Distinct responses of soil carbon-degrading enzyme activities to warming in two alpine meadow ecosystems on the Qinghai-Tibet Plateau

Abstract

Soil extracellular enzymes play a central role in regulating soil organic carbon (SOC) dynamics. However, the effects of varying warming magnitudes and duration on permafrost soil carbon-degrading enzyme activities remain poorly understood. Here, we investigated warming effects on three representative carbon-degrading enzymes (β-1,4-glucosidase (BG), peroxidase (PER), phenol oxidase (POX)) in alpine and swamp meadows on the Qinghai-Tibet Plateau. The warming experiments were conducted using Open-top chambers at different warming magnitudes (+2.4 and +4.9 °C) and duration (3 and 6 years) in both meadows. The activity of BG increased with warming duration in alpine meadows regardless of the warming magnitude (69% and 45% for lower and higher warming treatments, respectively), although the effect was significant (p<0.05) only under 6-year warming. In contrast, warming did not significantly (p>0.05) alter BG activity in swamp meadows. Warming decreased POX activity in both alpine (62%) and swamp meadows (81%), but the effect was significant only under 6-year higher warming. Moreover, PER activity was not significantly influenced by warming in either meadow. Dissolved organic carbon and above-ground biomass were the primary factors influencing soil enzyme activities under warming in alpine meadow, while soil water content in swamp meadow. Noticeably, a negative correlation (p<0.05) was observed between SOC and oxidase/hydrolase activity in alpine meadow, suggesting the suppression of oxidase activity may benefit SOC storage under warming. Noticeably, a negative correlation (p<0.05) between SOC and oxidase/hydrolase activity was found in alpine meadow but not in swamp meadow, which was due to the difference in above-ground biomass. These findings highlight the need to consider the time-cumulative warming effects on plant growth and enzyme ratios in carbon models to improve the accuracy of model predicting of soil carbon dynamics in permafrost regions.

Graphical abstract

Keywords

soil extracellular enzyme / soil organic carbon / warming magnitude / warming duration / alpine meadows / swamp meadows

Highlight

	● Soil C-acquiring enzyme activities of alpine and swamp meadows were examined under warming.
	● BG activity increased with warming duration in alpine meadow but not in swamp meadows.
	● Warming tended to decrease POX activity in both alpine and swamp meadows.
	● SOC was negatively correlated with the ratio of oxidase to hydrolase activity in alpine meadows.

References

[1] Abbott, B.W., Jones, J.B., Schuur, E.A.G., Chapin Iii, F.S., Bowden, W.B., Bret-Harte, M.S., Epstein, H.E., Flannigan, M.D., Harms, T.K., Hollingsworth, T.N., Mack, M.C., Mcguire, A.D., Natali, S.M., Rocha, A.V., Tank, S.E., Turetsky, M.R., Vonk, J.E., Wickland, K.P., Aiken, G.R., Alexander, H.D., Amon, R.M.W., Benscoter, B.W., Bergeron, Y., Bishop, K., Blarquez, O., Ben Bond-lamberty, N., Breen, A.L., Buffam, I., Cai, Y.H., Carcaillet, C., Carey, S.K., Chen, J.M., Chen, H.Y.H., Christensen, T.R., Cooper, L.W., Cornelissen, J.H.C., De Groot, W.J., Deluca, T.H., Dorrepaal, E., Fetcher, N., Finlay, J.C., Forbes, B.C., French, N.H.F., Gauthier, S., Girardin, M.P., Goetz, S.J., Goldammer, J.G., Gough, L., Grogan, P., Guo, L.D., Higuera, P.E., Hinzman, L., Hu, F.S., Hugelius, G., Jafarov, E.E., Jandt, R., Johnstone, J.F., Jan Karlsson, N., Kasischke, E.S., Kattner, G., Kelly, R., Keuper, F., Kling, G.W., Kortelainen, P., Kouki, J., Kuhry, P., Laudon, H., Laurion, I., Macdonald, R.W., Mann, P.J., Martikainen, P.J., Mcclelland, J.W., Molau, U., Oberbauer, S.F., Olefeldt, D., Paré, D., Parisien, M.A., Payette, S., Peng, C.H., Pokrovsky, O.S., Rastetter, E.B., Raymond, P.A., Raynolds, M.K., Rein, G., Reynolds, J.F., Robards, M., Rogers, B.M., Schädel, C., Schaefer, K., Schmidt, I.K., Shvidenko, A., Sky, J., Spencer, R.G.M., Starr, G., Striegl, R.G., Teisserenc, R., Tranvik, L.J., Virtanen, T., Welker, J.M., Zimov, S., 2016. Biomass offsets little or none of permafrost carbon release from soils, streams, and wildfire: an expert assessment. Environmental Research Letters11, 034014.

