Effects of dissolved organic matter from different plant sources on soil enzyme activities in subtropical forests

doi:10.17521/cjpe.2020.0097

Abstract

Abstract:

Aims This study aims to explore the effects of dissolved organic matter (DOM) from different plant sources on subtropical forest soil enzyme activities in order to provide a scientific basis for soil carbon cycling under rainfall leaching conditions in different forest ecosystems of subtropical areas.
Methods Three kinds of DOM, extracted from the fresh leaves of Cunninghamia lanceolata, Schima superb, and Phoebe zherman, were added to the soils of C. lanceolata plantation. Soil treated with deionized water of the same amount as the DOM solution served as the control. Incubation of treated and control soils was conducted for 25 days in the laboratory. The physical and chemical properties, microbial biomass, and enzyme activities of the soils were determined after incubation.
Important findings The results showed that, compared with the control treatment (CT), soil total organic carbon (SOC) content, soil total nitrogen (TN) content, and carbon-nitrogen ratio had no significant changes after adding DOM. However, the TN of treatment with added C. lanceolata leaf DOM (CL) was significantly lower than that of treatments with added S. superb leaf DOM (SL) and P. zherman leaf DOM (PL), and the carbon-nitrogen ratio in CL was significantly higher than that in SL and PL. The three treatments with added DOM increased soil dissolved organic carbon (DOC) content and dissolved organic nitrogen (DON) content overall. There was no significant change in soil microbial biomass carbon (MBC) content after all three DOM inputs, while the microbial biomass nitrogen (MBN) content in CL and SL treatments was reduced by 50.9% and 51.1%, respectively, compared to CT. However, MBN content in PL treatment was increased by 54.0% than CT. DOM input significantly increased the activities of β-glucosidase, cellobiohydrolase, and peroxidase in comparison with CT, but significantly decreased the activity of polyphenol oxidase. In addition, both β-glucosidase and cellobiohydrolase activities showed the following characteristics: CL > SL > PL. The results of correlation analysis showed that the contents of SOC, TN and MBN and the activities of β-glucosidase and cellobiohydrolase of the treatments with DOM were significantly correlated with the DOC content and humification index (HIX) of added DOM. In addition, soil MBN content and polyphenol oxidase activity were positively correlated with the pH value of added DOM. The results of redundancy analysis (RDA) showed that the key factors causing the change in soil enzyme activities after DOM input were DON and DOC content. In general, differences in the properties of DOM obtained from different plant sources affect the activities of soil carbon-acquisition hydrolase. DOM input increases the availability of soil carbon and nitrogen, and elicits different responses from the four carbon-acquisition enzymes. This study provides a theoretical basis for exploring the process of carbon cycling in the rain-rich subtropical forest ecosystem.

Key words: dissolved organic matter, soil enzyme, soil nutrient availability, fresh leaves, subtropical forest

MEI Kong-Can, CHENG Lei, ZHANG Qiu-Fang, LIN Kai-Miao, ZHOU Jia-Cong, ZENG Quan-Xin, WU Yue, XU Jian-Guo, ZHOU Jin-Rong, CHEN Yue-Min. Effects of dissolved organic matter from different plant sources on soil enzyme activities in subtropical forests[J]. Chin J Plant Ecol, 2020, 44(12): 1273-1284.

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URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2020.0097

