Season-dependence of soil extracellular enzyme activities in a Pinus koraiensis forest on Changbai Mountain

Abstract

Changbai Mountain, central in the distribution of Pinus koraiensis, supports a virgin Korean pine forest with vertical gradient distribution. Soil extracellular enzyme activity (EEA) and enzyme stoichiometry (ES) are reliable indicators of the energy and nutrients utilized by microbial communities and of soil nutrient changes. We measured four representative soil EEAs (sucrase, cellulase, urease, acid phosphatase) at two soil layers (A: 0–5 cm and B: 5–10 cm) beneath Korean pine forest at five elevations on Changbai Mountain during growing season. The vertical and seasonal variations of EEAs were analyzed by soil enzyme stoichiometry to quantify the role of soil microorganism in the nutrient cycling process. The activities of four soil extracellular enzymes and the ratios of enzyme activity to soil microbial biomass carbon (EA/ SMBC) did not vary with elevation. The first partition point of multiple regression trees was in September, and the second branch was split by elevation. Seasonal change had more influence on soil enzyme activity (A layer: 75.6%; B layer: 71.3%) than did change in elevation (A layer: 7.8%; B layer: 7.5%). Over one entire growing season, both vector length and vector angle were unchanged by elevation, but varied significantly by month. Among the soil physicochemical factors, available phosphorus and pH were the main factors affecting the four soil EEAs. The ratio of basal area of the coniferous tree to broad-leaved tree species (S_con/S_br), soil microbial biomass carbon (MBC) and nitrogen (MBN) influenced the four soil EEAs. The results of vector analysis revealed that C and N sources were generally sufficient, but P was limiting (vector angle > 45°). The vector angle for September was significantly higher than for other months. This result verified that phosphorus was the limiting factor affecting soil microorganism function in nutrient metabolism and cycling. Soil enzyme stoichiometry proved to be an efficient index for quantifying soil microorganism-mediated nutrient cycling in the Korean pine ecosystem.

Keywords

Korean pine forest / Soil extracellular enzyme / Enzyme stoichiometry / Seasonality / Elevation

References

[1] Ali RS, Ingwcersen J, Demyan MS, Funkuin YN, Wizemann HD, Kandeler E, Poll C. Modelling in situ activities of enzymes as a tool to explain seasonal variation of soil respiration from agro-ecosystems. Soil Biol Biochem, 2015, 81: 291-303.

[2] Baldrian P, Šnajdr J, Merhautová V, Dobiášová P, Cajthaml T, Valášková V. Responses of the extracellular enzyme activities in hardwood forest to soil temperature and seasonality and the potential effects of climate change. Soil Biol Biochem, 2013, 56: 60-68.

[3] Boeddinghaus RS, Nunan N, Berner D, Marhan S, Kandeler E. Do general spatial relationships for microbial biomass and soil enzyme activities exist in temperate grassland soils?. Soil Biol Biochem, 2015, 88: 430-440.

[4] Chen H, Luo P, Wen L, Yang LQ, Wang KL, Li DJ. Determinants of soil extracellular enzyme activity in a karst region, southwest China. Eur J Soil Biol, 2017, 80: 69-76.

[5] Chen H, Li DJ, Xiao KC, Wang KL. Soil microbial processes and resource limitation in karst and non-karst forests. Funct Ecol, 2018, 32: 1400-1409.

[6] Cui YX, Fang LC, Guo XB, Wang X, Zhang YJ, Li PF, Zhang XC. Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern loess plateau, China. Soil Biol Biochem, 2018, 116: 11-21.

[7] Das C, Mondal NK. Temporal and vertical variation of selected extracellular enzyme activities on tree litter degradation of a subtropical forest. Agric Res, 2019, 8: 84-91.

[8] Dong CC, Wang W, Liu HY, Xu XT, Zeng H. Temperate grassland shifted from nitrogen to phosphorus limitation induced by degradation and nitrogen deposition: evidence from soil extracellular enzyme stoichiometry. Ecolo Indic, 2019, 101: 453-464.

[9] Evans LS, Harnett J, Kahn-Jetter Z. Procedures to determine the amount of plant cover/basal area in field plots. Environ Exp Bot, 2006, 58(1): 180-187.

[10] Fan YC, Wang PC, Xiao WF, Zeng LX, Huang ZL, Lei JP. Seasonal dynamics of soil enzymes and its relationship with nutrients for two forests in Three Gorges Reservoir Area. J Huazhong Agri Univ-China, 2014, 33(4): 39-44.

[11] Ge Y, He JZ, Zhu YG, Zhang JB, Xu ZH, Zhang LM, Zheng YM. Differences in soil bacterial diversity: driven by contemporary disturbances or historical contingencies?. ISME J, 2008, 2(3): 254-264.

