Responses of soil extracellular enzyme activities to carbon input alteration and warming in a subtropical evergreen broad-leaved forest

doi:10.17521/cjpe.2020.0310

Abstract

Abstract:

Aims The objective was to investigate the responses of soil extracellular enzyme activities to carbon input alteration and warming in a subtropical evergreen broad-leaved forest of Ailao Mountain, Yunnan, southwest China.
Methods This study was based on two soil depths (0-5 and 5-10 cm) for four treatments under a long-term soil warming experiment in a subtropical evergreen broad-leaved forest of Ailao Mountain, Yunnan, southwest China. Potential activities of β-glucosidase (BG), polyphenol oxidase (POX), peroxidase (PER), β-1,4-N-acetylglucosaminidase (NAG) and acid phosphatase (AP) and their stoichiometric ratios were measured. Soil physical and chemical properties were also analyzed.
Important findings The results showed that in the control treatment, activities of all enzymes except POX decreased significantly with soil depth. Compared with the control treatment, long-term litter removal significantly reduced AP and BG activities at 0-5 cm soil depth, but had no significant effect on NAG, PER and POX activities at both 0-5 and 5-10 cm soil depths. Long-term root removal significantly reduced BG activity at 0-5 cm soil depth, while increased PER activity at both soil depths. Long-term root removal and warming treatment significantly reduced AP and BG activities at 0-5 cm soil depth, but had no significant effect on activities of other enzymes at both soil depths. The results of redundancy analysis showed that soil water content and NH₄⁺-N content were likely important factors driving the changes soil enzyme activities among treatments. This research provides critical information on the activities of soil enzymes related to carbon, nitrogen and phosphorus cycling in response to global change in this subtropical forest ecosystem.

Key words: soil extracellular enzyme activity, ecological stoichiometry, litter removal, root removal, warming

LIU Shan-Shan, ZHOU Wen-Jun, KUANG Lu-Hui, LIU Zhan-Feng, SONG Qing-Hai, LIU Yun- Tong, ZHANG Yi-Ping, LU Zhi-Yun, SHA Li-Qing. Responses of soil extracellular enzyme activities to carbon input alteration and warming in a subtropical evergreen broad-leaved forest[J]. Chin J Plant Ecol, 2020, 44(12): 1262-1272.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2020.0310

