Scientia Agricultura Sinica ›› 2025, Vol. 58 ›› Issue (13): 2604-2613.doi: 10.3864/j.issn.0578-1752.2025.13.009

• SOIL & FERTILIZER·WATER-SAVING IRRIGATION·AGROECOLOGY & ENVIRONMENT • Previous Articles     Next Articles

Soil Enzyme Activities and Their Stoichiometry Under Prolonged Rice Cultivation

ZHANG XinYao1,2(), WANG Ping1, LIU YaLong1(), WANG JingKuan1   

  1. 1 College of Land and Environment, Shenyang Agricultural University, Shenyang 110866
    2 Jilin Emergency Warning Information Dissemination Center, Changchun 130062
  • Received:2024-09-10 Accepted:2025-03-18 Online:2025-07-01 Published:2025-07-05

Abstract:

【Objective】 The theoretical evaluation of ecological stoichiometry of soil microbial metabolism and soil nutrient restriction in paddy soil was carried out, so as to provide the support for understanding the nutrient cycle of rice ecosystem. 【Method】 In this study, a chronosequence of paddy soils with 1 000 years was collected and analyzed soil enzyme activity and enzyme stoichiometry ratio with prolonged rice cultivation and clarified the influencing factors. 【Result】 The invertase activity increased with the chronosequence, while the activities of α-1,4-glucosidase, β-1,4-glucosidase, β-D-cellobiohydrolase and β-1,4-xylosidase enzymes decreased significantly at the early stage of chronosequence (50 years), and then increased significantly and remained stable. The dynamic of urease was similar to invertase, while the activities of n-acetyl-β-glucosaminidase were similar to most of the enzymes concerned in the carbon cycle. The C:N ratio of soil enzymes was the lowest at 1.28 when the soil was not cultivated (0 year), while the C:P and N:P ratios of soil enzymes were the highest at 1.77 and 1.38 at the same time, respectively. Generally, the C:N and C:P ratios of soil enzymes were all greater than 1 in all rice-growing years, while the N﹕P ratio of soil enzymes was less than 1 except for the uncultivated soil (0 year). 【Conclusion】 According to the comprehensive stoichiometric analysis (soil enzyme activity ratio, vector length and angle) could be seen that the soil microorganisms in the marsh before reclamation were mainly limited by carbon, while the soil microorganisms in the early stage (50 years) of rice cultivation after reclamation were mainly limited by phosphorus, and with the chronosequence, the soil microorganisms were changed to be limited by nitrogen. The research results could provide a theoretical basis for understanding the biogeochemical cycling mechanisms mediated by microorganisms in paddy ecosystems, as well as guiding soil nutrient management and ecological sustainable development.

Key words: soil enzyme, enzyme stoichiometry, paddy soil, soil chronosequence, soil development

Table 1

Soil physicochemical properties and elements stoichiometry"

植稻年限
Years of rice cultivation (a)
土壤有机碳
SOC (g·kg-1)
土壤全氮
TN (g·kg-1)
土壤全磷
TP (g·kg-1)
土壤酸碱度
pH
0 10.5±0.35c 1.15±0.03d 0.62±0.01d 7.83±0.09a
50 14.4±0.98b 1.58±0.08c 0.66±0.12cd 7.75±0.06a
100 19.2±2.15a 1.86±0.20b 0.78±0.02bc 6.93±0.20b
300 21.8±0.37a 2.33±0.01a 0.86±0.05b 6.20±0.43c
700 19.7±0.61a 1.95±0.04b 0.87±0.02b 5.96±0.08c
1000 20.9±1.57a 2.24±0.10a 1.20±0.04a 4.97±0.01d
植稻年限
Years of rice cultivation (a)
土壤碳氮比
Soil C:N
土壤碳磷比
Soil C:P
土壤氮磷比
Soil N:P
土壤黏粒含量
Clay content (%)
0 8.88±0.20c 17.37±0.70c 1.96±0.06c 9.92±0.54d
50 9.35±0.16b 24.05±4.99a 2.57±0.53ab 9.87±0.03d
100 10.30±0.06a 24.69±2.09a 2.40±0.20a 11.8±0.07c
300 9.58±0.17b 23.37±1.77a 2.46±0.15a 12.8±0.17b
700 10.16±0.09a 23.01±0.73a 2.26±0.07ab 15.5±0.17a
1000 9.71±0.37ab 20.19±0.67b 2.17±0.02b 15.9±0.29d

Fig. 1

Soil enzyme activities within paddy chronosequence CBH: β-cellobiohydrolase, XYL: β-xylosidase, AG: α-1,4-glucosidase, BG: β-1,4-glucosidase, INT: Invertase, UE: Urease, NAG: β-1,4-N- acetylglucos-aminidase, PHOS: Phosphatase. Different lowercase letters on the graph column indicate that there are significant differences in soil enzyme activities among different years of rice planting (P<0.05). The same as below"

Fig. 2

Natural logarithm of soil enzyme activity within paddy chronosequence"

Fig. 3

Stoichiometric ratio of soil enzyme activities within paddy chronosequence"