[12] Ge XG, Xiao WF, Zeng LX, Huang ZL, Huang LL, Tan BW. Relationships between soil nutrient contents and soil enzyme activities in Pinus massoniana stands with different ages in Three Gorges Reservoir Area. Chin J Appl Ecol, 2012, 23(2): 445-451.

[13] Ginrich SF. Measuring and evaluating stocking and stand density in upland hardwood forests in the central states. For Sci, 1967, 13(1): 38-53.

[14] Grandy AS, Neff JC, Weintraub MN. Carbon structure and enzyme activities in alpine and forest ecosystems. Soil Biol Biochem, 2007, 39(11): 2701-2711.

[15] Guan SY (1986) Soil enzyme and its research method. Beijing Agriculture Press, Beijin, China, pp 260–339 (in Chinese).

[16] Hendriksena NB, Creamerb RE, Stone D, Winding A. Soil exo-enzyme activities across Europe-the influence of climate, land-use and soil properties. Appl Soil Ecol, 2016, 97: 44-48.

[17] Henry HAL. Soil extracellular enzyme dynamics in a changing climate. Soil Biol Biochem, 2012, 47: 53-59.

[18] Husson F, Pagès J, Lê S. Exploratory Multivariate Analysis by Example Using R, 2014, Boca Raton, USA: CRC Press.

[19] Jian S, Li J, Ji C, Wang G, Mayes MA, Dzantor KE, Hui D, Luo YJ. Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: a meta-analysis. Soil Biol Biochem, 2016, 101: 32-43.

[20] Jiang YF, Yin XQ, Wang FB. Impact of soil mesofauna on the decomposition of two main species litters in a Pinus koraiensis mixed broad-leaved forest of the Changbai Mountains. Acta Ecol Sinica, 2014, 34(2): 110-115.

[21] Li GQ, Bau F, Sang WG. Different responses of radial growth to climate warming in Pinus koraiensis and Picea jezoensis var. komarovii at their upper elevational limits in Changbai Mountain. China Chin J Plant Ecol, 2011, 35: 500-511.

[22] Li W, Yu LJ, Li T, Xiang J, Wu G. Seasonal and spatial dynamics of soil enzyme activities and its relationship to soil fertility in Karst ecosystem−a case study of Guilin Yaji Karst Experimental Site. J Agro-Environ Sci, 2008, 27(1): 260-0266.

[23] Loeppmann S, Semenov M, Blagodatskaya E, Kuzyakov Y. Substrate quality affects microbial-and enzyme activities in rooted soil. J Plant Nutr Soil Sc, 2016, 179(1): 39-47.

[24] Lu RK. Analytical methods for soil and agro-chemistry, 2000, Beijing, China: China Agricultural Science and Technology Press 12 111

[25] Lucas RW, Casper BB, Jackson JK, Balser TC. Soil microbial communities and extracellular enzyme activity in the New Jersey Pinelands. Soil Biol Biochem, 2007, 39(10): 2508-2519.

[26] Lyu S, Wang X, Zhang Y, li Z,. Different responses of Korean pine (Pinus koraiensis) and Mongolia oak (Quercus mongolica) growth to recent climate warming in northeast China. Dendrochronologia, 2017, 45: 113-122.

[27] Medeiros EVD, Duda GP, Junior MAL, Hammecker C. Seasonal effect of land use type on soil absolute and specific enzyme activities in a Brazilian semi-arid region. CATENA, 2018, 172(1): 397-407.

[28] Moorhead DL, Rinkes ZL, Sinsabaugh RL, Weintraub MN. Dynamic relationships between microbial biomass, respiration, inorganic nutrients and enzyme activities: informing enzyme-based decomposition models. Fron Microbiol, 2013, 4(226): 1-12.

[29] Moorhead DL, Sinsabaugh RL, Brain HH, Weintraub MN. Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biol Biochem, 2016, 93: 1-7.

[30] Pathan SI, Žifčáková L, Ceccherini MT, Pantani OL, Větrovský T, Baldrian P. Seasonal variation and distribution of total and active microbial community of β-glucosidase encoding genes in coniferous forest soil. Soil Biol Biochem, 2017, 105: 71-80.

[31] Peng XQ, Wang W. Stoichiometry of soil extracellular enzyme activity along a climatic transect in temperate grasslands of northern China. Soil Biol Biochem, 2016, 98: 74-84.

[32] Pietikäinen J, Tikka PJ, Valkonen S, Isomäki A, Fritze H. Is the soil microbial community related to the basal area of trees in a Scots pine stand?. Soil Biol Biochem, 2007, 39: 1832-1834.