https://www.plant-ecology.com/EN/Y2020/V44/I12/1273

Figures/Tables 7

References 57

[1]	Ågren GI, Bosatta E, Magill AH (2001). Combining theory and experiment to understand effects of inorganic nitrogen on litter decomposition. Oecologia, 128, 94-98. DOI URL PMID
[2]	Allison SD, Vitousek PM (2005). Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biology & Biochemistry, 37, 937-944.
[3]	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, Berlin, Germany. 229-243.
[4]	Bao Y, Gao Y, Zeng XM, Yuan P, Si YT, Chen YM, Chen YY (2018). Relationships between carbon and nitrogen contents and enzyme activities in soil of three typical subtropical forests in China. Chinese Journal of Plant Ecology, 42, 508-516.
	[ 鲍勇, 高颖, 曾晓敏, 袁萍, 司友涛, 陈岳民, 陈滢伊 (2018). 中亚热带3种典型森林土壤碳氮含量和酶活性的关系. 植物生态学报, 42, 508-516.]
[5]	Boddy E, Hill PW, Farrar J, Jones DL (2007). Fast turnover of low molecular weight components of the dissolved organic carbon pool of temperate grassland field soils. Soil Biology & Biochemistry, 39, 827-835.
[6]	Chen GS, Yang ZJ, Gao R, Xie JS, Guo JF, Huang ZQ, Yang YS (2013). Carbon storage in a chronosequence of Chinese fir plantations in southern China. Forest Ecology and Management, 300, 68-76.
[7]	Chen J, Luo YQ, Li JW, Zhou XH, Cao JJ, Wang RW, Wang YQ, Shelton S, Jin Z, Walker LM, Feng ZZ, Niu SL, Feng WT, Jian SY, Zhou LY (2017). Costimulation of soil glycosidase activity and soil respiration by nitrogen addition. Global Change Biology, 23, 1328-1337. URL PMID
[8]	Chen X, Hao B, Jing X, He JS, Ma W, Zhu B (2019). Minor responses of soil microbial biomass, community structure and enzyme activities to nitrogen and phosphorus addition in three grassland ecosystems. Plant and Soil, 444, 21-37.
[9]	Curtin D, Campbell CA, Jalil A (1998). Effects of acidity on mineralization: pH-dependence of organic matter mineralization in weakly acidic soils. Soil Biology & Biochemistry, 30, 57-64.
[10]	Du YX, Zhang YY, Chen FZ, Chang YG, Liu ZW (2016). Photochemical reactivities of dissolved organic matter (DOM) in a sub-alpine lake revealed by EEM-PARAFAC: an insight into the fate of allochthonous DOM in alpine lakes affected by climate change. Science of the Total Environment, 568, 216-225.
[11]	Fan YX, Zhong XJ, Lin TC, Lyu MK, Wang MH, Hu WF, Yang ZJ, Chen GS, Guo JF, Yang YS (2020). Effects of nitrogen addition on DOM-induced soil priming effects in a subtropical plantation forest and a natural forest. Biology and Fertility of Soils, 56, 205-216.
[12]	Fang Y, Nazaries L, Singh BK, Singh BP (2018). Microbial mechanisms of carbon priming effects revealed during the interaction of crop residue and nutrient inputs in contrasting soils. Global Change Biology, 24, 2775-2790. URL PMID
[13]	Fontaine S, Barot S, Barré P, Bdioui N, Mary B, Rumpel C (2007). Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature, 450, 277-280. DOI URL PMID
[14]	Gao YQ, Dai XQ, Wang JL, Fu XL, Kou L, Wang HM (2019). Characteristics of soil enzymes stoichiometry in rhizosphere of understory vegetation in subtropical forest plantations. Chinese Journal of Plant Ecology, 43, 258-272.
	[ 高雨秋, 戴晓琴, 王建雷, 付晓莉, 寇亮, 王辉民 (2019). 亚热带人工林下植被根际土壤酶化学计量特征. 植物生态学报, 43, 258-272.]
[15]	Gauthier A, Amiotte-Suchet P, Nelson PN, Lévêque J, Zeller B, Hénault C (2010). Dynamics of the water extractable organic carbon pool during mineralisation in soils from a Douglas fir plantation and an oak-beech forest—An incubation experiment. Plant and Soil, 330, 465-479.
[16]	Guo JF, Yang YS, Chen GS, Lin P (2005). Dissolved organic carbon and nitrogen in precipitation, throughfall and stemflow from Schima superba and Cunninghamia lanceolata plantations in subtropical China. Journal of Forestry Research, 16, 19-22.
[17]	Inubushi K, Brookes PC, Jenkinson DS (1991). Soil microbial biomass C, N and ninhydrin-N in aerobic and anaerobic soils measured by the fumigation-extraction method. Soil Biology & Biochemistry, 23, 737-741.
[18]	Ji YH, Zhang QF, Zhou JC, You ZT, Xu PC, Lin WS, Chen YM, Yang YS (2018). Spectral characteristics and quantities of dissolved organic matter released from leaves with competitive and stress-tolerant ecological strategies in a subtropical region. Acta Ecologica Sinica, 38, 3998-4007.
