.D., von Fischer, J.C. 2018. A meta-analysis of temperature sensitivity as a microbial trait. Global Change Biology24, 4211–4224.

[6] Bardgett, R.D., Hobbs, P.J., Frostegård, Å., 1996. Changes in soil fungal: bacterial biomass ratios following reductions in the intensity of management of an upland grassland. Biology and Fertility of Soils22, 261–264.

[7] Bates, D., Mächler, M., Bolker, B., Walker, S., 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software67, 1–48.

[8] Bölscher, T., Wadsö, L., Börjesson, G., Herrmann, A.M., 2016. Differences in substrate use efficiency: impacts of microbial community composition, land use management, and substrate complexity. Biology and Fertility of Soils52, 547–559.

[9] Bond-Lamberty, B., Thomson, A. 2010. Temperature-associated increases in the global soil respiration record. Nature464, 579–582.

[10] Brookes, P.C., Landman, A., Pruden, G., Jenkinson, D.S., 1985. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biology and Biochemistry17, 837–842.

[11] Cable, J.M., Ogle, K., Lucas, R.W., Huxman, T.E., Loik, M.E., Smith, S.D., Tissue, D.T., Ewers, B.E., Pendall, E., Welker, J.M., Charlet, T.N., Cleary, M., Griffith, A., Nowak, R.S., Rogers, M., Steltzer, H., Sullivan, P.F., Van Gestel, N.C., 2011. The temperature responses of soil respiration in deserts: a seven desert synthesis. Biogeochemistry103, 71–90.

[12] Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Lozupone, C.A., Turnbaugh, P.J., Fierer, N., Knight, R., 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America108, 4516–4522.

[13] Carey, J.C., Tang, J.W., Templer, P.H., Kroeger, K.D., Crowther, T.W., Burton, A.J., Dukes, J.S., Emmett, B., Frey, S.D., Heskel, M.A., Jiang, L.F., Machmuller, M.B., Mohan, J., Panetta, A.M., Reich, P.B., Reinsch, S., Wang, X., Allison, S.D., Bamminger, C., Bridgham, S., Collins, S.L., De Dato, G., Eddy, W.C., Enquist, B.J., Estiarte, M., Harte, J., Henderson, A., Johnson, B.R., Larsen, K.S., Luo, Y.Q., Marhan, S., Melillo, J.M., Peñuelas, J., Pfeifer-Meister, L., Poll, C., Rastetter, E., Reinmann, A.B., Reynolds, L.L., Schmidt, I.K., Shaver, G.R., Strong, A.L., Suseela, V., Tietema, A. 2016. Temperature response of soil respiration largely unaltered with experimental warming. Proceedings of the National Academy of Sciences of the United States of America113, 13797–13802.

[14] Chen, H.Y., Jing, Q.F., Liu, X., Zhou, X.H., Fang, C.M., Li, B., Zhou, S.R., Nie, M., 2022a. Microbial respiratory thermal adaptation is regulated by r-/K-strategy dominance. Ecology Letters25, 2489–2499.

[15] Chen, S.T., Zhang, M.M., Zou, J.W., Hu, Z.H., 2022b. Relationship between basal soil respiration and the temperature sensitivity of soil respiration and their key controlling factors across terrestrial ecosystems. Journal of Soils and Sediments22, 769–781.

[16] Chen, Y.J., Neilson, J.W., Kushwaha, P., Maier, R.M., Barberán, A., 2021. Life-history strategies of soil microbial communities in an arid ecosystem. The ISME Journal15, 649–657.

[17] Cox, P.M., Betts, R.A., Jones, C.D., Spall, S.A., Totterdell, I.J., 2000. Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature408, 184–187.

[18] Crowther, T.W., Todd-Brown, K.E.O., Rowe, C.W., Wieder, W.R., Carey, J.C., Machmuller, M.B., Snoek, B.L., Fang, S., Zhou, G., Allison, S.D., Blair, J.M., Bridgham, S.D., Burton, A.J., Carrillo, Y., Reich, P.B., Clark, J.S., Classen, A.T., Dijkstra, F.A., Elberling, B., Emmett, B.A., Estiarte, M., Frey, S.D., Guo, J., Harte, J., Jiang, L., Johnson, B.R., Kröel-Dulay, G., Larsen, K.S., Laudon, H., Lavallee, J.M., Luo, Y., Lupascu, M., Ma, L.N., Marhan, S., Michelsen, A., Mohan, J., Niu, S., Pendall, E., Peñuelas, J., Pfeifer-Meister, L., Poll, C., Reinsch, S., Reynolds, L.L., Schmidt, I.K., Sistla, S., Sokol, N.W., Templer, P.H., Treseder, K.K., Welker, J.M., Bradford, M.A., 2016. Quantifying global soil carbon losses in response to warming. Nature540, 104–108.

