Responses of Soil Enzyme Activities to Nitrogen Addition and Its Impact Factors at the Alpine Steppe of Northern Tibet

doi:10.11733/j.issn.1007-0435.2021.03.017

Acta Agrestia Sinica ›› 2021, Vol. 29 ›› Issue (3): 555-562.DOI: 10.11733/j.issn.1007-0435.2021.03.017

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Responses of Soil Enzyme Activities to Nitrogen Addition and Its Impact Factors at the Alpine Steppe of Northern Tibet

WU Jian-bo, WANG Xiao-dan

Xianzha Alpine Steppe and Wetland Ecosystem Observation and Experiment Station, Key Laboratory of Mountain Environment Evolution and Regulation, Institute of Mountain Hazard and Environment CAS, Chengdu, Sichuan Province 610041, China

Received:2020-09-21 Revised:2020-10-31 Online:2021-03-15 Published:2021-04-02

藏北高寒草原土壤酶活性对氮添加的响应及其影响因素

吴建波, 王小丹

中国科学院申扎高寒草原与湿地生态系统观测试验站;山地表生过程与生态调控重点实验室, 中国科学院、水利部成都山地灾害与环境研究所, 四川成都 610041

通讯作者: 王小丹
作者简介:吴建波(1979-),男,河北邢台人,博士,主要从事高寒草地生态研究,E-mail:wujianbo@imde.ac.cn
基金资助:
第二次青藏高原综合科学考察研究（SQ2019QZKK2004）；国家重点研发计划（2016YFC0502002）；国家自然科学基金项目（41401072）资助

Abstract

Abstract: To clarify the activities of various soil enzymes responding to the nitrogen deposition,we established a field experiment by adding ammonium nitrate to stimulate nitrogen deposition at alpine steppe in 2013. Four nitrogen fertilizer treatments (0,2,5,and 10 g·m^-2·yr^-1) were applied at 24 plots. We collected plant samples by the quadrat sampling method and soil samples by the double diaonal line in 2017. We analyzed the soil enzyme activity at four levels after 5 years of nitrogen addition. The results showed that the activity of invertase,cellulose,polyphenol oxidase and peroxidase significantly decreased due to nitrogen addition (P < 0.01). The activity of urease and neutral phosphatase was significantly increased by nitrogen addition (P < 0.01). Results from Pearson analysis and redundancy analysis showed that soil pH was not affected by nitrogen addition,which did not influence soil enzyme. Nitrogen increased the content of soil nitric nitrogen and ammoniacal nitrogen. The aboveground litter and underground biomass were also increased and root lignin content was decreased due to nitrogen addition. Soil microorganisms prefer low molecular weight organic nitrogen and carbon compounds,which would depress the carbon hydrolase and oxidase,and activate the urase. Nitrogen addition activated plants and increased the absorption of phosphorus,which would improve the activity of phosphatase. Therefore,the changes in the plant property under nitrogen addition were the most important factors for the soil enzyme at alpine steppe.

Key words: Nitrogen deposition, Soil enzyme activity, Plant property, Microbial property, Soil property

摘要： 为阐明藏北高寒草原土壤酶活性对氮沉降响应规律，本研究于2013年开展模拟氮沉降试验(氮添加水平：0，2，5和10 g·m^-2·yr^-1)，采用样方法对植物取样，双对角线法对土壤取样，分析土壤酶活性在氮添加5年后的变异特征及影响土壤酶活性的主要环境要素。结果表明：蔗糖酶、纤维素酶、多酚氧化酶和过氧化氢酶活性在氮添加后显著降低(P<0.01)，而脲酶和中性磷酸酶活性在氮添加后显著增加(P<0.01)。通过相关性分析和冗余分析表明：氮添加未显著影响土壤pH，土壤pH对土壤酶不存在显著影响。氮添加增加土壤活性氮含量，提高凋落物量和地下生物量，降低根系木质素含量；氮添加增加土壤中易分解的碳氮资源，降低碳相关水解酶和氧化酶活性，提高脲酶活性；氮添加提高了植物对磷的需求，增强磷酸酶活性。因此，氮添加引起植物特征的变化是影响土壤酶活性的主要因素。

关键词: 氮沉降, 土壤酶, 植物特征, 微生物特征, 土壤特征

CLC Number:

S154.1

WU Jian-bo, WANG Xiao-dan. Responses of Soil Enzyme Activities to Nitrogen Addition and Its Impact Factors at the Alpine Steppe of Northern Tibet[J]. Acta Agrestia Sinica, 2021, 29(3): 555-562.

