Ecoenzymatic stoichiometry reveals increased phosphorus limitation of microbial metabolism in tropical forests along elevation gradients

Abstract

Tropical forests exert the largest influence on the global carbon (C) cycle and climate, and soil microorganisms play an essential role in the feedbacks of the global C cycle and climate. However, the issue of how nutrient limitation of microbial metabolism affects the soil C cycle and its responses to climate change in tropical forests remains poorly understood. Here, we investigated the elevational patterns of microbial metabolic limitations in typical tropical forests by studying ecoenzymatic stoichiometry along three elevation gradients (with an overall elevation range of 100−1400 m above sea level (a.s.l.)) in south China. Results showed that microbial metabolism in tropical forest soils was strongly limited by phosphorus (P) and increased with increasing elevation, suggesting that there was greater microbial P limitation where temperatures were lower. In contrast, microbialC limitation was relatively low and did not show a consistent elevational pattern. Temperature emerged as the most significant predictor of microbial metabolic limitations, showing a positive correlation with microbial C limitation but a negative correlation with microbial P limitation. Based on an investigation of three topical forest elevation gradients (< 1500 m a.s.l.), our findings predict that global warming may alleviate microbial P limitation while exacerbate microbial C limitation.

Graphical abstract

Keywords

extracellular enzyme activity / extracellular enzyme stoichiometry / microbial metabolic limitations / elevation gradients / tropical forests

Highlight

	● Soil microorganisms in tropical forests were strongly limited by P and increased with increasing elevation.
	● Microbial C limitation was relatively low and lacked a consistent elevational pattern in tropical forest soils.
	● Temperature emerged as the most significant predictor of microbial metabolic limitations, showing a positive correlation with microbial C limitation but a negative correlation with microbial P limitation.

References

[1] Bardgett, R.D., Freeman, C., Ostle, N.J., 2008. Microbial contributions to climate change through carbon cycle feedbacks. The ISME Journal2, 805–814.

[2] Bremner, J.M., Mulvaney, C.S., 1982. Nitrogen-total. In: Page, A.L., Miller, R.H., Keeney, D.R., eds. Methods of Soil Analysis. Madison: Agronomy Society of America, 595–624.

[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] Camenzind, T., Hättenschwiler, S., Treseder, K.K., Lehmann, A., Rillig, M.C., 2018. Nutrient limitation of soil microbial processes in tropical forests. Ecological Monographs88, 4–21.

[5] Cao, X.W., Shi, Z.M., Chen, J., Liu, S., Zhang, M.M., Chen, M., Xu, G.X., Wu, J.M., Xing, H.S., Li, F.F., 2022. Extracellular enzyme characteristics and microbial metabolic limitation in soil of subalpine forest ecosystems on the eastern Qinghai-Tibetan Plateau. Plant and Soil479, 337–353.

[6] Cleveland, C.C., Liptzin, D., 2007. C:N:P stoichiometry in soil: is there a "Redfield ratio" for the microbial biomass. Biogeochemistry85, 235–252.

[7] Cui, Y.X., Bing, H.J., Fang, L.C., Jiang, M., Shen, G.T., Yu, J.L., Wang, X., Zhu, H., Wu, Y.H., Zhang, X.C., 2019. Extracellular enzyme stoichiometry reveals the carbon and phosphorus limitations of microbial metabolisms in the rhizosphere and bulk soils in alpine ecosystems. Plant and Soil458, 7–20.

[8] Cui, Y.X., Peng, S.S., Delgado-Baquerizo, M., Rillig, M.C., Terrer, C., Zhu, B., Jing, X., Chen, J., Li, J.Q., Feng, J., He, Y., Fang, L.C., Moorhead, D.L., Sinsabaugh, R.L., Peñuelas, J., 2023. Microbial communities in terrestrial surface soils are not widely limited by carbon. Global Change Biology29, 4412–4429.

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

[10] 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.