	[ 纪宇皝, 张秋芳, 周嘉聪, 游章湉, 徐鹏程, 林伟盛, 陈岳民, 杨玉盛 (2018). 亚热带地区竞争型和忍耐型树种叶片可溶性有机质数量及光谱学特征. 生态学报, 38, 3998-4007.]
[19]	Jiang Y, Lei Y, Qin W, Korpelainen H, Li C (2019). Revealing microbial processes and nutrient limitation in soil through ecoenzymatic stoichiometry and glomalin-related soil proteins in a retreating glacier forefield. Geoderma, 338, 313-324.
[20]	Jing X, Chen X, Tang M, Ding ZJ, Jiang L, Li P, Ma SH, Tian D, Xu LC, Zhu JX, Ji CJ, Shen HH, Zheng CY, Fang JY, Zhu B (2017). Nitrogen deposition has minor effect on soil extracellular enzyme activities in six Chinese forests. Science of the Total Environment, 607-608, 806-815.
[21]	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.
[22]	Kalbitz K, Geyer W, Geyer S (1999). Spectroscopic properties of dissolved humic substances—A reflection of land use history in a fen area. Biogeochemistry, 47, 219-238.
[23]	Kalbitz K, Solinger S, Park JH, Michalzik B, Matzner E (2000). Controls on the dynamics of dissolved organic matter in soils: a review. Soil Science, 165, 277-304.
[24]	Kang GL, Gao R, Yang YS, Chen GS, Yang ZJ, Si YT (2014). Quantities and qualities of leaf-leached DOM of four species in a secondary Castanopsis carlesii forest. Journal of Subtropical Resources and Environment, 9, 30-37.
	[ 康根丽, 高人, 杨玉盛, 陈光水, 杨智杰, 司友涛 (2014). 米槠次生林内4种植物叶片DOM的数量和质量特征. 亚热带资源与环境学报, 9, 30-37.]
[25]	Kotroczó Z, Veres Z, Fekete I, Krakomperger Z, Tóth JA, Lajtha K, Tóthmérész B (2014). Soil enzyme activity in response to long-term organic matter manipulation. Soil Biology & Biochemistry, 70, 237-243.
[26]	Li YL, Zhang XB, Ren FL, Sun N, Xu M, Xu MG (2020). A meta-analysis of long-term fertilization impact on soil dissolved organic carbon and nitrogen across Chinese cropland. Scientia Agricultura Sinica, 53, 1224-1233.
	[ 李亚林, 张旭博, 任凤玲, 孙楠, 徐梦, 徐明岗 (2020). 长期施肥对中国农田土壤溶解性有机碳氮含量影响的整合分析. 中国农业科学, 53, 1224-1233.]
[27]	Lin KM, Zhang ZQ, Ye FM, Lin Y, Li QS (2010). Dynamic analysis of decomposition characteristics and content change of nutrient elements of leaf litter of Cunninghamia lanceolata, Phoebe bournei and Schima superba under C. lanceolata artificial forest. Journal of Plant Resources and Environment, 19(2), 34-39.
	[ 林开敏, 章志琴, 叶发茂, 林艳, 李卿叁 (2010). 杉木人工林下杉木、楠木和木荷叶凋落物分解特征及营养元素含量变化的动态分析. 植物资源与环境学报, 19(2), 34-39.]
[28]	Luo G, Li L, Friman VP, Guo J, Guo S, Shen Q, Ling N (2018). Organic amendments increase crop yields by improving microbe-mediated soil functioning of agroecosystems: a meta-analysis. Soil Biology & Biochemistry, 124, 105-115.
[29]	Lyu M, Xie J, Vadeboncoeur MA, Wang M, Qiu X, Ren Y, Jiang M, Yang Y, Kuzyakov Y (2018). Simulated leaf litter addition causes opposite priming effects on natural forest and plantation soils. Biology and Fertility of Soils, 54, 925-934.
[30]	Miano TM, Senesi N (1992). Synchronous excitation fluorescence spectroscopy applied to soil humic substances chemistry. Science of the Total Environment, 117, 41-51.
[31]	Näsholm T, Ekblad A, Nordin A, Giesler R, Högberg M, Högberg P (1998). Boreal forest plants take up organic nitrogen. Nature, 392, 914-916.
[32]	Ni MY, Zhang QF, Gao JT, Zheng Y, Zhou JC, Chen YM, Yang YS (2018). Seasonal response of extracellular enzyme activity to precipitation exclusion in a subtropical Cunninghamia lanceolata plantation. Acta Ecologica Sinica, 38, 2119-2127.
	[ 倪梦颖, 张秋芳, 高金涛, 郑永, 周嘉聪, 陈岳民, 杨玉盛 (2018). 亚热带杉木人工林土壤胞外酶活性对隔离降雨的季节响应. 生态学报, 38, 2119-2127.]
[33]	Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, et al. (2013). New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany, 61, 167-234.
[34]	Peterson ME, Curtin D, Thomas S, Clough TJ, Meenken ED (2013). Denitrification in vadose zone material amended with dissolved organic matter from topsoil and subsoil. Soil Biology & Biochemistry, 61, 96-104.
[35]	Piao S, Fang J, Ciais P, Peylin P, Huang Y, Sitch S, Wang T (2009). The carbon balance of terrestrial ecosystems in China. Nature, 458, 1009-1013. URL PMID