[19] Davidson, E.A, Janssens, I.A. 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature440, 165–173.

[20] Delgado-Baquerizo, M., Reich, P.B., Trivedi, C., Eldridge, D.J., Abades, S., Alfaro, F.D., Bastida, F., Berhe, A.A., Cutler, N.A., Gallardo, A., García-Velázquez, L., Hart, S.C., Hayes, P.E., He, J.Z., Hseu, Z.Y., Hu, H.W., Kirchmair, M., Neuhauser, S., Pérez, C.A., Reed, S.C., Santos, F., Sullivan, B.W., Trivedi, P., Wang, J.T., Weber-Grullon, L., Williams, M.A., Singh, B.K., 2020. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nature Ecology & Evolution4, 210–220.

[21] Demyan, M.S., Rasche, F., Schulz, E., Breulmann, M., Müller, T., Cadisch, G., 2012. Use of specific peaks obtained by diffuse reflectance Fourier transform mid-infrared spectroscopy to study the composition of organic matter in a Haplic Chernozem. European Journal of Soil Science63, 189–199.

[22] Ding, J.Z., Chen, L.Y., Zhang, B.B., Liu, L., Yang, G.B., Fang, K., Chen, Y.L., Li, F., Kou, D., Ji, C.J., Luo, Y.Q., Yang, Y.H., 2016. Linking temperature sensitivity of soil CO₂ release to substrate, environmental, and microbial properties across alpine ecosystems. Global Biogeochemical Cycles30, 1310–1323.

[23] Dong, L.W., Sun, Y., Ran, J.Z., Hu, W.G., Ji, M.F., Du, Q.J., Xiong, J.L., Gong, H.Y., Yao, S.R., Adnan Akram, M., Zhang, Y.H., Hou, Q.Q., Li, H.L., Sun, Y., Lu, J.L., Wang, X.T., Aqeel, M., Zhu, J.X., Schmidt, M.W.I., Niklas, K.J., Deng, J.M., 2022. Ecosystem organic carbon storage and their drivers across the drylands of China. CATENA214, 106280.

[24] Eng, A.Y., Narayanan, A., Alster, C.J., DeAngelis, K.M., 2023. Thermal adaptation of soil microbial growth traits in response to chronic warming. Applied and Environmental Microbiology89, e0082523.

[25] Fang, C.M., Smith, P., Moncrieff, J.B., Smith, J.U., 2005. Similar response of labile and resistant soil organic matter pools to changes in temperature. Nature433, 57–59.

[26] Feng, J., Wang, J., Song, Y., Zhu, B., 2018. Patterns of soil respiration and its temperature sensitivity in grassland ecosystems across China. Biogeosciences15, 5329–5341.

[27] Fierer, N., Colman, B.P., Schimel, J.P., Jackson, R.B., 2006. Predicting the temperature dependence of microbial respiration in soil: a continental-scale analysis. Global Biogeochemical Cycles20, B3026.

[28] Finn, D.R., Bergk-Pinto, B., Hazard, C., Nicol, G.W., Tebbe, C.C., Vogel, T.M., 2021. Functional trait relationships demonstrate life strategies in terrestrial prokaryotes. FEMS Microbiology Ecology97, fiab068.

[29] Fox, J., Weisberg, S., 2019. An R Companion to Applied Regression. 3rd ed. Philadelphia: Sage.

[30] Gent, P.R., Danabasoglu, G., Donner, L.J., Holland, M.M., Hunke, E.C., Jayne, S.R., Lawrence, D.M., Neale, R.B., Rasch, P.J., Vertenstein, M., Worley, P.H., Yang, Z.L., Zhang, M.H., 2011. The community climate system model version 4. Journal of Climate24, 4973–4991.

[31] Gershenson, A., Bader, N.E., Cheng, W.X., 2009. Effects of substrate availability on the temperature sensitivity of soil organic matter decomposition. Global Change Biology15, 176–183.

