Long-term warming does not affect soil ecoenzyme activity and original microbial nutrient limitation on the Qinghai–Tibet Plateau

Abstract

•No notable effect from long-term warming on activity of nutrient-acquiring enzymes.

•Long-term warming does not notably affect enzymatic stoichiometry.

•Significant, positive correlation between ecoenzyme activity and soil nutrients, microbial biomass.

•Phosphorus limitation found for all soil microbes at different depths.

Microbes play an important role in the carbon cycle and nutrient flow of the soil ecosystem. However, the response of microbial activities to long-term warming over decades is poorly understood. To determine how warming changes ecoenzyme activity and microbial nutrient limitation, we conducted a long-term, 21 years, experiment, on the Qinghai–Tibet Plateau. We selected typical grass- and shrub-covered plots, used fiberglass open-top chambers (OTCs) to raise the temperature, conducted soil sampling at different depths, studied the response of nutrient-acquiring enzyme activity and stoichiometry, and conducted vector analysis of stoichiometry. Our results showed that long-term warming did not have a notable effect on the activity of nutrient-acquiring enzymes or enzymatic stoichiometry. However, Spearman correlation analysis indicated a significant and positive correlation between ecoenzyme activity and the available nutrients and microbial biomass in soil. Vector analysis of stoichiometry showed phosphorus limitation for all soil microbes at different depths, regardless of whether the soil experienced warming. These changes in enzymatic stoichiometry and vector analysis suggested that microbial nutrient limitation was not alleviated substantially by long-term warming, and warming did not considerably affect the stratification of microbial nutrient limitation. Our research has also shown that long-term warming does not significantly change soil ecoenzyme activity and original microbial nutrient limitation at different soil depths within the OTUsʼ impact range. These results could help improve understanding of microbial thermal acclimation and response to future long-term global warming.

Graphical abstract

Keywords

Global warming / Ecoenzymatic stoichiometry / Microbial nutrient limitation / Thermal acclimation / Qinghai–Tibet Plateau

References

[1] Bai, T., Tao, J., Li, Z., Shu, M., Yan, X., Wang, P., Ye, C., Guo, H., Wang, Y., Hu, S., 2019. Different microbial responses in top- and sub-soils to elevated temperature and substrate addition in a semiarid grassland on the Loess Plateau. European Journal of Soil Science 70, 1025–1036

[2] Barta, J., Slajsova, P., Tahovska, K., Picek, T., Santruckova, H., 2014. Different temperature sensitivity and kinetics of soil enzymes indicate seasonal shifts in C, N and P nutrient stoichiometry in acid forest soil. Biogeochemistry 117, 525–537

[3] Bradford, M.A., 2013. Thermal adaptation of decomposer communities in warming soils. Frontiers in Microbiology 4, 4

[4] Bradford, M.A., Davies, C.A., Frey, S.D., Maddox, T.R., Melillo, J.M., Mohan, J.E., Reynolds, J.F., Treseder, K.K., Wallenstein, M.D., 2008. Thermal adaptation of soil microbial respiration to elevated temperature. Ecology Letters 11, 1316–1327

[5] Bradford, M.A., Watts, B.W., Davies, C.A., 2010. Thermal adaptation of heterotrophic soil respiration in laboratory microcosms. Global Change Biology 16, 1576–1588

[6] 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 & Biochemistry 17, 837–842

[7] Caldwell, B.A., 2005. Enzyme activities as a component of soil biodiversity: A review. Pedobiologia 49, 637–644

[8] Chen, H., Zheng, M., Mao, Q., Xiao, K., Wang, K., Li, D., 2019. Cropland conversion changes the status of microbial resource limitation in degraded karst soil. Geoderma 352, 197–203

[9] Chen, W., Zhou, H., Wu, Y., Wang, J., Zhao, Z., Li, Y., Qiao, L., Chen, K., Liu, G., Xue, S., 2020. Direct and indirect influences of long-term fertilization on microbial carbon and nitrogen cycles in an alpine grassland. Soil Biology & Biochemistry 149, 149

[10] Cleveland, C.C., Liptzin, D., 2007. C: N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85, 235–252

[11] Craine, J.M., Fierer, N., McLauchlan, K.K., 2010. Widespread coupling between the rate and temperature sensitivity of organic matter decay. Nature Geoscience 3, 854–857