https://www.plant-ecology.com/EN/Y2020/V44/I12/1262

Figures/Tables 7

References 59

[1]	Allison SD, Vitousek PM (2004). Extracellular enzyme activities and carbon chemistry as drivers of tropical plant litter decomposition. Biotropica, 36, 285-296.
[2]	Allison SD, Weintraub MN, Gartner TB, Waldrop MP (2010). Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function//Shukla G, Varma A. Soil Enzymology. Springer-Verlag, Berlin. 229-243.
[3]	Baldrian P (2009). Ectomycorrhizal fungi and their enzymes in soils: Is there enough evidence for their role as facultative soil saprotrophs? Oecologia, 161, 657-660. URL PMID
[4]	Brzostek ER, Greco A, Drake JE, Finzi AC (2013). Root carbon inputs to the rhizosphere stimulate extracellular enzyme activity and increase nitrogen availability in temperate forest soils. Biogeochemistry, 115, 65-76.
[5]	Chaer GM, Myrold DD, Bottomley PJ (2009). A soil quality index based on the equilibrium between soil organic matter and biochemical properties of undisturbed coniferous forest soils of the Pacific Northwest. Soil Biology & Biochemistry, 41, 822-830.
[6]	Chen J, Elsgaard L, van Groenigen KJ, Olesen JE, Liang Z, Jiang Y, Laerke PE, Zhang YF, Luo YQ, Hungate BA, Sinsabaugh RL, Jørgensen U (2020). Soil carbon loss with warming: new evidence from carbon-degrading enzymes. Global Change Biology, 26, 1944-1952.
[7]	Cleveland CC, Liptzin D (2007). C:N:P stoichiometry in soil: Is there a “Redfield ratio” for the microbial biomass? Biogeochemistry, 85, 235-252.
[8]	Crow SE, Lajtha K, Filley TR, Swanston CW, Bowden RD, Caldwell BA (2009). Sources of plant-derived carbon and stability of organic matter in soil: implications for global change. Global Change Biology, 15, 2003-2019.
[9]	Fekete I, Kotroczó Z, Varga C, Nagy PT, Várbíró G, Bowden RD, Tóth JA, Lajtha K (2014). Alterations in forest detritus inputs influence soil carbon concentration and soil respiration in a Central-European deciduous forest. Soil Biology & Biochemistry, 74, 106-114.
[10]	Ge XG, Xiao WF, Zeng LX, Huang ZL, Zhou BZ, Schaub M, Li MH (2017). Relationships between soil-litter interface enzyme activities and decomposition in Pinus massoniana plantations in China. Journal of Soils and Sediments, 17, 996-1008.
[11]	Gianfreda L (2015). Enzymes of importance to rhizosphere processes. Journal of Soil Science and Plant Nutrition, 15, 283-306.
[12]	Harrington RA, Fownes JH, Vitousek PM (2001). Production and resource use efficiencies in N- and P-limited tropical forests: a comparison of responses to long-term fertilization. Ecosystems, 4, 646-657.
[13]	Hill BH, Elonen CM, Jicha TM, Kolka RK, Lehto LLP, Sebestyen SD, Seifert-Monson LR (2014). Ecoenzymatic stoichiometry and microbial processing of organic matter in northern bogs and fens reveals a common P-limitation between peatland types. Biogeochemistry, 120, 203-224.
[14]	Hu R, Wang XP, Xu JS, Zhang YF, Pan YX, Su X (2020). Themechanism of soil nitrogen transformation under different biocrusts to warming and reduced precipitation: from microbial functional genes to enzyme activity. Science of the Total Environment, 722, 137849. DOI: 10.1016/j.scitotenv. 2020.137849.
[15]	IPCC (2013). Climate Change 2013: the Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge.
[16]	Jiang MH, Ni MY, Zhou JC, Chen YM, Yang YS (2018). Effects of warming and precipitation reduction on soil enzyme activity in a young Cunning-hamia lanceolata plantation. Chinese Journal of Ecology, 37, 3210-3219.
	[ 江淼华, 倪梦颖, 周嘉聪, 陈岳民, 杨玉盛 (2018). 增温和降雨减少对杉木幼林土壤酶活性的影响. 生态学杂志, 37, 3210-3219.]
[17]	Jones DL, Willett VB (2006). Experimental evaluation of methods to quantify Dissolved organic nitrogen (DON) and Dissolved organic carbon (DOC) in soil. Soil Biology & Biochemistry, 38, 991-999.
[18]	Kang H, Lee D (2005). Inhibition of extracellular enzyme activities in a forest soil by additions of inorganic nitrogen. Communications in Soil Science and Plant Analysis, 36, 2129-2135.