[32] Hamdi, S., Moyano, F., Sall, S., Bernoux, M., Chevallier, T., 2013. Synthesis analysis of the temperature sensitivity of soil respiration from laboratory studies in relation to incubation methods and soil conditions. Soil Biology and Biochemistry58, 115–126.

[33] Heimann, M., Reichstein, M., 2008. Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature451, 289–292.

[34] Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., Jarvis, A., 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology25, 1965–1978.

[35] Hou, J.F., Dijkstra, F.A., Zhang, X.W., Wang, C., Lü, X.T., Wang, P., Han, X.G., Cheng, W.X., 2019. Aridity thresholds of soil microbial metabolic indices along a 3,200 km transect across arid and semi-arid regions in northern China. PeerJ7, e6712.

[36] Huang, G., Su, Y.G., Wu, G.P., Huang, Z.Y., Lin, S.N., Cheng, H., 2022. Cyanobacterial- and moss-forming biocrusts consistently decrease the temperature sensitivity of microbial respiration along a continental precipitation gradient. Functional Ecology36, 3107–3119.

[37] Huntingford C., Atkin, O.K., Martinez-de la Torre, A., Mercado, L.M., Heskel, M.A., Harper, A.B., Bloomfield, K.J., O’sullivan, O.S., Reich, P.B., Wythers, K.R., Butler, E.E., Chen, M., Griffin, K.L., Meir, P., Tjoelker, M.G., Turnbull, M.H., Sitch, S., Wiltshire, A., Malhi, Y., 2017. Implications of improved representations of plant respiration in a changing climate. Nature Communication8, 1602.

[38] Jobbágy, E.G., Jackson, R.B., 2000. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecological Applications10, 423–436.

[39] Jones, C.D., Hughes, J.K., Bellouin, N., Hardiman, S.C., Jones, G.S., Knight, J., Liddicoat, S., O'connor, F.M., Andres, R.J., Bell, C., Boo, K.O., Bozzo, A., Butchart, N., Cadule, P., Corbin, K.D., Doutriaux-Boucher, M., Friedlingstein, P., Gornall, J., Gray, L., Halloran, P.R., Hurtt, G., Ingram, W.J., Lamarque, J.F., Law, R.M., Meinshausen, M., Osprey, S., Palin, E.J., Parsons Chini, L., Raddatz, T., Sanderson, M.G., Sellar, A.A., Schurer, A., Valdes, P., Wood, N., Woodward, S., Yoshioka, M., Zerroukat, M., 2011. The HadGEM2-ES implementation of CMIP5 centennial simulations. Geoscientific Model Development4, 543–570.

[40] Karhu, K., Auffret, M.D., Dungait, J.A.J., Hopkins, D.W., Prosser, J.I., Singh, B.K., Subke, J.A., Wookey, P.A., Ågren, G.I., Sebastià, M.T., Gouriveau, F., Bergkvist, G., Meir, P., Nottingham, A.T., Salinas, N., Hartley, I.P., 2014. Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature513, 81–84.

[41] Knorr, W., Prentice, I.C., House, J.I., Holland, E.A., 2005. Long-term sensitivity of soil carbon turnover to warming. Nature433, 298–301.

[42] Koven, C.D., Hugelius, G., Lawrence, D.M., Wieder, W.R., 2017. Higher climatological temperature sensitivity of soil carbon in cold than warm climates. Nature Climate Change7, 817–822.

[43] Lefcheck, J.S., 2016. piecewiseSEM: Piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods in Ecology and Evolution7, 573–579.

[44] Lehmann, J., Kleber, M., 2015. The contentious nature of soil organic matter. Nature528, 60–68.

[45] Li, H., Yang, S., Semenov, M.V., Yao, F., Ye, J., Bu, R.C., Ma, R.A., Lin, J.J., Kurganova, I., Wang, X.G., Deng, Y., Kravchenko, I., Jiang, Y., Kuzyakov, Y., 2021. Temperature sensitivity of SOM decomposition is linked with a K-selected microbial community. Global Change Biology27, 2763–2779.

[46] Li, J.Q., Nie, M., Pendall, E., 2019. An incubation study of temperature sensitivity of greenhouse gas fluxes in three land-cover types near Sydney, Australia. Science of the Total Environment688, 324–332.