[12] Crowther, T.W., Bradford, M.A., 2013. Thermal acclimation in widespread heterotrophic soil microbes. Ecology Letters 16, 469–477

[13] Cui, Y., Fang, L., Guo, X., Wang, X., Zhang, Y., Li, P., Zhang, X., 2018. Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern Loess Plateau, China. Soil Biology & Biochemistry 116, 11–21

[14] Curiel Yuste, J., Ma, S., Baldocchi, D.D., 2010. Plant-soil interactions and acclimation to temperature of microbial-mediated soil respiration may affect predictions of soil CO₂ efflux. Biogeochemistry 98, 127–138

[15] Dacal, M., Bradford, M.A., Plaza, C., Maestre, F.T., Garcia-Palacios, P., 2019. Soil microbial respiration adapts to ambient temperature in global drylands. Nature Ecology & Evolution 3, 232–238

[16] Davidson, E.A., Janssens, I.A., 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173

[17] Deltedesco, E., Keiblinger, K.M., Piepho, H.P., Antonielli, L., Poetsch, E.M., Zechmeister-Boltenstern, S., Gorfer, M., 2020. Soil microbial community structure and function mainly respond to indirect effects in a multifactorial climate manipulation experiment. Soil Biology & Biochemistry 142, 142

[18] Eliasson, P.E., McMurtrie, R.E., Pepper, D.A., Stromgren, M., Linder, S., Agren, G.I., 2005. The response of heterotrophic CO₂ flux to soil warming. Global Change Biology 11, 167–181

[19] Fierer, N., Schimel, J.P., Holden, P.A., 2003. Variations in microbial community composition through two soil depth profiles. Soil Biology & Biochemistry 35, 167–176

[20] Fissore, C., Giardina, C.P., Kolka, R.K., Trettin, C.C., King, G.M., Jurgensen, M.F., Barton, C.D., McDowell, S.D., 2008. Temperature and vegetation effects on soil organic carbon quality along a forested mean annual temperature gradient in North America. Global Change Biology 14, 193–205

[21] Ganjurjav, H., Gao, Q., Gornish, E.S., Schwartz, M.W., Liang, Y., Cao, X., Zhang, W., Zhang, Y., Li, W., Wan, Y., Li, Y., Danjiu, L., Guo, H., Lin, E., 2016. Differential response of alpine steppe and alpine meadow to climate warming in the central Qinghai-Tibetan Plateau. Agricultural and Forest Meteorology 223, 233–240

[22] Giasson, M.A., Ellison, A.M., Bowden, R.D., Crill, P.M., Davidson, E.A., Drake, J.E., Frey, S.D., Hadley, J.L., Lavine, M., Melillo, J.M., Munger, J.W., Nadelhoffer, K.J., Nicoll, L., Ollinger, S.V., Savage, K.E., Steudler, P.A., Tang, J., Varner, R.K., Wofsy, S.C., Foster, D.R., Finzi, A.C., 2013. Soil respiration in a northeastern US temperate forest: a 22-year synthesis. Ecosphere 4, art140

[23] Gong, S.W., Zhang, T., Guo, J.X., 2019. Warming and Nitrogen Addition Change the Soil and Soil Microbial Biomass C:N:P Stoichiometry of a Meadow Steppe. International Journal of Environmental Research and Public Health 16, 2705

[24] Gruber, N., Galloway, J.N., 2008. An Earth-system perspective of the global nitrogen cycle. Nature 451, 293–296

[25] Guo, X., Gao, Q., Yuan, M., Wang, G., Zhou, X., Feng, J., Shi, Z., Hale, L., Wu, L., Zhou, A., Tian, R., Liu, F., Wu, B., Chen, L., Jung, C.G., Niu, S., Li, D., Xu, X., Jiang, L., Escalas, A., Wu, L., He, Z., Van Nostrand, J.D., Ning, D., Liu, X., Yang, Y., Schuur, E.A.G., Konstantinidis, K.T., Cole, J.R., Penton, C.R., Luo, Y., Tiedje, J.M., Zhou, J., 2020. Gene-informed decomposition model predicts lower soil carbon loss due to persistent microbial adaptation to warming. Nature Communications 11, 4897

[26] IPCC, 2018. Special Report on Global Warming of 1.5°C. Cambridge University Press, UK.