[11] Du, E.Z., Terrer, C., Pellegrini, A.F.A., Ahlström, A., van Lissa, C.J., Zhao, X., Xia, N., Wu, X.H., Jackson, R.B., 2020. Global patterns of terrestrial nitrogen and phosphorus limitation. Nature Geoscience13, 221–226.

[12] He, Q.Q., Wu, Y.H., Bing, H.J., Zhou, J., Wang, J.P., 2020. Vegetation type rather than climate modulates the variation in soil enzyme activities and stoichiometry in subalpine forests in the eastern Tibetan Plateau. Geoderma374, 114424.

[13] He, X.J., Chu, C.J., Yang, Y.C., Shu, Z.F., Li, B.H., Hou, E.Q., 2021. Bedrock and climate jointly control the phosphorus status of subtropical forests along two elevational gradients. CATENA206, 105525.

[14] He, X.J., Hou, E.Q., Liu, Y., Wen, D.Z., 2016. Altitudinal patterns and controls of plant and soil nutrient concentrations and stoichiometry in subtropical China. Scientific Reports6, 24261.

[15] Hou, E.Q., Chen, C.R., Luo, Y.Q., Zhou, G.Y., Kuang, Y.W., Zhang, Y.G., Heenan, M., Lu, X.K., Wen, D.Z., 2018. Effects of climate on soil phosphorus cycle and availability in natural terrestrial ecosystems. Global Change Biology24, 3344–3356.

[16] Hou, E.Q., Luo, Y.Q., Kuang, Y.W., Chen, C.R., Lu, X.K., Jiang, L.F., Luo, X.Z., Wen, D.Z., 2020. Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems. Nature Communications11, 637.

[17] Huang, C.M., Gong, Z.T., 2000. Study on pedogenesis and development of mountain soils in Jianfengling mountain area. Mountain Research18, 193–200.

[18] Jansson, J.K., Taş, N., 2014. The microbial ecology of permafrost. Nature Reviews Microbiology12, 414–425.

[19] Kaspari, M., Powers, J.S., 2016. Biogeochemistry and geographical ecology: embracing all twenty-five elements required to build organisms. The American Naturalist188, S62–S73.

[20] Li, J.S., Wu, B.Y., Zhang, D.D., Cheng, X.L., 2023. Elevational variation in soil phosphorus pools and controlling factors in alpine areas of Southwest China. Geoderma431, 116361.

[21] Lie, Z.Y., Zhou, G.Y., Huang, W.J., Kadowaki, K., Tissue, D.T., Yan, J.H., Peñuelas, J., Sardans, J., Li, Y.L., Liu, S.Z., Chu, G.W., Meng, Z., He, X.H., Liu, J.X., 2022. Warming drives sustained plant phosphorus demand in a humid tropical forest. Global Change Biology28, 4085–4096.

[22] Lin, Y., Gross, A., Silver, W.L., 2022. Low redox decreases potential phosphorus limitation on soil biogeochemical cycling along a tropical rainfall gradient. Ecosystems25, 387–403.

[23] Lin, Y.T., Li, H.B., Huang, X.S., Wu, L.F., Zhu, N.J., Lin, Y.B., Liu, Z.F., Kuang, Y.W., 2018. Variation of diversity and biomass of woody plant along altitude of Lianhua Mountain in Huizhou of Guangdong Province and their correlation analyses. Journal of Plant Resources and Environment27, 42–52.

[24] Luo, T.S., Chen, D.X., Li, S.C., Li, Y.D., Chen, B.F., 2005. Resources evaluation on Lianhuashan-Baipenzhu nature reserve of Guangdong Province. Guangdong Forestry Science and Technology19, 7–12.

[25] McDaniel, M.D., Kaye, J.P., Kaye, M.W., 2013. Increased temperature and precipitation had limited effects on soil extracellular enzyme activities in a post-harvest forest. Soil Biology and Biochemistry56, 90–98.