[33] Ping Y, Han DX, Wang N, Hu YB, Mu LQ, Feng FJ. Vertical zonation of soil fungal community structure in a korean pine forest on Changbai Mountain. China World J Microb Bio, 2017 33 1 12

[34] Rastin N, Rosenplänter K, Hüttermann A. Seasonal variation of enzyme activity and their dependence on certain soil factors in a beech forest soil. Soil Biol Biochem, 1988, 20: 637-642.

[35] Saetre P. Spatial patterns of ground vegetation, soil microbial biomass and activity in a mixed spruce-birch stand. Ecography, 2010, 22(2): 183-192.

[36] Saetre P, Bååth E. Spatial variation and patterns of soil microbial community structure in a mixed spruce–birch stand. Soil Biol Biochem, 2000, 32: 909-917.

[37] Salazar S, Sánchez LE, Alvarez J, Valverde A, Galindo P, Igual JM, Peix A, Santa-Regina I. Correlation among soil enzyme activities under different forest system management practices. Ecol Eng, 2011, 37(8): 1123-1131.

[38] Siles JA, Cajthaml T, Filipová A, Minerbi S, Margesin R. Altitudinal, seasonal and interannual shifts in microbial communities and chemical composition of soil organic matter in alpine forest soils. Soil Biol Biochem, 2017, 112: 1-13.

[39] Sinsabaugh RL, Hill BH, Shah JJF. Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature, 2009, 462: 795-798.

[40] Sinsabaugh RL, Shah JJF. Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol Syst, 2012, 43: 313-342.

[41] Šnajdr J, Valášková V, Merhautová VR, Herinková J, Cajthaml T, Baldrian P. Spatial variability of enzyme activities and microbial biomass in the upper layers of Quercus petraea forest soil. Soil Biol Biochem, 2008, 40: 2068-2075.

[42] Stone MM, DeForest JL, Plante AF. Changes in extracellular enzyme activity and microbial community structure with soil depth at the Luquillo Critical Zone Observatory. Soil Biol Biochem, 2014, 75: 237-247.

[43] Tabatabai MA, Bremner JM. Assay of urease activity in soils. Soil Biol Biochem, 1972, 4: 479-487.

[44] Uksa M, Schloter M, Kautz T, Athmann M, Köpke U, Fischer D. Spatial variability of hydrolytic and oxidative potential enzyme activities in different subsoil compartments. Biol Fert Soils, 2015, 51(4): 517-521.

[45] Vance ED, Brookes PC, Jenkinson DS. An extraction method for measuring soil microbial biomass C. Soil Biol Biochem, 1987, 19: 703-707.

[46] Veres Z, Kotroczó Z, Fekete I, Tóth JA, Lajtha K, Townsend K, Tóthmérész B. Soil extracellular enzyme activities are sensitive indicators of detrital inputs and carbon availability. Appl Soil Ecol, 2015, 92: 18-23.

[47] Vitousek PM, Porder S, Houlton BZ, Chadwick OA. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl, 2010, 20: 5-15.

[48] Wang CY, Lü YN, Lei W, Liu XY, Tian XJ. Insights into seasonal variation of litter decomposition and related soil degradative enzyme activities in subtropical forest in China. J Forestry Res, 2013, 24(4): 683-689.

[49] Wang N, Wang MJ, Li SL, Wang NN, Feng FJ, Han SJ. Effects of precipitation variation on growing seasonal dynamics of soil microbial biomass in broadleaved Korean pine mixed forest. Chin J Appl Ecol, 2015, 26(5): 1297-1305.

[50] Waring BG, Weintraub SR, Sinsabaugh RL. Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry, 2014, 117: 101-113.

[51] Xun W, Huang T, Zhao J, Ran W, Wang BR, Shen QR, Zhang RF. Environmental conditions rather than microbial inoculum composition determine the bacterial composition, microbial biomass and enzymatic activity of reconstructed soil microbial communities. Soil Biol Biochem, 2015, 90: 10-18.

[52] Zhang MM, Wang N, Zhang JY, Hu YB, Cai DJ, Guo JH, Wu D, Sun GY. Soil physicochemical properties and the rhizosphere soil fungal community in a mulberry (Morus alba L.)/Alfalfa (Medicago sativa L.) intercropping system. Forests, 2019 10 2 167

[53] Zhao SQ, Fang JY, Zong ZJ, Zhu B, Shen HH. Composition, structure and species diversity of plant communities along an altitudinal gradient on the northern slope of Mt. Changbai. Northeast China Biodivers Sci, 2004, 12: 164-173.