[27] Kalbitz, K., Schmerwitz, J., Schwesig, D., Matzner, E., 2003. Biodegradation of soil-derived dissolved organic matter as related to its properties. Geoderma 113, 273–291

[28] Liu, H., Yang, X., Liang, C., Li, Y., Qiao, L., Ai, Z., Xue, S., Liu, G., 2019. Interactive effects of microplastics and glyphosate on the dynamics of soil dissolved organic matter in a Chinese loess soil. Catena 182, 182

[29] Luo, C., Rodriguez-R, L.M., Johnston, E.R., Wu, L., Cheng, L., Xue, K., Tu, Q., Deng, Y., He, Z., Shi, J.Z., Yuan, M.M., Sherry, R.A., Li, D., Luo, Y., Schuur, E.A.G., Chain, P., Tiedje, J.M., Zhou, J., Konstantinidis, K.T., 2014. Soil Microbial Community Responses to a Decade of Warming as Revealed by Comparative Metagenomics. Applied and Environmental Microbiology 80, 1777–1786

[30] Machmuller, M.B., Mohan, J.E., Minucci, J.M., Phillips, C.A., Wurzburger, N., 2016. Season, but not experimental warming, affects the activity and temperature sensitivity of extracellular enzymes. Biogeochemistry 131, 255–265

[31] Majuakim, L., Kitayama, K., 2013. Influence of polyphenols on soil nitrogen mineralization through the formation of bound protein in tropical montane forests of Mount Kinabalu, Borneo. Soil Biology & Biochemistry 57, 14–21

[32] Manzoni, S., Schimel, J.P., Porporato, A., 2012. Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93, 930–938

[33] Meng, C., Tian, D., Zeng, H., Li, Z., Chen, H.Y.H., Niu, S., 2019. Global meta-analysis on the responses of soil extracellular enzyme activities to warming. Science of the Total Environment 705, 135992

[34] Moorhead, D.L., Rinkes, Z.L., Sinsabaugh, R.L., Weintraub, M.N., 2013. Dynamic relationships between microbial biomass, respiration, inorganic nutrients and enzyme activities: informing enzyme-based decomposition models. Frontiers in Microbiology 4, 4

[35] Moorhead, D.L., Sinsabaugh, R.L., Hill, B.H., Weintraub, M.N., 2016. Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biology & Biochemistry 93, 1–7

[36] Olsen, S.R., Sommers, L.E., 1982. Phosphorous. In: Page, A.L., Miller, R.H., Keeney, D.R. (Eds.), Methods of Soil Analysis, Part 2, Chemical and Microbial Properties. Agronomy Monograph, vol. 9. Agronomy Society of America, pp. 403e430 (Madison, Wisconsin).

[37] Peng, X., Wang, W., 2016. Stoichiometry of soil extracellular enzyme activity along a climatic transect in temperate grasslands of northern China. Soil Biology & Biochemistry 98, 74–84

[38] Romero-Olivares, A.L., Allison, S.D., Treseder, K.K., 2017. Soil microbes and their response to experimental warming over time: A meta-analysis of field studies. Soil Biology & Biochemistry 107, 32–40

[39] Romero-Olivares, A.L., Taylor, J.W., Treseder, K.K., 2015. Neurospora discreta as a model to assess adaptation of soil fungi to warming. BMC Evolutionary Biology 15, 15

[40] Rosinger, C., Rousk, J., Sanden, H., 2019. Can enzymatic stoichiometry be used to determine growth-limiting nutrients for microorganisms? - A critical assessment in two subtropical soils. Soil Biology & Biochemistry 128, 115–126

[41] Rui, Y., Wang, Y., Chen, C., Zhou, X., Wang, S., Xu, Z., Duan, J., Kang, X., Lu, S., Luo, C., 2012. Warming and grazing increase mineralization of organic P in an alpine meadow ecosystem of Qinghai-Tibet Plateau, China. Plant and Soil 357, 73–87

[42] Rustad, L.E., Campbell, J.L., Marion, G.M., Norby, R.J., Mitchell, M.J., Hartley, A.E., Cornelissen, J.H.C., Gurevitch, J., Gcte, N., 2001. A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126, 543–562