[36]	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 Biology & Biochemistry, 34, 1309-1315.
[37]	Schimel J, Balser TC, Wallenstein M (2007). Microbial stress response physiology and its implications for ecosystem function. Ecology, 88, 1386-1394. DOI URL PMID
[38]	Singh JS, Gupta VK (2018). Soil microbial biomass: a key soil driver in management of ecosystem functioning. Science of the Total Environment, 634, 497-500.
[39]	Sinsabaugh RL (2010). Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biology & Biochemistry, 42, 391-404.
[40]	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. DOI URL
[41]	Šnajdr J, Valášková V, Merhautová V, Herinková J, Cajthaml T, Baldrian P (2008). Spatial variability of enzyme activities and microbial biomass in the upper layers of Quercus petraea forest soil. Soil Biology & Biochemistry, 40, 2068-2075.
[42]	Song XZ, Chen XF, Zhou GM, Jiang H, Peng CH (2017). Observed high and persistent carbon uptake by Moso bamboo forests and its response to environmental drivers. Agricultural and Forest Meteorology, 247, 467-475.
[43]	Soussana JF, Lemaire G (2014). Coupling carbon and nitrogen cycles for environmentally sustainable intensification of grasslands and crop-livestock systems. Agriculture, Ecosystems & Environment, 190, 9-17.
[44]	Vance ED, Brookes PC, Jenkinson DS (1987). An extraction method for measuring soil microbial biomass C. Soil Biology & Biochemistry, 19, 703-707.
[45]	Wan JJ, Guo JF, Ji SR, Ren WL, Yang YS (2016). Effects of dissolved organic matter input on soil CO₂ emission and microbial community composition in a subtropical forest. Scientia Silvae Sinicae, 52(2), 106-113.
	[ 万菁娟, 郭剑芬, 纪淑蓉, 任卫岭, 杨玉盛 (2016). 可溶性有机物输入对亚热带森林土壤CO₂排放及微生物群落的影响. 林业科学, 52(2), 106-113.]
[46]	Wang JY, Song CC, Wang XW, Wang LL (2011). Progress in the study of effect of freeze-thaw processes on the organic carbon pool and microorganisms in soils. Journal of Glaciology and Geocryology, 33, 442-452.
	[ 王娇月, 宋长春, 王宪伟, 王丽丽 (2011). 冻融作用对土壤有机碳库及微生物的影响研究进展. 冰川冻土, 33, 442-452.]
[47]	Wang QK, Wang SL, He TX, Liu L, Wu JB (2014). Response of organic carbon mineralization and microbial community to leaf litter and nutrient additions in subtropical forest soils. Soil Biology & Biochemistry, 71, 13-20.
[48]	Wang XB, Song DL, Liang GQ, Zhang Q, Ai C, Zhou W (2015). Maize biochar addition rate influences soil enzyme activity and microbial community composition in a fluvo-aquic soil. Applied Soil Ecology, 96, 265-272.
[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]	Wieder WR, Cleveland CC, Townsend AR (2008). Tropical tree species composition affects the oxidation of dissolved organic matter from litter. Biogeochemistry, 88, 127-138.
[51]	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.
[52]	Zhang CX, Nan ZB (2010). Research progress of soil microbial biomass in China. Pratacultural Science, 27, 50-57.
	[ 张成霞, 南志标 (2010). 土壤微生物生物量的研究进展. 草业科学, 27, 50-57.]
[53]	Zheng HF, Liu Y, Zhang J, Chen YM, Yang L, Li HJ, Wang LF (2018). Factors influencing soil enzyme activity in China’s forest ecosystems. Plant Ecology, 219, 31-44.
[54]	Zhou JB, Chen ZJ, Zheng XF (2005). Soluble organic nitrogen in soil and its roles in the supply and transformation of N. Chinese Journal of Soil Science, 36, 244-248.
	[ 周建斌, 陈竹君, 郑险峰 (2005). 土壤可溶性有机氮及其在氮素供应及转化中的作用. 土壤通报, 36, 244-248.]
[55]	Zhou JC, Liu XF, Zheng Y, Ji YH, Li XF, Xu PC, Chen YM, Yang YS (2017). Effects of nitrogen deposition on soil microbial biomass and enzyme activities in Castanopsis carlesii natural forests in subtropical regions. Acta Ecologica Sinica, 37, 127-135.
	[ 周嘉聪, 刘小飞, 郑永, 纪宇皝, 李先锋, 徐鹏程, 陈岳民, 杨玉盛 (2017). 氮沉降对中亚热带米槠天然林微生物生物量及酶活性的影响. 生态学报, 37, 127-135.]
[56]	Zhou Y, Boutton TW, Wu XB (2018). Soil phosphorus does not keep pace with soil carbon and nitrogen accumulation following woody encroachment. Global Change Biology, 24, 1992-2007. DOI URL PMID
[57]	Zhu ZK, Ge T, Luo Y, Liu SL, Xu XL, Tong CL, Shibistova O, Guggenberger G, Wu JS (2018). Microbial stoichiometric flexibility regulates rice straw mineralization and its priming effect in paddy soil. Soil Biology & Biochemistry, 121, 67-76.