[47] Li, J.Q., Pei, J.M., Pendall, E., Fang, C.M., Nie, M., 2020a. Spatial heterogeneity of temperature sensitivity of soil respiration: A global analysis of field observations. Soil Biology and Biochemistry141, 107675.

[48] Li, J.Q., Pei, J.M., Pendall, E., Reich, P.B., Noh, N. J., Li, B., Fang, C.M., Nie, M., 2020b. Rising temperature may trigger deep soil carbon loss across forest ecosystems. Advanced Science7, 2001242.

[49] Li, J.Q., Yan, D., Pendall, E., Pei, J.M., Noh, N.J., He, J.S., Li, B., Nie, M., Fang, C.M., 2018. Depth dependence of soil carbon temperature sensitivity across Tibetan permafrost regions. Soil Biology and Biochemistry126, 82–90.

[50] Li, X.J., Xie, J.S., Zhang, Q.F., Lyu, M., Xiong, X.L., Liu, X.F., Lin, T., Yang, Y.S., 2020c. Substrate availability and soil microbes drive temperature sensitivity of soil organic carbon mineralization to warming along an elevation gradient in subtropical Asia. Geoderma364, 114198.

[51] Liaw, A., Wiener, M., 2002. Classification and regression by randomForest. R News2, 18–22.

[52] Malik, A.A., Martiny, J.B.H., Brodie, E.L., Martiny, A.C., Treseder, K.K., Allison, S.D., 2020. Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change. The ISME Journal14, 1–9.

[53] McKinlay, J.B., Cook, G.M., Hards, K., 2020. Chapter four–microbial energy management–A product of three broad tradeoffs. Advances in Microbial Physiology77, 139–185.

[54] Moni, C., Lerch, T.Z., de Zarruk, K.K., Strand, L.T., Forte, C., Certini, G., Rasse, D.P., 2015. Temperature response of soil organic matter mineralisation in arctic soil profiles. Soil Biology and Biochemistry88, 236–246.

[55] Nadeau, J.A., Qualls, R.G., Nowak, R.S., Blank, R.R., 2007. The potential bioavailability of organic C, N, and P through enzyme hydrolysis in soils of the Mojave Desert. Biogeochemistry82, 305–320.

[56] Niu, B., Zhang, X.Z., Piao, S.L., Janssens, I.A., Fu, G., He, Y.T., Zhang, Y.J., Shi, P.L., Dai, E.F., Yu, C.Q., Zhang, J., Yu, G.R., Xu, M., Wu, J.S., Zhu, L.P., Desai, A.R., Chen, J.Q., Bohrer, G., Gough, C.M., Mammarella, I., Varlagin, A., Fares, S., Zhao, X.Q., Li, Y.N., Wang, H.M., Ouyang, Z., 2021. Warming homogenizes apparent temperature sensitivity of ecosystem respiration. Science Advances7, eabc7358.

[57] Nottingham, A. T., Meir, P., Velasquez, E., Turner, B.L., 2020. Soil carbon loss by experimental warming in a tropical forest. Nature584, 234–237.

[58] Pang, X.Y., Zhu, B.A., Lü, X.T., Cheng, W.X., 2015. Labile substrate availability controls temperature sensitivity of organic carbon decomposition at different soil depths. Biogeochemistry126, 85–98.

[59] Paul, E.A., 2015. Soil Microbiology, Ecology and Biochemistry. 4th ed. Amsterdam: Elsevier.

[60] Peng, S.S., Piao, S.L., Wang, T., Sun, J.Y., Shen, Z.H., 2009. Temperature sensitivity of soil respiration in different ecosystems in China. Soil Biology and Biochemistry41, 1008–1014.

[61] Podrebarac, F.A., Laganière, J., Billings, S.A., Edwards, K.A., Ziegler, S.E., 2016. Soils isolated during incubation underestimate temperature sensitivity of respiration and its response to climate history. Soil Biology and Biochemistry93, 60–68.

[62] Pries, C.E.H., Castanha, C., Porras, R.C., Torn, M.S., 2017. The whole-soil carbon flux in response to warming. Science355, 1420–1423.

[63] Qin, S.Q., Chen, L.Y., Fang, K., Zhang, Q.W., Wang, J., Liu, F.T., Yu, J.C., Yang, Y.H., 2019. Temperature sensitivity of SOM decomposition governed by aggregate protection and microbial communities. Science Advances5, eaau1218.