[43] Saiya-Cork, K.R., Sinsabaugh, R.L., Zak, D.R., 2002. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biology & Biochemistry 34, 1309–1315

[44] Schindlbacher, A., Schnecker, J., Takriti, M., Borken, W., Wanek, W., 2015. Microbial physiology and soil CO₂ efflux after 9 years of soil warming in a temperate forest—no indications for thermal adaptations. Global Change Biology 21, 4265–4277

[45] Sinsabaugh, R.L., Antibus, R.K., Linkins, A.E., McClaugherty, C.A., Rayburn, L., Repert, D., Weiland, T., 1993. Wood decomposition – nitrogen and phosphorus dynamics in relation to extracellular enzyme-activity. Ecology 74, 1586–1593

[46] Sinsabaugh, R.L., Belnap, J., Findlay, S.G., Shah, J.J.F., Hill, B.H., Kuehn, K.A., Kuske, C.R., Litvak, M.E., Martinez, N.G., Moorhead, D.L., Warnock, D.D., 2014. Extracellular enzyme kinetics scale with resource availability. Biogeochemistry 121, 287–304

[47] Sinsabaugh, R.L., Hill, B.H., Follstad Shah, J.J., 2009. Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462, 795–798

[48] Sinsabaugh, R.L., Lauber, C.L., Weintraub, M.N., Ahmed, B., Allison, S.D., Crenshaw, C., Contosta, A.R., Cusack, D., Frey, S., Gallo, M.E., Gartner, T.B., Hobbie, S.E., Holland, K., Keeler, B.L., Powers, J.S., Stursova, M., Takacs-Vesbach, C., Waldrop, M.P., Wallenstein, M.D., Zak, D.R., Zeglin, L.H., 2008. Stoichiometry of soil enzyme activity at global scale. Ecology Letters 11, 1252–1264

[49] Sinsabaugh, R.L., Moorhead, D.L., 1994. Resource-allocation to extracellular enzyme-production – a model for nitrogen and phosphorus control of litter decomposition. Soil Biology & Biochemistry 26, 1305–1311

[50] Sinsabaugh, R.L., Shah, J.J.F., 2011. Ecoenzymatic stoichiometry of recalcitrant organic matter decomposition: the growth rate hypothesis in reverse. Biogeochemistry 102, 31–43

[51] Sinsabaugh, R.L., Shah, J.J.F., 2012. Ecoenzymatic Stoichiometry and Ecological Theory. In: D.J. Futuyma (Ed.), Annual Review of Ecology, Evolution, and Systematics, Vol 43. Annual Review of Ecology Evolution and Systematics, pp. 313–343.

[52] Sinsabaugh, R.L., Shah, J.J.F., Hill, B.H., Elonen, C.M., 2012. Ecoenzymatic stoichiometry of stream sediments with comparison to terrestrial soils. Biogeochemistry 111, 455–467

[53] Steinweg, J.M., Dukes, J.S., Wallenstein, M.D., 2012. Modeling the effects of temperature and moisture on soil enzyme activity: Linking laboratory assays to continuous field data. Soil Biology & Biochemistry 55, 85–92

[54] Tapia-Torres, Y., Elser, J.J., Souza, V., García-Oliva, F., 2015. Ecoenzymatic stoichiometry at the extremes: How microbes cope in an ultra-oligotrophic desert soil. Soil Biology & Biochemistry 87, 34–42

[55] Theuerl, S., Buscot, F., 2010. Laccases: toward disentangling their diversity and functions in relation to soil organic matter cycling. Biology and Fertility of Soils 46, 215–225

[56] Tian, P., Razavi, B.S., Zhang, X., Wang, Q., Blagodatskaya, E., 2020. Microbial growth and enzyme kinetics in rhizosphere hotspots are modulated by soil organics and nutrient availability. Soil Biology & Biochemistry 141, 141

[57] Treseder, K.K., Marusenko, Y., Romero-Olivares, A.L., Maltz, M.R., 2016. Experimental warming alters potential function of the fungal community in boreal forest. Global Change Biology 22, 3395–3404

[58] Tucker, C.L., Bell, J., Pendall, E., Ogle, K., 2013. Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming? Global Change Biology 19, 252–263

[59] Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass C. Soil Biology & Biochemistry 19, 703–707