[19]	Karhu K, Auffret MD, Dungait JAJ, Hopkins DW, Prosser JI, Singh BK, Subke JA, Wookey PA, Agren GI, Sebastià MT, Gouriveau F, Bergkvist G, Meir P, Nottingham AT, Salinas N, Hartley IP (2014). Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature, 513, 81-84. URL PMID
[20]	Li GL, Kim S, Han SH, Chang HN, Du DL, Son Y (2018). Precipitation affects soil microbial and extracellular enzymatic responses to warming. Soil Biology & Biochemistry, 120, 212-221.
[21]	Lu M, Zhou XH, Yang Q, Li H, Lou YQ, Fang CM, Chen JK, Yang X, Li B (2013). Responses of ecosystem carbon cycle to experimental warming: a meta-analysis. Ecology, 94, 726-738. URL PMID
[22]	Lu ZY (2016). Effects of Increasing Temperature and Root Cutting on Soil Nitrogen Mineralization in Evergreen Broad-leaved Forest of Ailao Mountain. Master degree dissertation, University of Chinese Academy of Sciences, Beijing.
	[ 鲁志云 (2016). 增温和切根对哀牢山常绿阔叶林土壤氮矿化的影响. 硕士学位论文, 中国科学院大学, 北京.]
[23]	Luo YQ, Sherry R, Zhou XH, Wan SQ (2009). Terrestrial carbon- cycle feedback to climate warming: experimental evidence on plant regulation and impacts of biofuel feedstock harvest. Global Change Biology: Bioenergy, 1, 62-74.
[24]	Martens DA, Johanson JB, Frankenberger WT JR (1992). Production and persistence of soil enzymes with repeated addition of organic residues. Soil Science, 153, 53-61.
[25]	McDaniel MD, Kaye JP, Kaye MW (2013). Increased temperature and precipitation had limited effects on soil extracellular enzyme activities in a post-harvest forest. Soil Biology & Biochemistry, 56, 90-98.
[26]	Michalak A (2006). Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish Journal of Environmental Studies, 15, 523-530.
[27]	Moorhead DL, Sinsabaugh RL, Hill BH, Weintraub MN (2016). Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biology & Biochemistry, 93, 1-7.
[28]	Peng XQ, 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.
[29]	Piotrowska-Długosz A, Charzyński P (2015). The impact of the soil sealing degree on microbial biomass, enzymatic activity, and physicochemical properties in the Ekranic Technosols of Toruń (Poland). Journal of Soils and Sediments, 15, 47-59.
[30]	Ren CJ, Zhao FZ, Shi Z, Chen J, Han XH, Yang GH, Feng YZ, Ren GX (2017). Differential responses of soil microbial biomass and carbon-degrading enzyme activities to altered precipitation. Soil Biology & Biochemistry, 115, 1-10.
[31]	Rustad L, Campbell J, Marion G, Norby R, Mitchell M, Hartley A, Cornelissen J, Gurevitch J, GCTE-NEWS (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. DOI URL PMID
[32]	Sardans J, Peñuelas J, Estiarte M (2008). Changes in soil enzymes related to C and N cycle and in soil C and N content under prolonged warming and drought in a Mediterranean shrubland. Applied Soil Ecology, 39, 223-235.
[33]	Seo J, Jang I, Jung JY, Lee YK, Kang H (2015). Warming and increased precipitation enhance phenol oxidase activity in soil while warming induces drought stress in vegetation of an Arctic ecosystem. Geoderma, 259- 260, 347-353.
[34]	Sinsabaugh RL, Carreiro MM, Repert DA (2002). Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry, 60, 1-24.
[35]	Sinsabaugh RL, Follstad Shah JJ (2012). Ecoenzymatic stoichiometry and ecological theory. Annual Review of Ecology, Evolution, and Systematics, 43, 313-343.
[36]	Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009). Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature, 462, 795-798. URL PMID
[37]	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. Ecology Letters, 11, 1252-1264. DOI URL PMID
[38]	Spohn M, Kuzyakov Y (2014). Spatial and temporal dynamics of hotspots of enzyme activity in soil as affected by living and dead roots—A soil zymography analysis. Plant and Soil, 379, 67-77.
[39]	Steinweg JM, Dukes JS, Paul EA, Wallenstein MD (2013). Microbial responses to multi-factor climate change: effects on soil enzymes. Frontiers in Microbiology, 4, 146. DOI: 10.3389/fmicb.2013.00146. DOI URL PMID
