Abstract
Soil extracellular enzymes catalyze soil biochemical processes, and the geographical patterns of their activities and stoichiometry can reflect soil microbial functional dynamics. In previous research, latitudinal and longitudinal variations in soil extracellular enzyme activity (EEA) have been intensively investigated. However, its elevation patterns and depth variations (especially > 40 cm) received much less attention. Here, we measured potential activities of enzymes of carbon (C) (β-1,4-glucosidase), nitrogen (N) (β-1,4-N-acetylglucosaminidase; leucine aminopeptidase), and phosphorus (P) (acid phosphatase) up to 1 m soil depth along a vertical grassland belt in Xinjiang Uygur Autonomous Region, China. Soils were sampled from three elevation gradients (low, < 1000 m; mid, 1000–2000 m; high, 2000–3000 m) at five depths (0–10, 10–20, 20–40, 40–60, 60–100 cm). Soil EEA generally increased with elevation, while specific EEA normalized by microbial biomass C was lowest at mid-elevation. Both enzymatic C:N and C:P ratios were highest at mid-elevation. Soil EEA declined with depth but the extents varied with elevation. Depth variations in soil enzymatic stoichiometry also differed among three elevation gradients. Enzyme C:N and C:P ratios only decreased with soil depth at low elevation. From low to high elevation, enzyme N:P was highest at depths of 20–40 cm, 40–60 cm, and 0–10 cm, respectively. Key influential factors of soil EEA varied from low to high elevation. At low elevation, soil nutrient affected soil EEA indirectly through affecting microbial biomass. At mid-elevation, soil moisture influenced soil EEA directly and indirectly via pH. At high elevation, only soil pH impacted soil EEA directly.
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References
Allison SD, Jastrow JD (2006) Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biol Biochem 38:3245–3256
Allison SD, Gartner TB, Holland K, Weintraub M, Sinsabaugh RL (2007) Soil enzymes:linking proteomics and ecological process. Manual of environmental microbiology. ASM Press, Washington, DC, pp 704–711
Allison SD, Weintraub MN, Gartner TB, Waldrop MP (2011) Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function. In: Shukla GC, Varma A (eds) Soil Enzymology. Springer, Berlin Heidelberg, pp 229–243
Banerjee S, Bora S, Thrall PH, Richardson AE (2016) Soil C and N as causal factors of spatial variation in extracellular enzyme activity across grassland-woodland ecotones. Appl Soil Ecol 105:1–8
Bell TH, Klironomos JN, Henry HAL (2010) Seasonal responses of extracellular enzyme activity and microbial biomass to warming and nitrogen addition. Soil Sci Soc of Am J 74:820–828
Belnap J (2011) Biological phosphorus cycling in dryland regions. In: Bünemann EK, Oberson A, Frossard E (eds) Phosphorus in action. Springer, Berlin, pp 371–406
Bowles TM, Acosta-Martínez V, Calderón F, Jackson LE (2014) Soil enzyme activities, microbial communities, and carbon and nitrogen availability in organic agroecosystems across an intensively-managed agricultural landscape. Soil Biol Biochem 68:252–262
Brockett BFT, Prescott CE, Grayston SJ (2012) Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol Biochem 44:9–20
Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14:319–329
Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234
Cenini VL, Fornara DA, McMullan G, Ternan N, Carolan R, Crawley MJ, Clément JC, Lavorel S (2016) Linkages between extracellular enzyme activities and the carbon and nitrogen content of grassland soils. Soil Biol Biochem 96:198–206
Chang EH, Chen TH, Tian G, Chiu CY (2016) The effect of altitudinal gradient on soil microbial community activity and structure in moso bamboo plantations. Appl Soil Ecol 98:213–220
Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil:is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252