[2] 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.

[3] Burns, R.G., DeForest, J.L., Marxsen, J., Sinsabaugh, R.L., Stromberger, M.E., Wallenstein, M.D., Weintraub, M.N., Zoppini, A., 2013. Soil enzymes in a changing environment: current knowledge and future directions. Soil Biology and Biochemistry58, 216–234.

[4] Chang, R.Y., Liu, S.G., Chen, L.Y., Li, N., Bing, H.J., Wang, T., Chen, X.P., Li, Y., Wang, G.X., 2021. Soil organic carbon becomes newer under warming at a permafrost site on the Tibetan Plateau. Soil Biology and Biochemistry152, 108074.

[5] Chen, H., Zhu, Q.A., Peng, C.H., Wu, N., Wang, Y.F., Fang, X.Q., Gao, Y.H., Zhu, D., Yang, G., Tian, J.Q., Kang, X.M., Piao, S., Ouyang, H., Xiang, W.H., Luo, Z.B., Jiang, H., Song, X.Z., Zhang, Y., Yu, G.R., Zhao, X.Q., Gong, P., Yao, T.D., Wu, J.H., 2013. The impacts of climate change and human activities on biogeochemical cycles on the Qinghai-Tibetan Plateau. Global Change Biology19, 2940–2955.

[6] Chen, J., Elsgaard, L., Van Groenigen, K.J., Olesen, J.E., Liang, Z., Jiang, Y., Lærke, P.E., Zhang, Y.F., Luo, Y.Q., Hungate, B.A., Sinsabaugh, R.L., Jørgensen, U., 2020. Soil carbon loss with warming: new evidence from carbon-degrading enzymes. Global Change Biology26, 1944–1952.

[7] Chen, J., Luo, Y.Q., García-Palacios, P., Cao, J.J., Dacal, M., Zhou, X.H., Li, J.W., Xia, J.Y., Niu, S.L., Yang, H.Y., Shelton, S., Guo, W., Van Groenigen, K.J., 2018a. Differential responses of carbon-degrading enzyme activities to warming: implications for soil respiration. Global Change Biology24, 4816–4826.

[8] Chen, J., Luo, Y., Van Groenigen, K. J., B.A ., Hungate, Cao, J., Zhou, X., Wang, R.W., 2018b. A keystone microbial enzyme for nitrogen control of soil carbon storage. Science Advances4, eaaq1689.

[9] Chen, J., Zhang, Y., Kuzyakov, Y., Wang, D., Olesen, J.E., 2023. Challenges in upscaling laboratory studies to ecosystems in soil microbiology research. Global Change Biology29, 569–574.

[10] Chen, X.P., Wang, G.X., Huang, K.W., Hu, Z.Y., Song, C.L., Liang, Y.M., Wang, J., Song, X.Y., Lin, S., 2017. The effect of nitrogen deposition rather than warming on carbon flux in alpine meadows depends on precipitation variations. Ecological Engineering107, 183–191.

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

[12] Ding, J.Z., Li, F., Yang, G.B., Chen, L.Y., Zhang, B.B., Liu, L., Fang, K., Qin, S.Q., Chen, Y.L., Peng, Y.F., Ji, C.J., He, H.L., Smith, P., Yang, Y.H., 2016. The permafrost carbon inventory on the Tibetan Plateau: a new evaluation using deep sediment cores. Global Change Biology22, 2688–2701.

[13] Fanin, N., Mooshammer, M., Sauvadet, M., Meng, C., Alvarez, G., Bernard, L., Bertrand, I., Blagodatskaya, E., Bon, L., Fontaine, S., Niu, S.L., Lashermes, G., Maxwell, T., Weintraub, M.N., Wingate, L., Moorhead, D., Nottingham, A.T., 2022. Soil enzymes in response to climate warming: mechanisms and feedbacks. Functional Ecology36, 1378–1395.

[14] Frostegård, Å., Bååth, E., Tunlio, A., 1993. Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biology and Biochemistry25, 723–730.

[15] Indorf, C., Dyckmans, J., Khan, K.S., Joergensen, R.G., 2011. Optimisation of amino sugar quantification by HPLC in soil and plant hydrolysates. Biology and Fertility of Soils47, 387–396.

[16] Jing, X., Wang, Y.H., Chung, H., Mi, Z.R., Wang, S.P., Zeng, H., He, J.S., 2014. No temperature acclimation of soil extracellular enzymes to experimental warming in an alpine grassland ecosystem on the Tibetan Plateau. Biogeochemistry117, 39–54.