吴建波, 王小丹. 藏北高寒草原土壤酶活性对氮添加的响应及其影响因素[J]. 草地学报, 2021, 29(3): 555-562.

References

[1] Fenner A. Effects of long-term atmospheric nitrogen deposition on extracellular enzyme activity in semi-arid shrubland soil[D]. California:California State Universsity,2015:1-31
[2] Sinsabaugh R L,Moorhead D L. Resource allocation to extracellular enzyme production:a model for nitrogen and phosphorus control of litter decomposition[J]. Soil Biology and Biochemistry,1994,26(10):1305-1311
[3] Allison S D,Vitousek P M. Responses of extracellular enzymes to simple and complex nutrient inputs[J]. Soil Biology and Biochemistry,2005,37(5):937-944
[4] Tian X F,Hu H W,Ding Q,et al. Influence of nitrogen fertilization on soil ammonia oxidizer and denitrifier abundance,microbial biomass,and enzyme activities in an alpine meadow[J]. Biology and Fertility of Soils,2014,50(4):703-713
[5] 孙亚男,李茜,李以康,等. 氮、磷养分添加对高寒草甸土壤酶活性的影响[J]. 草业学报,2016,25(2):18-26
[6] Jing X,Yang X,Ren F,et al. Neutral effect of nitrogen addition and negative effect of phosphorus addition on topsoil extracellular enzymatic activities in an alpine grassland ecosystem[J]. Applied Soil Ecology,2016(107):205-213
[7] Li W,Zhang R,Liu S,et al. Effect of loss of plant functional group and simulated nitrogen deposition on subalpine ecosystem properties on the Tibetan Plateau[J]. Science of the Total Environment,2018(631):289-297
[8] Liu X,Zhang S. Nitrogen addition shapes soil enzyme activity patterns by changing pH rather than the composition of the plant and microbial communities in an alpine meadow soil[J]. Plant and Soil,2019,440(1-2):11-24
[9] Dong J,Cui X,Wang S,et al. Changes in biomass and quality of alpine steppe in response to N & P fertilization in the Tibetan Plateau[J]. PLoS One,2016,11(5):e0156146
[10] Li C,Peng Y,Nie X,et al. Differential responses of heterotrophic and autotrophic respiration to nitrogen addition and precipitation changes in a Tibetan alpine steppe[J]. Scientific Reports,2018,8(1):1-13
[11] Li Y,Nie C,Liu Y,et al. Soil microbial community composition closely associates with specific enzyme activities and soil carbon chemistry in a long-term nitrogen fertilized grassland[J]. Science of The Total Environment,2019(654):264-274
[12] Wu J B,Wang X D. Temporal stability of aboveground net primary production in northern Tibet alpine steppe in response to nitrogen addition[J]. Journal of Mountain Science,2019,16(11):2679-2686
[13] Wu J B,Wang X D. Stoichiometric homeostasis does not affect species dominance and stability in an alpine steppe,Tibetan Plateau. Arctic,Antarctic,and Alpine Research,2019,51(1):1-8
[14] Wu J B,Li N,Wang X D. Nitrogen deposition strengthens the relationship between plants and the soil fungal community in alpine steppe,North Tibet. Applied Soil Ecology,2020(147):103441
[15] 杜忠毓,安慧,王波,等. 养分添加和降水变化对荒漠草原植物群落物种多样性和生物量的影响[J]. 草地学报,2020,28(4):1100-1110
[16] Sinsabaugh R L,Lauber C L,Weintraub M N,et al. Stoichiometry of soil enzyme activity at global scale[J]. Ecology Letters,2008,11(11):1252-1264
[17] Zhang G N,Chen Z H,Zhang A M,et al. Effects of nitrogen deposition on typical hydrolytic enzyme activities by fluorimetric assay. Asian Journal of Chemistry,2013,25(18):10335-10338