[26] 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 Microbiology4, 223.

[27] 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 and Biochemistry93, 1–7.

[28] Mou, Z.J., Kuang, L.H., He, L.F., Zhang, J., Zhang, X.Y., Hui, D.F., Li, Y., Wu, W.J., Mei, Q.M., He, X.J., Kuang, Y.W., Wang, J., Wang, Y.Q., Lambers, H., Sardans, J., Peñuelas, J., Liu, Z.F., 2021. Climatic and edaphic controls over the elevational pattern of microbial necromass in subtropical forests. CATENA207, 105707.

[29] Nannipieri, P., Trasar-Cepeda, C., Dick, R.P., 2018. Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biology and Fertility of Soils54, 11–19.

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

[31] Nottingham, A.T., Turner, B.L., Whitaker, J., Ostle, N.J., McNamara, N.P., Bardgett, R.D., Salinas, N., Meir, P., 2015. Soil microbial nutrient constraints along a tropical forest elevation gradient: a belowground test of a biogeochemical paradigm. Biogeosciences Discussions12, 6489–6523.

[32] Olsen, S.R., Sommers, L.E., 1982. Phosphorus. In: Page, A.L., Miller, R.H., Keeny, D.R., eds. Methods of Soil Analysis. Madison: Agronomy Society of America, 403–430.

[33] Osburn, E.D., Aylward, F.O., Barrett, J.E., 2021. Historical land use has long-term effects on microbial community assembly processes in forest soils. ISME Communications1, 48.

[34] Osburn, E.D., McBride, S.G., Aylward, F.O., Badgley, B.D., Strahm, B.D., Knoepp, J.D., Barrett, J.E., 2019. Soil bacterial and fungal communities exhibit distinct long-term responses to disturbance in temperate forests. Frontiers in Microbiology10, 2872.

[35] Pan, Y.D., Birdsey, R.A., Fang, J.Y., Houghton, R., Kauppi, P.E., Kurz, W.A., Phillips, O.L., Shvidenko, A., Lewis, S.L., Canadell, J.G., Ciais, P., Jackson, R.B., Pacala, S.W., McGuire, A.D., Piao, S.L., Rautiainen, A., Sitch, S., Hayes, D., 2011. A large and persistent carbon sink in the world's forests. Science333, 988–993.

[36] Parham, J.A., Deng, S.P., 2000. Detection, quantification and characterization of β-glucosaminidase activity in soil. Soil Biology and Biochemistry32, 1183–1190.

[37] Pascual, J., Blanco, S., Ramos, J.L., van Dillewijn, P., 2018. Responses of bulk and rhizosphere soil microbial communities to thermoclimatic changes in a Mediterranean ecosystem. Soil Biology and Biochemistry118, 130–144.

[38] Reed, S.C., Townsend, A.R., Taylor, P.G., Cleveland, C.C., 2011. Phosphorus cycling in tropical forests growing on highly weathered soils. In: Bünemann, E., Oberson, A., Frossard, E., eds. Phosphorus in Action. Berlin, Heidelberg: Springer, 339–369.

[39] Ren, C.J., Zhang, W., Zhong, Z.K., Han, X.H., Yang, G.H., Feng, Y.Z., Ren, G.X., 2018. Differential responses of soil microbial biomass, diversity, and compositions to altitudinal gradients depend on plant and soil characteristics. Science of the Total Environment610–611, 750–758.

[40] Ren, C.J., Zhou, Z.H., Guo, Y.X., Yang, G.H., Zhao, F.Z., Wei, G.H., Han, X.H., Feng, L., Feng, Y.Z., Ren, G.X., 2021. Contrasting patterns of microbial community and enzyme activity between rhizosphere and bulk soil along an elevation gradient. CATENA196, 104921.

[41] Serna-Chavez, H.M., Fierer, N., Van Bodegom, P.M., 2013. Global drivers and patterns of microbial abundance in soil. Global Ecology and Biogeography22, 1162–1172.