Cuesta F, Muriel P, Llambí LD, Halloy S, Aguirre N, Beck S, Carilla J, Meneses RI, Cuello S, Grau A, Gámez LE, Irazábal J, Jácome J, Jaramillo R, Ramírez L, Samaniego N, Suárez-Duque D, Thompson N, Tupayachi A, Viñas P, Yager K, Becerra MT, Pauli H, Gosling WD (2017) Latitudinal and altitudinal patterns of plant community diversity on mountain summits across the tropical Andes. Ecography 40:1–14
Curtin D, Beare MH, Qiu W, Chantigny MH (2015) Temperature dependence of organic matter solubility:influence of biodegradation during soil-water extraction. Soil Sci Soc of Am J 79:858–863
Dungait JAJ, Hopkins DW, Gregory AS, Whitmore AP (2012) Soil organic matter turnover is governed by accessibility not recalcitrance. Glob Chang Biol 18:1781–1796
García-Palacios P, Prieto I, Ourcival JM, Hättenschwiler S (2016) disentangling the litter quality and soil microbial contribution to leaf and fine root litter decomposition responses to reduced rainfall. Ecosystems 19:490–503
Garten CT Jr (2004) Potential net soil N mineralization and decomposition of glycine-13C in forest soils along an elevation gradient. Soil Biol Biochem 36:1491–1496
Garten CT Jr, Hanson PJ (2006) Measured forest soil C stocks and estimated turnover times along an elevation gradient. Geoderma 136:342–352
German DP, Marcelo KRB, Stone MM, Allison SD (2012) The Michaelis-Menten kinetics of soil extracellular enzymes in response to temperature:a cross-latitudinal study. Glob Change Biol 18:1468–1479
Gonzalez JM, Portillo MC, Piñeiro-Vidal M (2015) Latitude-dependent underestimation of microbial extracellular enzyme activity in soils. Int J Environ Sci Tech 12:2427–2434
Henry HAL (2012) Soil extracellular enzyme dynamics in a changing climate. Soil Biol Biochem 47:53–59
Heuck C, Weig A, Spohn M (2015) Soil microbial biomass C:N:P stoichiometry and microbial use of organic phosphorus. Soil Biol Biochem 85:119–129
Hofmann K, Lamprecht A, Pauli H, Illmer P (2016) Distribution of prokaryotic abundance and microbial nutrient cycling across a high-alpine altitudinal gradient in the austrian central alps is affected by vegetation, temperature, and soil nutrients. Microb Ecol 72:1–13
Jenkinson DS, Powlson DS (1976) The effects of biocidal treatments on metabolism in soil—V: A method for measuring soil biomass. Soil Biol Biochem 8:209–213
Jing X, Yang X, Ren F, Zhou H, Zhu B, He JS (2016) Neutral effect of nitrogen addition and negative effect of phosphorus addition on topsoil extracellular enzymatic activities in an alpine grassland ecosystem. Appl Soil Ecol 107:205–213
Jing X, Chen X, Tang M, Ding Z, Jiang L, Li P, Ma S, Tian D, Xu L, Zhu J, Ji C, Shen H, Zheng C, Fang J, Zhu B (2017) Nitrogen deposition has minor effect on soil extracellular enzyme activities in six Chinese forests. Sci Total Environ 607–608:806–815
Jobbágy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436
Joergensen RG, Mueller T (1996) The fumigation-extraction method to estimate soil microbial biomass:calibration of the kEN value. Soil Biol Biochem 28:33–37
Kumar M, Männistö MK, Elsas JD, Nissinen RM (2016) Plants impact structure and function of bacterial communities in Arctic soils. Plant Soil 399:319–332
Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microb 75:5111–5120
Liu HS, Li LH, Han XG, Huang JH, Sun JX, Wang HY (2006) Respiratory substrate availability plays a crucial role in the response of soil respiration to environmental factors. Appl Soil Ecol 32:284–292
Luo L, Meng H, Gu JD (2017) Microbial extracellular enzymes in biogeochemical cycling of ecosystems. J Environ Manage 197:539–549
Manzoni S, Schimel JP, Porporato A (2012) Responses of soil microbial communities to water stress:results from a meta-analysis. Ecology 93:930–938
Margesin R, Jud M, Tscherko D, Schinner F (2009) Microbial communities and activities in alpine and subalpine soils. FEMS Microbiol Ecol 67:208–218
Marx MC, Kandeler E, Wood M, Wermbter N, Jarvis SC (2005) Exploring the enzymatic landscape:distribution and kinetics of hydrolytic enzymes in soil particle-size fractions. Soil Biol Biochem 37:35–48
Peng X, Wang W (2016) Stoichiometry of soil extracellular enzyme activity along a climatic transect in temperate grasslands of northern China. Soil Biol Biochem 98:74–84
Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315
Schinner F (1982) Soil microbial activities and litter decomposition related to altitude. Plant Soil 65:87–94
Schortemeyer M, Hartwig UA, Hendrey GR, Sadowsky MJ (1996) Microbial community changes in the rhizospheres of white clover and perennial ryegrass exposed to free air carbon dioxide enrichment (FACE). Soil Biol Biochem 28:1717–1724
Siles JA, Cajthaml T, Minerbi S, Margesin R (2016) Effect of altitude and season on microbial activity, abundance and community structure in Alpine forest soils. FEMS Microbiol Ecol 92:fiw008
Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264
Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798
Sistla SA, Schimel JP (2013) Seasonal patterns of microbial extracellular enzyme activities in an arctic tundra soil: Identifying direct and indirect effects of long-term summer warming. Soil Biol Biochem 66:119–129
Sistla SA, Asao S, Schimel JP (2012) Detecting microbial N-limitation in tussock tundra soil:implications for arctic soil organic carbon cycling. Soil Biol Biochem 55:78–84
Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN, Tabatabai MA, Johnston CT, Sumner ME (1996) Methods of soil analysis part 3: chemical methods. Soil Science Society of America and American Society of Agronomy, Madison
Stark S, Eskelinen A, Männistö MK (2012) Regulation of microbial community composition and activity by soil nutrient availability, soil pH, and herbivory in the tundra. Ecosystems 15:18–33
Stark S, Männistö MK, Eskelinen A (2014) Nutrient availability and pH jointly constrain microbial extracellular enzyme activities in nutrient-poor tundra soils. Plant Soil 383:373–385
Steinweg JM, Dukes JS, Wallenstein MD (2012) Modeling the effects of temperature and moisture on soil enzyme activity: linking laboratory assays to continuous field data. Soil Biol Biochem 55:85–92
Steinweg JM, Dukes JS, Paul EA, Wallenstein MD (2013) Microbial responses to multi-factor climate change:effects on soil enzymes. Front Microbiol 4:146
Stone MM, Weiss MS, Goodale CL, Adams MB, Fernandez IJ, German DP, Allison SD (2012) Temperature sensitivity of soil enzyme kinetics under N- fertilization in two temperate forests. Glob Change Biol 18:1173–1184
Stone MM, DeForest JL, Plante AF (2014) Changes in extracellular enzyme activity and microbial community structure with soil depth at the Luquillo Critical Zone Observatory. Soil Biol Biochem 75:237–247
Trasar-Cepeda C, Leirós MC, Gil-Sotres F (2008) Hydrolytic enzyme activities in agricultural and forest soils. Some implications for their use as indicators of soil quality. Soil Biol Biochem 40:2146–2155
Turner BL (2010) Variation in pH optima of hydrolytic enzyme activities in tropical rain forest soils. Appl Environ Microb 76:6485–6493
Waring BG, Weintraub SR, Sinsabaugh RL (2014) Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117:101–113
Xu Z, Yu G, Zhang X, Ge J, He N, Wang Q, Wang D (2015) The variations in soil microbial communities, enzyme activities and their relationships with soil organic matter decomposition along the northern slope of Changbai Mountain. Appl Soil Ecol 86:19–29
Yang Y, Fang J, Ji C, Ma W, Su S, Tang Z (2010) Soil inorganic carbon stock in the Tibetan alpine grasslands. Glob Biogeochem Cy 24:GB4022
Acknowledgements
This research was supported by the Projects of the National Key Research and Development Program (Nos. 2016YFC0500701) and the National Natural Science Foundation of China (Nos. 31630009, 31670325, and 31621091). We thank two anonymous reviewers for giving constructive comments on this manuscript, and Jeremy Kamen, MSc, from Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.
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Zuo, Y., Li, J., Zeng, H. et al. Vertical pattern and its driving factors in soil extracellular enzyme activity and stoichiometry along mountain grassland belts. Biogeochemistry 141, 23–39 (2018). https://doi.org/10.1007/s10533-018-0499-x
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DOI: https://doi.org/10.1007/s10533-018-0499-x