[18] Wang R,Filley T R,Xu Z,et al. Coupled response of soil carbon and nitrogen pools and enzyme activities to nitrogen and water addition in a semi-arid grassland of Inner Mongolia[J]. Plant and Soil,2014,381(1-2):323-336
[19] 刘红梅,周广帆,李洁,等. 氮沉降对贝加尔针茅草原土壤酶活性的影响[J]. 生态环境学报,2018,27(8):1387-1394
[20] Chen H,Li D,Zhao J,et al. Effects of nitrogen addition on activities of soil nitrogen acquisition enzymes:A meta-analysis[J]. Agriculture,Ecosystems and Environment,2018(252):126-131
[21] Burns R G,Deforest J L,Marxsen J,et al. Soil enzymes in a changing environment:current knowledge and future directions[J]. Soil Biology and Biochemistry,2013(58):216-234
[22] Cornwell W K,Cornelissen J H C,Amatangelo K,et al. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide[J]. Ecology Letters,2008,11(10):1065-1071
[23] Marklein A R,Houlton B Z. Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems[J]. New Phytologist,2012,193(3):696-704
[24] Jian S,Li J,Chen J,et al. Soil extracellular enzyme activities,soil carbon and nitrogen storage under nitrogen fertilization:A meta-analysis[J]. Soil Biology and Biochemistry,2016(101):32-43
[25] 范珍珍,王鑫,王超,等. 整合分析氮磷添加对土壤酶活性的影响[J]. 应用生态学报,2018,29(4):1266-1272
[26] 吴建波,王小丹. 围封年限对藏北退化高寒草原植物群落特征和生物量的影响[J]. 草地学报,2017,25(2):261-266
[27] 鲍士旦. 土壤农化分析[M]. 第三版. 北京:中国农业出版社,2000,22-106
[28] 李小涵,王朝辉. 两种测定土壤有机碳方法的比较[J]. 分析仪器,2009(5):78-80
[29] 张英利,许安民,尚浩博,等. AA3型连续流动分析仪测定土壤和植物全氮的方法研究[J]. 西北农林科技大学学报:自然科学版,2006,34(10):128-132
[30] Van Soest P J. Development of a comprehensive system of feed analyses and its application to forages[J]. Journal of Animal Science,1967,26(1):119-128
[31] Lu H,Wang W,Li F,et al. Mixed-surfactant-enhanced phytoremediation of PAHs in soil:Bioavailability of PAHs and responses of microbial community structure[J]. Science of The Total Environment,2019(653):658-666
[32] 林启美,吴玉光,刘焕龙. 熏蒸法测定土壤微生物量碳的改进[J]. 生态学杂志,1999(2):63-66
[33] Shen J,Zhang L,Zhu Y,et al. Abundance and composition of ammonia oxidizing bacteria and ammonia oxidizing archaea communities of an alkaline sandy loam[J]. Environmental Microbiology,2008,10(6):1601-1611
[34] Blagodatskaya E V,Blagodatsky S A,Anderson T H,et al. Priming effects in Chernozem induced by glucose and N in relation to microbial growth strategies[J]. Applied Soil Ecology,2007,37(1-2):95-105
[35] Bradford M A,Fierer N,Jackson R B,et al. Nonlinear root-derived carbon sequestration across a gradient of nitrogen and phosphorous deposition in experimental mesocosms[J]. Global Change Biology,2008,14(5):1113-1124
[36] Liu L,Greaver T L. A global perspective on belowground carbon dynamics under nitrogen enrichment[J]. Ecology Letters,2010,13(7):819-828
[37] Cusack D F,Torn M S,McDowell W H,et al. The response of heterotrophic activity and carbon cycling to nitrogen additions and warming in two tropical soils[J]. Global Change Biology,2010,16(9):2555-2572
[38] Phillips R P,Finzi A C,Bernhardt E S. Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under longterm CO₂ fumigation[J]. Ecology letters,2011,14(2)187-194
[39] 赵晓琛,皇甫超河,刘红梅,等. 贝加尔针茅草原土壤酶活性及微生物量碳氮对养分添加的响应[J]. 草地学报,2016,24(1):47-53
[40] Sinsabaugh R L. Phenol oxidase,peroxidase and organic matter dynamics of soil[J]. Soil Biology and Biochemistry,2010,42(3):391-404