[42] Siles, J.A., Cajthaml, T., Filipová, A., Minerbi, S., Margesin, R., 2017. Altitudinal, seasonal and interannual shifts in microbial communities and chemical composition of soil organic matter in Alpine forest soils. Soil Biology and Biochemistry112, 1–13.

[43] Sinsabaugh, R.L., Follstad Shah, J.J., 2012. Ecoenzymatic stoichiometry and ecological theory. Annual Review of Ecology, Evolution, and Systematics43, 313–343.

[44] Sinsabaugh, R.L., Hill, B.H., Follstad Shah, J.J., 2009. Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature462, 795–798.

[45] 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 Letters11, 1252–1264.

[46] Sundqvist, M.K., Sanders, N.J., Wardle, D.A., 2013. Community and ecosystem responses to elevational gradients: processes, mechanisms, and insights for global change. Annual Review of Ecology, Evolution, and Systematics44, 261–280.

[47] Tabatabai, M.A., 1994. Soil enzymes. In: Weaver, R.W., Angle, J.S., Bottomley, P.S., eds. Methods of Soil Analysis. Madison: Soil Science Society of America, 775–833.

[48] Tian, P., Razavi, B.S., Zhang, X.C., Wang, Q.K., Blagodatskaya, E., 2020. Microbial growth and enzyme kinetics in rhizosphere hotspots are modulated by soil organics and nutrient availability. Soil Biology and Biochemistry141, 107662.

[49] Truong, C., Gabbarini, L.A., Corrales, A., Mujic, A.B., Escobar, J.M., Moretto, A., Smith, M.E., 2019. Ectomycorrhizal fungi and soil enzymes exhibit contrasting patterns along elevation gradients in southern Patagonia. New Phytologist222, 1936–1950.

[50] Van Der Heijden, M.G.A., Bardgett, R.D., Van Straalen, N.M., 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters11, 296–310.

[51] Wang, L., Li, K., Guo, J.Y., Liu, X.M., Gao, J.H., Ma, L., Wei, J.H., Lu, M., Li, C.R., 2022. Extracellular enzyme stoichiometry reveals soil microbial carbon and phosphorus limitations in the Yimeng Mountain area, China. Forests13, 692.

[52] Yang, Y., Liang, C., Wang, Y.Q., Cheng, H., An, S.S., Chang, S.X., 2020. Soil extracellular enzyme stoichiometry reflects the shift from P- to N-limitation of microorganisms with grassland restoration. Soil Biology and Biochemistry149, 107928.

[53] Zhang, D.D., Wu, B.Y., Li, J.S., Cheng, X.L., 2023. Soil microbial relative resource limitation exhibited contrasting seasonal patterns along an elevational gradient in Yulong Snow Mountain. Functional Ecology37, 1328–1338.

[54] Zhang, S.H., Pan, Y., Zhou, Z.H., Deng, J., Zhao, F.Z., Guo, Y.X., Han, X.H., Yang, G.H., Feng, Y.Z., Ren, G.X., Ren, C.J., 2022. Resource limitation and modeled microbial metabolism along an elevation gradient. CATENA209, 105807.

[55] Zhao, F.Z., Ren, C.J., Han, X.H., Yang, G.H., Wang, J., Doughty, R., 2018. Changes of soil microbial and enzyme activities are linked to soil C, N and P stoichiometry in afforested ecosystems. Forest Ecology and Management427, 289–295.

[56] Zhou, J., Wu, Y.H., Bing, H.J., Yang, Z.J., Wang, J.P., Sun, H.Y., Sun, S.Q., Luo, J., 2016. Variations in soil phosphorus biogeochemistry across six vegetation types along an altitudinal gradient in SW China. CATENA142, 102–111.

[57] 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.

RIGHTS & PERMISSIONS

Higher Education Press