DOM来源 DOM from different plant sources	溶解有机碳含量 Dissolved organic carbon content (g·kg^-1)	溶解有机氮含量 Dissolved organic nitrogen content (mg·kg^-1)	腐殖化指数 Humification index	酸碱度 pH
杉木 Cunninghamia lanceolata	19.32 ± 0.90^a	7.63 ± 1.44^b	0.27 ± 0.02^c	5.44 ± 0.11^b
木荷 Schima superba	12.77 ± 2.86^b	26.10 ± 2.11^a	1.67 ± 0.55^b	5.28 ± 0.03^c
楠木 Phoebe zherman	6.95 ± 0.45^c	11.20 ± 2.72^b	4.36 ± 0.59^a	5.76 ± 0.02^a
p	<0.01	<0.01	<0.01	<0.01

DOM来源 DOM from different plant sources	溶解有机碳含量 Dissolved organic carbon content (g·kg^-1)	溶解有机氮含量 Dissolved organic nitrogen content (mg·kg^-1)	腐殖化指数 Humification index	酸碱度 pH
杉木 Cunninghamia lanceolata	19.32 ± 0.90^a	7.63 ± 1.44^b	0.27 ± 0.02^c	5.44 ± 0.11^b
木荷 Schima superba	12.77 ± 2.86^b	26.10 ± 2.11^a	1.67 ± 0.55^b	5.28 ± 0.03^c
楠木 Phoebe zherman	6.95 ± 0.45^c	11.20 ± 2.72^b	4.36 ± 0.59^a	5.76 ± 0.02^a
p	<0.01	<0.01	<0.01	<0.01

土壤酶 Soil enzyme	缩写 Abbreviation	底物 Substrate	功能 Function
β-葡萄糖苷酶 β-glucosidase	βG	4-MUB-β-D-glucoside	水解纤维素 Hydrolyze cellulose
纤维素水解酶 Cellobiohydrolase	CBH	4-MUB-β-D-cellobioside	水解纤维素 Hydrolyze cellulose
过氧化物酶 Peroxidase	PEO	L-dihydroxyphenylalanine	降解木质素 Degrade lignin
多酚氧化酶 Polyphenol oxidase	PPO	L-dihydroxyphenylalanine	降解木质素 Degrade lignin

土壤酶 Soil enzyme	缩写 Abbreviation	底物 Substrate	功能 Function
β-葡萄糖苷酶 β-glucosidase	βG	4-MUB-β-D-glucoside	水解纤维素 Hydrolyze cellulose
纤维素水解酶 Cellobiohydrolase	CBH	4-MUB-β-D-cellobioside	水解纤维素 Hydrolyze cellulose
过氧化物酶 Peroxidase	PEO	L-dihydroxyphenylalanine	降解木质素 Degrade lignin
多酚氧化酶 Polyphenol oxidase	PPO	L-dihydroxyphenylalanine	降解木质素 Degrade lignin

处理 Treatment	土壤总有机碳含量 Total soil organic carbon content (g·kg^-1)	总氮含量 Total soil nitrogen content (g·kg^-1)	碳氮比 C:N	酸碱度 pH	溶解有机碳含量 Dissolved organic carbon content (mg·kg^-1)	溶解有机氮含量 Dissolved organic nitrogen content (mg·kg^-1)
CT	75.96 ± 0.14^a	4.72 ± 0.13^ab	16.11 ± 0.45^ab	4.49 ± 0.02^b	32.65 ± 12.20^b	5.39 ± 1.32^b
CL	70.94 ± 2.17^a	4.26 ± 0.23^b	16.69 ± 0.72^a	4.70 ± 0.12^a	139.02 ± 24.90^a	26.95 ± 8.65^a
SL	70.55 ± 1.77^a	4.53 ± 0.10^ab	15.58 ± 0.07^b	4.72 ± 0.09^a	154.06 ± 56.81^a	9.42 ± 1.44^b
PL	75.63 ± 5.22^a	4.89 ± 0.40^a	15.48 ± 0.31^b	4.59 ± 0.12^ab	110.24 ± 20.41^a	6.51 ± 1.78^b
p	0.10	0.06	0.04	0.06	0.01	<0.01