[40]	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 Biology & Biochemistry, 55, 85-92.
[41]	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 Biology & Biochemistry, 75, 237-247.
[42]	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. Global Change Biology, 18, 1173-1184.
[43]	Tan ZH, Zhang YP, Liang NS, Hsia YJ, Zhang YJ, Zhou GY, Li YL, Juang JY, Chu HS, Yan JH, Yu GR, Sun XM, Song QH, Cao KF, Schaefer DA, Liu YH (2012). An observational study of the carbon-sink strength of East Asian subtropical evergreen forests. Environmental Research Letters, 7, 044017. DOI: 10.1088/1748-9326/7/4/044017.
[44]	Veres Z, Kotroczó Z, Fekete I, Tóth JA, Lajtha K, Townsend K, Tóthmérész B (2015). Soil extracellular enzyme activities are sensitive indicators of detrital inputs and carbon availability. Applied Soil Ecology, 92, 18-23.
[45]	Wang SP, Duan JC, Xu GP, Wang YF, Zhang ZH, Rui YC, Luo CY, Xu B, Zhu XX, Chang XF, Cui XY, Niu HS, Zhao XQ, Wang WY (2012). Effects of warming and grazing on soil N availability, species composition, and ANPP in an alpine meadow. Ecology, 93, 2365-2376. URL PMID
[46]	Wang XC, Lu Q (2006). Beta-glucosidase activity in paddy soils of the Taihu Lake region, China. Pedosphere, 16, 118-124.
[47]	Waring BG, Weintraub SR, Sinsabaugh RL (2014). Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry, 117, 101-113.
[48]	Warton DI, Duursma RA, Falster DS, Taskinen S (2012). Smatr 3—An R package for estimation and inference about allometric lines. Methods in Ecology and Evolution, 3, 257-259.
[49]	Wei CC, Liu XF, Lin CF, Li XF, Li Y, Zheng YX (2018). Response of soil enzyme activities to litter input changes in two secondary Castanopsis carlessii forests in subtropical China. Chinese Journal of Plant Ecology, 42, 692-702.
	[ 魏翠翠, 刘小飞, 林成芳, 李先锋, 李艳, 郑裕雄 (2018). 凋落物输入改变对亚热带两种米槠次生林土壤酶活性的影响. 植物生态学报, 42, 692-702.]
[50]	Weintraub SR, Wieder WR, Cleveland CC, Townsend AR (2013). Organic matter inputs shift soil enzyme activity and allocation patterns in a wet tropical forest. Biogeochemistry, 114, 313-326.
[51]	Wu CS, Liang NS, Sha LQ, Xu XL, Zhang YP, Lu HZ, Song L, Song QH, Xie YN (2016). Heterotrophic respiration does not acclimate to continuous warming in a subtropical forest. Scientific Reports, 6, 21561. DOI: 10.1038/srep21561. URL PMID
[52]	Wu CS, Zhang YP, Xu XL, Sha LQ, You GY, Liu YH, Xie YN (2014). Influence of interactions between litter decomposition and rhizosphere activity on soil respiration and on the temperature sensitivity in a subtropical montane forest in SW China. Plant and Soil, 381, 215-224.
[53]	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.
[54]	Yang WQ, Wang KY (2004). Advances in forest soil enzymology. Scientia Silvae Sinicae, 40, 152-159.
	[ 杨万勤, 王开运 (2004). 森林土壤酶的研究进展. 林业科学, 40, 152-159.]
[55]	Zhang XL, Hu ZQ, Chu SL (2005). Methods for measuring soil water content: a reciew. Chinese Journal of Soil Science, 1, 118-7123.
	[ 张学礼, 胡振琪, 初士立 (2005). 土壤含水量测定方法研究进展. 土壤通报, 1, 118-7123.]
[56]	Zheng WG, Xue L, Xu PB, Liang LL, Feng HF (2011). Soil response to litter in a Pinus caribaea woodland. Journal of South China Agricultural University, 32, 120-123.
	[ 郑卫国, 薛立, 许鹏波, 梁丽丽, 冯慧芳 (2011). 加勒比松林地土壤对凋落物的响应. 华南农业大学学报, 32, 120-123.]
[57]	Zhou LG, Liu YT, Zhang YP, Sha LQ, Song QH, Zhou WJ, Balasubramanian D, Palingamoorthy G, Gao JB, Lin YX, Li J, Zhou RW, Zar Myo ST, Tang XH, Zhang J, Zhang P, Wang SS, Grace J (2019). Soil respiration after six years of continuous drought stress in the tropical rainforest in Southwest China. Soil Biology & Biochemistry, 138, 107564. DOI: 10.1016/j.soilbio.2019.107564.
[58]	Zhou XQ, Chen CR, Wang YF, Xu ZH, Han HY, Li LH, Wan SQ (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.
[59]	Zhu H (2016). Discussion on the origin of mid-montane wet evergreen broad-leaved forest in Yunnan. Plant Science Journal, 34, 715-723.
	[ 朱华 (2016). 云南中山湿性常绿阔叶林起源的探讨. 植物科学学报, 34, 715-723.]