[60] Veres, Z., Kotroczo, Z., Fekete, I., Toth, J.A., Lajtha, K., Townsend, K., Tothmeresz, B., 2015. Soil extracellular enzyme activities are sensitive indicators of detrital inputs and carbon availability. Applied Soil Ecology 92, 18–23

[61] Wang, C., Wang, G., Wang, Y., Zi, H., Lerdau, M., Liu, W., 2017. Effects of long-term experimental warming on plant community properties and soil microbial community composition in an alpine meadow. Israel Journal of Ecology & Evolution 63, 85–96

[62] Wang, J., Wang, X., Liu, G., Wang, G., Wu, Y., Zhang, C., 2020. Fencing as an effective approach for restoration of alpine meadows: Evidence from nutrient limitation of soil microbes. Geoderma 363, 363

[63] Waring, B.G., Weintraub, S.R., Sinsabaugh, R.L., 2014. Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117, 101–113

[64] Wei, H., Guenet, B., Vicca, S., Nunan, N., AbdElgawad, H., Pouteau, V., Shen, W., Janssens, I.A., 2014. Thermal acclimation of organic matter decomposition in an artificial forest soil is related to shifts in microbial community structure. Soil Biology & Biochemistry 71, 1–12

[65] Wu, Y., Chen, W., Li, Q., Guo, Z., Li, Y., Zhao, Z., Zhai, J., Liu, G., Xue, S., 2021. Ecoenzymatic stoichiometry and nutrient limitation under a natural secondary succession of vegetation on the Loess Plateau, China. Land Degradation & Development 32, 399–409

[66] Xiao, W., Chen, X., Jing, X., Zhu, B., 2018. A meta-analysis of soil extracellular enzyme activities in response to global change. Soil Biology & Biochemistry 123, 21–32

[67] Xu, W., Yuan, W., 2017. Responses of microbial biomass carbon and nitrogen to experimental warming: A meta-analysis. Soil Biology & Biochemistry 115, 265–274

[68] Xue, S., Yang, X., Liu, G., Gai, L., Zhang, C., Ritsema, C.J., Geissen, V., 2017. Effects of elevated CO₂ and drought on the microbial biomass and enzymatic activities in the rhizospheres of two grass species in Chinese loess soil. Geoderma 286, 25–34

[69] Yu, P., Tang, X., Liu, S., Liu, W., Zhang, A., 2020. Short Term Effects of Revegetation on Labile Carbon and Available Nutrients of Sodic Soils in Northeast China. Land (Basel) 9, 10

[70] Zhang, B., Chen, S.Y., Zhang, J.F., He, X.Y., Liu, W.J., Zhao, Q., Zhao, L., Tian, C.J., 2015. Depth-related responses of soil microbial communities toexperimental warming in an alpine meadow on the Qinghai-Tibet Plateau. European Journal of Soil Science 66, 496–504

[71] Zhang, J., Ai, Z., Liang, C., Wang, G., Liu, G., Xue, S., 2019. How microbes cope with short-term N addition in a Pinus tabuliformis forest-ecological stoichiometry. Geoderma 337, 630–640

[72] Zheng, H.F., Liu, Y., Chen, Y.M., Zhang, J., Li, H.J., Wang, L.F., Chen, Q.M., 2020. Short-term warming shifts microbial nutrient limitation without changing the bacterial community structure in an alpine timberline of the eastern Tibetan Plateau. Geoderma 360, 360

[73] Zheng, W., Zhou, J.c., Lin, W.s., Zheng, Y., Li, C., Li, X.f., Ji, Y.h., Yang, Z.j., 2019. Effects of soil warming on soil microbial extracellular enzyme activities with different depths in a young Chinese fir (Cunninghamia lanceolata) plantation of subtropics. Chinese Journal of Applied Ecology 30, 832–840.

[74] Zhou, X., Chen, C., Wang, Y., Xu, Z., Han, H., Li, L., Wan, S., 2013. Warming and increased precipitation have differential effects on soil extracellular enzyme activities in a temperate grassland. Science of the Total Environment 444, 552–558

[75] Zi, H.B., Hu, L., Wang, C.T., Wang, G.X., Wu, P.F., Lerdau, M., Ade, L.J., 2018. Responses of soil bacterial community and enzyme activity to experimental warming of an alpine meadow. European Journal of Soil Science 69, 429–438

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