[64] Ramin, K.I, Allison, S.D., 2019. Bacterial tradeoffs in growth rate and extracellular enzymes. Frontiers in Microbiology10, 2956.

[65] Reynolds, L.L., Lajtha, K., Bowden, R.D., Johnson, B.R., Bridgham, S.D., 2017. The carbon quality-temperature hypothesis does not consistently predict temperature sensitivity of soil organic matter mineralization in soils from two manipulative ecosystem experiments. Biogeochemistry136, 249–260.

[66] Rong, G.H., Zhang, X.J., Wu, H.Y., Ge, N.N., Yao, Y.F., Wei, X.R., 2021. Changes in soil organic carbon and nitrogen mineralization and their temperature sensitivity in response to afforestation across China’s Loess Plateau. CATENA202, 105226.

[67] Schipper, L.A., Hobbs, J.K., Rutledge, S., Arcus, V.L., 2014. Thermodynamic theory explains the temperature optima of soil microbial processes and high Q₁₀ values at low temperatures. Global Change Biology20, 3578–3586.

[68] Slessarev, E.W., Lin, Y., Jiménez, B.Y., Homyak, P.M., Chadwick, O.A., D’Antonio, C.M., Schimel, J.P., 2020. Cellular and extracellular C contributions to respiration after wetting dry soil. Biogeochemistry147, 307–324.

[69] Smith, N.G., Dukes, J.S., 2013. Plant respiration and photosynthesis in global-scale models: incorporating acclimation to temperature and CO₂. Global Change Biology19, 45–63.

[70] Strickland, M.S., Rousk, J., 2010. Considering fungal: bacterial dominance in soils–methods, controls, and ecosystem implications. Soil Biology and Biochemistry42, 1385–1395.

[71] Su, Y.G., Chen, Y.W., Padilla, F.M., Zhang, Y.M., Huang, G., 2020. The influence of biocrusts on the spatial pattern of soil bacterial communities: a case study at landscape and slope scales. Soil Biology and Biochemistry142, 107721.

[72] Su, Y.G., Huang, G., Lin, S.N., Huang, Z.Y., Wu, G.P., Cheng, H., 2023a. Patterns of organic carbon and nitrogen stocks in soil particle-size fractions along an aridity gradient in northern China's deserts. CATENA221, 106785.

[73] Su, Y.G., Huang, G., Liu, J., 2023b. Biocrusts alleviate the aggravating C limitation in microbial respiration with increasing aridity. Geoderma429, 116210.

[74] Tang, J., Cheng, H., Fang, C.M., 2017. The temperature sensitivity of soil organic carbon decomposition is not related to labile and recalcitrant carbon. PLoS One12, e0186675.

[75] Thiessen, S., Gleixner, G., Wutzler, T., Reichstein, M., 2013. Both priming and temperature sensitivity of soil organic matter decomposition depend on microbial biomass–An incubation study. Soil Biology and Biochemistry57, 739–748.

[76] Thomas, A.D., Hoon, S.R., Dougill, A.J., 2011. Soil respiration at five sites along the Kalahari Transect: effects of temperature, precipitation pulses and biological soil crust cover. Geoderma167, 284–294.

[77] Tucker, C.L., Ferrenberg, S., Reed, S.C., 2019. Climatic sensitivity of dryland soil CO2 fluxes differs dramatically with biological soil crust successional state. Ecosystems22, 15–32.

[78] Tucker, C.L., Reed, S.C., 2016. Low soil moisture during hot periods drives apparent negative temperature sensitivity of soil respiration in a dryland ecosystem: a multi-model comparison. Biogeochemistry128, 155–169.

[79] Wagg, C., Bender, S.F., Widmer, F., van der Heijden, M.G.A., 2014. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proceedings of the National Academy of Sciences of the United States of America111, 5266–5270.

[80] Wang, B., Zha, T.S., Jia, X., Wu, B., Zhang, Y.Q., Qin, S.G., 2014a. Soil moisture modifies the response of soil respiration to temperature in a desert shrub ecosystem. Biogeosciences11, 259–268.

[81] Wang, C., Morrissey, E.M., Mau, R.L., Hayer, M., Piñeiro, J., Mack, M.C., Marks, J.C., Bell, S.L., Miller, S.N., Dijkstra, E.S.P., Koch, B.J., Stone, B.W., Purcell, A.M., Blazewicz, S.J., Hofmockel, K.S., Pett-Ridge, J., Hungate, B.A., 2021. The temperature sensitivity of soil: microbial biodiversity, growth, and carbon mineralization. The ISME Journal15, 2738–2747.