酶 Enzyme	缩写 Abbreviation	功能 Function
β-葡萄糖苷酶 β-glucosidase	BG	分解易降解碳 Decomposition of labile carbon
多酚氧化酶 Polyphenol oxidase	POX	分解难降解碳 Decomposition of recalcitrant carbon
过氧化物酶 Peroxidase	PER	分解难降解碳 Decomposition of recalcitrant carbon
β-1,4-N-乙酰氨基葡萄糖苷酶 β-1,4-N-acetylglucosaminidase	NAG	分解氮 Hydrolyze nitrogen
酸性磷酸酶 Acid phosphatase	AP	分解磷 Hydrolyze phosphorus

酶 Enzyme	缩写 Abbreviation	功能 Function
β-葡萄糖苷酶 β-glucosidase	BG	分解易降解碳 Decomposition of labile carbon
多酚氧化酶 Polyphenol oxidase	POX	分解难降解碳 Decomposition of recalcitrant carbon
过氧化物酶 Peroxidase	PER	分解难降解碳 Decomposition of recalcitrant carbon
β-1,4-N-乙酰氨基葡萄糖苷酶 β-1,4-N-acetylglucosaminidase	NAG	分解氮 Hydrolyze nitrogen
酸性磷酸酶 Acid phosphatase	AP	分解磷 Hydrolyze phosphorus

观测项目 Observation item	测定值 Value
酸碱度 pH	4.25 ± 0.05
容重 Bulk density (g·cm^-3)	0.54 ± 0.02
总孔隙度 Total porosity (%)	71.7 ± 2.0
土壤最大持水量 Maximum water capacity of soil (%)	119.1 ± 6.0
有机质含量 Organic matter content (g·kg^-1)	175.1 ± 11.7
总氮含量 Total nitrogen content (g·kg^-1)	7.18 ± 0.34
碳氮比 C:N	14.1 ± 1.6

观测项目 Observation item	测定值 Value
酸碱度 pH	4.25 ± 0.05
容重 Bulk density (g·cm^-3)	0.54 ± 0.02
总孔隙度 Total porosity (%)	71.7 ± 2.0
土壤最大持水量 Maximum water capacity of soil (%)	119.1 ± 6.0
有机质含量 Organic matter content (g·kg^-1)	175.1 ± 11.7
总氮含量 Total nitrogen content (g·kg^-1)	7.18 ± 0.34
碳氮比 C:N	14.1 ± 1.6

处理 Treatment	土壤含水量 Soil water content (%)	铵态氮含量 NH₄⁺-N content (mg·kg^-1)	硝态氮含量 NO₃^--N content (mg·kg^-1)	溶解有机碳含量 Dissolved organic carbon content (mg·kg^-1)	溶解总氮含量 Total dissolved nitrogen content (mg·kg^-1)	溶解有机氮含量 Dissolved organic nitrogen content (mg·kg^-1)	矿质氮含量 Mineral-N content (mg·kg^-1)
0-5 cm
CK	34.35 ± 2.30^aA	61.11 ± 11.30^abA	10.26 ± 3.75^aA	235.88 ± 21.76^aA	118.79 ± 16.82^abA	47.43 ± 7.77^aA	71.36 ± 9.19^abA
LR	26.35 ± 0.81^bA	43.74 ± 4.55^bA	10.03 ± 3.31^aA	267.48 ± 21.10^aA	93.92 ± 4.01^bA	40.16 ± 3.41^aA	53.76 ± 1.49^bA
TR	33.65 ± 1.35^aA	89.08 ± 6.10^aA	2.49 ± 0.27^aA	259.62 ± 17.47^aA	143.56 ± 7.52^aA	51.99 ± 8.12^aA	91.57 ± 5.93^aA
TR+W	29.41 ± 1.16^abA	52.56 ± 1.19^bA	3.90 ± 0.16^aA	232.33 ± 20.29^aA	103.89 ± 7.87^abA	47.44 ± 8.38^aA	56.45 ± 1.31^bA
5-10 cm
CK	32.44 ± 1.07^aA	29.12 ± 3.22^aB	5.73 ± 0.23^bA	207.73 ± 13.46^bA	48.11 ± 2.88^bB	13.27 ± 4.96^aB	34.84 ± 3.09^aB
LR	30.00 ± 0.58^bB	28.72 ± 1.68^aA	7.55 ± 0.74^abA	269.07 ± 13.14^aA	61.43 ± 2.79^aB	25.16 ± 1.52^aB	36.27 ± 2.34^aB
TR	32.56 ± 0.72^aA	28.88 ± 1.77^aB	9.35 ± 0.90^aB	189.94 ± 10.05^bB	52.78 ± 4.49^abB	14.55 ± 3.98^aB	38.23 ± 1.73^aB
TR+W	30.95 ± 0.37^abA	33.42 ± 1.94^aB	5.18 ± 0.75^bA	214.82 ± 9.62^bA	53.44 ± 3.15^abB	14.83 ± 2.20^aB	38.60 ± 2.01^aB