[41] Waldrop M P,Zak D R,Sinsabaugh R L,et al. Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity[J]. Ecological Applications,2004,14(4):1172-1177
[42] Hobbie S E,Eddy W C,Buyarski C R,et al. Response of decomposing litter and its microbial community to multiple forms of nitrogen enrichment[J]. Ecological monographs,2012,82(3):389-405
[43] Talbot J M,Treseder K K. Interactions among lignin,cellulose,and nitrogen drive litter chemistry-decay relationships[J]. Ecology,2012,93(2):345-354
[44] Polacco J C. Is nickel a universal component of plant ureases?[J]. Plant Science Letters,1977,10(3):249-255
[45] Dunn R M,Mikola J,Bol R,et al. Influence of microbial activity on plant-microbial competition for organic and inorganic nitrogen[J]. Plant and Soil,2006,289(1-2):321-334
[46] Schimel J P,Weintraub M N. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil:a theoretical model[J]. Soil Biology and Biochemistry,2003,35(4):549-563
[47] Elser J J,Fagan W F,Kerkhoff A J,et al. Biological stoichiometry of plant production:metabolism,scaling and ecological response to global change[J]. New Phytologist,2010,186(3):593-608
[48] Penuelas J,Poulter B,Sardans J,et al. Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe[J]. Nature Communications,2013,4(1):1-10
[49] Cui Y,Fang L,Guo X,et al. Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern Loess Plateau,China[J]. Soil Biology and Biochemistry,2018(116):11-21
[50] Talbot J M,Martin F,Kohler A,et al. Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry[J]. Soil Biology and Biochemistry,2015(88):441-456
[51] Deng Q,Hui D,Dennis S,et al. Responses of terrestrial ecosystem phosphorus cycling to nitrogen addition:A meta-analysis[J]. Global Ecology and Biogeography,2017,26(6):713-728
[52] 王理德,王方琳,郭春秀,等. 土壤酶学硏究进展[J]. 土壤,2016,48(1):12-21
[53] Brown J H,Gillooly J F,Allen A P,et al. Toward a metabolic theory of ecology[J]. Ecology,2004,85(7):1771-1789
[54] Kuijken R P,Snel J H,Heddes M,et al. The importance of a sterile rhizosphere when phenotyping for root exudation[J]. Plant and Soil,2015,387(1-2):131-142
[55] 闫钟清,齐玉春,彭琴,等. 降水和氮沉降增加对草地土壤酶活性的影响[J]. 生态学报,2017,37(9):3019-3027
[56] Ligaba A,Shen H,Shibata K,et al. The role of phosphorus in aluminium induced citrate and malate exudation from rape (Brassica napus)[J]. Physiologia Plantarum,2004,120(4):575-584
[57] Ryan M H,Tibbett M,Edmonds-Tibbett T,et al. Carbon trading for phosphorus gain:the balance between rhizosphere carboxylates and arbuscular mycorrhizal symbiosis in plant phosphorus acquisition[J]. Plant,Cell and Environment,2012,35(12):2170-2180
[58] Ryan P R,James R A,Weligama C,et al. Can citrate efflux from roots improve phosphorus uptake by plants? Testing the hypothesis with near-isogenic lines of wheat[J]. Physiologia Plantarum,2014,151(3):230-242
[59] Herrera Paredes S,Gao T,Law T F,et al. Design of synthetic bacterial communities for predictable plant phenotypes[J]. PLoS Biology,2018,16(2):e2003962
[60] Trivedi P,Leach J E,Tringe S G,et al. Plant-microbiome interactions:from community assembly to plant health[J]. Nature Reviews Microbiology,2020(18):607-621

Responses of Soil Enzyme Activities to Nitrogen Addition and Its Impact Factors at the Alpine Steppe of Northern Tibet

藏北高寒草原土壤酶活性对氮添加的响应及其影响因素

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