[17] Joergensen, R.G., Mueller, T., 1996. The fumigation-extraction method to estimate soil microbial biomass: calibration of the kEN value. Soil Biology and Biochemistry28, 33–37.

[18] Kalbitz, K., Schmerwitz, J., Schwesig, D., Matzner, E., 2003. Biodegradation of soil-derived dissolved organic matter as related to its properties. Geoderma113, 273–291.

[19] Lai, J.S., Zou, Y., Zhang, J.L., Peres-Neto, P.R., 2022. Generalizing hierarchical and variation partitioning in multiple regression and canonical analyses using the rdacca. hp R package. Methods in Ecology and Evolution13, 782–788.

[20] Lei, T.Z., Si, G.C., Wang, J., Zhang, G.X., 2017. Microbial communities and associated enzyme activities in alpine wetlands with increasing altitude on the Tibetan Plateau. Wetlands37, 401–412.

[21] Li, G.L., Kim, S., Han, S.H., Chang, H.N., Du, D.L., Son, Y., 2018. Precipitation affects soil microbial and extracellular enzymatic responses to warming. Soil Biology and Biochemistry120, 212–221.

[22] Li, N., Wang, W.X., Yang, Y., Gao, Y.H., Liu, G.S., 2011. Plant production, and carbon and nitrogen source pools, are strongly intensified by experimental warming in alpine ecosystems in the Qinghai-Tibet Plateau. Soil Biology and Biochemistry43, 942–953.

[23] MacDougall, A.H., Avis, C.A., Weaver, A.J., 2012. Significant contribution to climate warming from the permafrost carbon feedback. Nature Geoscience5, 719–721.

[24] Marion, G.M., Henry, G.H.R., Freckman, D.W., Johnstone, J., Jones, G., Jones, M.H., Lévesque, E., Molau, U., Mølgaard, P., Parsons, A.N., Svoboda, J., Virginia, R.A., 1997. Open-top designs for manipulating field temperature in high-latitude ecosystems. Global Change Biology3, 20–32.

[25] Meng, C., Tian, D.S., Zeng, H., Li, Z.L., Chen, H.Y.H., Niu, S.L., 2020. Global meta-analysis on the responses of soil extracellular enzyme activities to warming. Science of the Total Environment705, 135992.

[26] Menon, R., Jackson, C.R., Holland, M.M., 2013. The influence of vegetation on microbial enzyme activity and bacterial community structure in freshwater constructed wetland sediments. Wetlands33, 365–378.

[27] Mishra, U., Hugelius, G., Shelef, E., Yang, Y.H., Strauss, J., Lupachev, A., Harden, J.W., Jastrow, J.D., Ping, C.L., Riley, W.J., Schuur, E.A.G., Matamala, R., Siewert, M., Nave, L.E., Koven, C.D., Fuchs, M., Palmtag, J., Kuhry, P., Treat, C.C., Zubrzycki, S., Hoffman, F.M., Elberling, B., Camill, P., Veremeeva, A., Orr, A., 2021. Spatial heterogeneity and environmental predictors of permafrost region soil organic carbon stocks. Science Advances7, eaaz5236.

[28] Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O'hara, R., Simpson, G. L., Solymos, 2019. P. Package ‘vegan’. Community ecology package, version 20192( 9), .

[29] 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 and Biochemistry34, 1309–1315.

[30] Schimel, J., 2003. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biology and Biochemistry35, 549–563.

[31] Schuur, E.A.G., McGuire, A.D., Schädel, C., Grosse, G., Harden, J.W., Hayes, D.J., Hugelius, G., Koven, C.D., Kuhry, P., Lawrence, D.M., Natali, S.M., Olefeldt, D., Romanovsky, V.E., Schaefer, K., Turetsky, M.R., Treat, C.C., Vonk, J.E., 2015. Climate change and the permafrost carbon feedback. Nature520, 171–179.

[32] Sinsabaugh, R.L., 2010. Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biology and Biochemistry42, 391–404.

[33] 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: stoichiometry of soil enzyme activity. Ecology Letters11, 1252–1264.

[34] Stroud, E., Craig, B.L.H., Henry, H.A.L., 2022. Short-term vs. long-term effects of warming and nitrogen addition on soil extracellular enzyme activity and litter decomposition in a grass-dominated system. Plant and Soil481, 165–177.

[35] Su, F.G., Duan, X.L., Chen, D.L., Hao, Z.C., Cuo, L., 2013. Evaluation of the global climate models in the CMIP5 over the Tibetan Plateau. Journal of Climate26, 3187–3208.