[82] Wang, M.M., Guo, X.W., Zhang, S., Xiao, L.J., Mishra, U., Yang, Y.H., Zhu, B.A., Wang, G.C., Mao, X.L., Qian, T., Jiang, T., Shi, Z., Luo, Z.K., 2022. Global soil profiles indicate depth-dependent soil carbon losses under a warmer climate. Nature Communications13, 5514.

[83] Wang, Q.K., Liu, S.G., Tian, P., 2018. Carbon quality and soil microbial property control the latitudinal pattern in temperature sensitivity of soil microbial respiration across Chinese forest ecosystems. Global Change Biology24, 2841–2849.

[84] Wang, X., Liu, L.L., Piao, S.L., Janssens, I.A., Tang, J.W., Liu, W.X., Chi, Y.G., Wang, J., Xu, S., 2014b. Soil respiration under climate warming: differential response of heterotrophic and autotrophic respiration. Global Change Biology20, 3229–3237.

[85] Wang, X., Piao, S., Ciais, P., Friedlingstein, P., Myneni, R.B., Cox, P., Miller, J., Peng, S.S., Wang, T., Yang, H., Chen, A., 2014. A two-fold increase of carbon cycle sensitivity to tropical temperature variations. Nature506, 212–215.

[86] Wetterstedt, J.Å.M., Persson, T., Ågren, G.I., 2010. Temperature sensitivity and substrate quality in soil organic matter decomposition: results of an incubation study with three substrates. Global Change Biology16, 1806–1819.

[87] White, T.J., Bruns, T., Lee, S., Taylor, J., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J., eds. PCR Protocols: A Guide to Methods and Applications. San Diego: Academic Press, 315–322.

[88] Xu, M., Li, Z. 2016. Accumulated temperature changes in desert region and surrounding area during 1960–2013: a case study in the Alxa Plateau, Northwest China. Environmental Earth Sciences75, 1–12.

[89] Yang, S., Wu, H., Wang, Z.R., Semenov, M.V., Ye, J., Yin, L.M., Wang, X.G., Kravchenko, I., Semenov, V., Kuzyakov, Y., Jiang, Y., Li, H., 2022. Linkages between the temperature sensitivity of soil respiration and microbial life strategy are dependent on sampling season. Soil Biology and Biochemistry172, 108758.

[90] Zak, D.R., Ringelberg, D.B., Pregitzer, K.S., Randlett, D.L., White, D.C., Curtis, P.S., 1996. Soil microbial communities beneath Populus grandidentata grown under elevated atmospheric CO₂. Ecological Applications6, 257–262.

[91] Zeng, X.M., Feng, J., Chen, J., Delgado-Baquerizo, M., Zhang, Q.G., Zhou, X.Q., Yuan, Y.S., Feng, S.H., Zhang, K.X., Liu, Y.R., Huang, Q.Y., 2022. Microbial assemblies associated with temperature sensitivity of soil respiration along an altitudinal gradient. Science of the Total Environment820, 153257.

[92] Zhang, H.J., Yao, X.D., Zeng, W.J., Fang, Y., Wang, W., 2020. Depth dependence of temperature sensitivity of soil carbon dioxide, nitrous oxide and methane emissions. Soil Biology and Biochemistry149, 107956.

[93] Zheng, Z.M., Yu, G.R., Fu, Y.L., Wang, Y.S., Sun, X.M., Wang, Y.H., 2009. Temperature sensitivity of soil respiration is affected by prevailing climatic conditions and soil organic carbon content: a trans-China based case study. Soil Biology and Biochemistry41, 1531–1540.

[94] Zhu, B.A., Cheng, W.X., 2011. Constant and diurnally-varying temperature regimes lead to different temperature sensitivities of soil organic carbon decomposition. Soil Biology and Biochemistry43, 866–869.

[95] Zogg, G.P., Zak, D.R., Ringelberg, D.B., White, D. C., MacDonald, N.W., Pregitzer, K.S., 1997. Compositional and functional shifts in microbial communities due to soil warming. Soil Science Society of America Journal61, 475–481.

RIGHTS & PERMISSIONS

Higher Education Press