[36] Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. Microbial biomass measurements in forest soils: determination of k_C values and tests of hypotheses to explain the failure of the chloroform fumigation-incubation method in acid soils. Soil Biology and Biochemistry19, 689–696.

[37] Verbrigghe, N., Meeran, K., Bahn, M., Canarini, A., Fransen, E., Fuchslueger, L., Ingrisch, J., Janssens, I.A., Richter, A., Sigurdsson, B.D., Soong, J.L., Vicca, S., 2022. Long-term warming reduced microbial biomass but increased recent plant-derived C in microbes of a subarctic grassland. Soil Biology and Biochemistry167, 108590.

[38] Wang, J.L., Zhou, M.J., Hu, H.B., Kuai, J., Wang, X., Chu, L., 2023. Effects of soil warming on soil microbial metabolism limitation in a Quercus acutissima forest in north subtropical China. Forests14, 19.

[39] Wang, T., Tian, Z.M., Tunlid, A., Persson, P., 2020. Nitrogen acquisition from mineral-associated proteins by an ectomycorrhizal fungus. New Phytologist228, 697–711.

[40] Willers, C., Jansen Van Rensburg, P.J., Claassens, S., 2015. Phospholipid fatty acid profiling of microbial communities–a review of interpretations and recent applications. Journal of Applied Microbiology119, 1207–1218.

[41] Wu, Q.B., Zhang, T.J., 2010. Changes in active layer thickness over the Qinghai-Tibetan Plateau from 1995 to 2007. Journal of Geophysical Research: Atmospheres115, D09107.

[42] Xiao, W., Chen, X., Jing, X., Zhu, B., 2018. A meta-analysis of soil extracellular enzyme activities in response to global change. Soil Biology and Biochemistry123, 21–32.

[43] Xu, H.W., Huang, L.L., Chen, J., Zhou, H.L., Wan, Y., Qu, Q., Wang, M.G., Xue, S., 2023. Changes in soil microbial activity and their linkages with soil carbon under global warming. CATENA232, 107419.

[44] Xue, K., Yuan, M.M., Shi, J.Z., Qin, Y.J., Deng, Y., Cheng, L., Wu, L.Y., He, Z.L., Van Nostrand, J.D., Bracho, R., Natali, S., Schuur, E.A.G., Luo, C.W., Konstantinidis, K.T., Wang, Q., Cole, J., Tiedje, J., Luo, Y.Q., Zhou, J.Z., 2016. Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming. Nature Climate Change6, 595–600.

[45] Yakushev, A.V., Kuznetsova, I.N., Blagodatskaya, E.V., Blagodatsky, S.A., 2014. Temperature dependence of the activity of polyphenol peroxidases and polyphenol oxidases in modern and buried soils. Eurasian Soil Science47, 459–465.

[46] Yan, Z.Q., Li, Y., Wu, H.D., Zhang, K.R., Hao, Y.B., Wang, J.Z., Zhang, X.D., Yan, L., Kang, X.M., 2020. Different responses of soil hydrolases and oxidases to extreme drought in an alpine peatland on the Qinghai-Tibet Plateau, China. European Journal of Soil Biology99, 103195.

[47] Yuan, X., Chen, Y., Qin, W.K., Xu, T.L., Mao, Y.H., Wang, Q., Chen, K.L., Zhu, B., 2021. Plant and microbial regulations of soil carbon dynamics under warming in two alpine swamp meadow ecosystems on the Tibetan Plateau. Science of the Total Environment790, 148072.

[48] Zhang, T., Wang, G.X., Yang, Y., Mao, T.X., Chen, X.P., 2017. Grassland types and season-dependent response of ecosystem respiration to experimental warming in a permafrost region in the Tibetan Plateau. Agricultural and Forest Meteorology247, 271–279.

[49] Zhang, Y., Chen, J., Cheng, X.L., 2023. Revisiting the relationships between soil nitrous oxide emissions and microbial functional gene abundances. Global Change Biology29, 4697–4699.

[50] Zhou, J.Z., Xue, K., Xie, J.P., Deng, Y., Wu, L.Y., Cheng, X.L., Fei, S.F., Deng, S.P., He, Z.L., Van Nostrand, J.D., Luo, Y.Q., 2012. Microbial mediation of carbon-cycle feedbacks to climate warming. Nature Climate Change2, 106–110.

[51] Zuccarini, P., Asensio, D., Ogaya, R., Sardans, J., Peñuelas, J., 2020. Effects of seasonal and decadal warming on soil enzymatic activity in a P-deficient Mediterranean shrubland. Global Change Biology26, 3698–3714.

RIGHTS & PERMISSIONS

Higher Education Press