Fig. 4

Vector length and angle of soil enzyme stoichiometry with paddy chronosequence"

Table 2

The contribution rate soil physicochemical factors to soil enzyme activity and stoichiometric ratio"

土壤理化因子
Soil physicochemical factors
土壤酶活性 Soil enzyme activity 土壤酶化学计量比 Soil enzyme stoichiometric ratio
贡献率 Contribution (%) P P value 贡献率 Contribution (%) P P value
黏粒含量Clay 43.1 0.002 2.5 0.550
氮磷比N:P 25.0 0.028 47.6 0.010
总磷TP 7.8 0.232 16.7 0.134
酸碱度pH 7.7 0.226 15 0.092
碳磷比C:P 6.3 0.330 0.7 0.840
总有机碳SOC 5.8 0.382 10.5 0.194
碳氮比C:N 2.8 0.644 5.2 0.358
总氮TN 1.6 0.842 1.7 0.666

Fig. 5

Heat map of the relationship between soil enzyme activities and soil physicochemical factors * and ** represents a significance at 5% and 1% level, respectively"

[1]
SARDANS J, JANSSENS I A, CIAIS P, OBERSTEINER M, PEÑUELAS J. Recent advances and future research in ecological stoichiometry. Perspectives in Plant Ecology, Evolution and Systematics, 2021, 50: 125611.
[2]
张康, 李佳佳, 魏振浩, 樊妙春, 上官周平. 利用土壤化学计量学和酶计量学揭示刺槐林土壤微生物的养分限制状况. 应用生态学报, 2024, 35(7): 1799-1806.

doi: 10.13287/j.1001-9332.202407.004
ZHANG K, LI J J, WEI Z H, FAN M C, SHANGGUAN Z P. Revealing nutrient limitation status of microorganisms in the soil of Robinia pseudoacacia plantation through soil stoichiometry and enzyme metrology. Chinese Journal of Applied Ecology, 2024, 35(7): 1799-1806. (in Chinese)

doi: 10.13287/j.1001-9332.202407.004
[3]
CUI Y X, FANG L C, GUO X B, WANG X, ZHANG Y J, LI P F, ZHANG X C. Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern Loess Plateau, China. Soil Biology and Biochemistry, 2018, 116: 11-21.
[4]
朱长伟, 孟威威, 石柯, 牛润芝, 姜桂英, 申凤敏, 刘芳, 刘世亮. 不同轮耕模式下小麦各生育时期土壤养分及酶活性变化特征. 中国农业科学, 2022, 55(21): 4237-4251. doi: 10.3864/j.issn.0578-1752.2022.21.011.
ZHU C W, MENG W W, SHI K, NIU R Z, JIANG G Y, SHEN F M, LIU F, LIU S L. The characteristics of soil nutrients and soil enzyme activities during wheat growth stage under different tillage patterns. Scientia Agricultura Sinica, 2022, 55(21): 4237-4251. doi: 10.3864/j.issn.0578-1752.2022.21.011. (in Chinese)
[5]
SINSABAUGH R L, LAUBER C L, WEINTRAUB M N, AHMED B, ALLISON S D, CRENSHAW C, CONTOSTA A R, CUSACK D, FREY S, GALLO M E, GARTNER T B, HOBBIE S E, HOLLAND K, KEELER B L, POWERS J S, STURSOVA M, TAKACS-VESBACH C, WALDROP M P, WALLENSTEIN M D, ZAK D R, ZEGLIN L H. Stoichiometry of soil enzyme activity at global scale. Ecology Letters, 2008, 11(11): 1252-1264.

doi: 10.1111/j.1461-0248.2008.01245.x pmid: 18823393
[6]
SINSABAUGH R L, HILL B H, FOLLSTAD SHAH J J. Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature, 2009, 462(7274): 795-798.
[7]
SINSABAUGH R L, MANZONI S, MOORHEAD D L, RICHTER A. Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecology Letters, 2013, 16(7): 930-939.

doi: 10.1111/ele.12113 pmid: 23627730
[8]
LIU Y L, GE T D, VAN GROENIGEN K J, YANG Y H, WANG P, CHENG K, ZHU Z K, WANG J K, LI Y, GUGGENBERGER G, SARDANS J, PENUELAS J, WU J S, KUZYAKOV Y, Rice paddy soils are a quantitatively important carbon store according to a global synthesis. Communications Earth & Environment, 2021, 2: 154.
[9]
LIU Y L, GE , ZHU Z K, LIU S L, LUO Y, LI Y, WANG P, GAVRICHKOVA O, XU X L, WANG J K, WU J S, GUGGENBERGER G, KUZYAKOV Y. Carbon input and allocation by rice into paddy soils: A review. Soil Biology and Biochemistry, 2019, 133: 97-107.
[10]
邬佳玲, 魏亮, 祝贞科, 葛体达, 吴金水, 毛瑢. 碳和养分添加对亚热带稻田土壤酶活性化学计量学特征的影响. 土壤与作物, 2020, 9(3): 231-239.
WU J L, WEI L, ZHU Z K, GE , WU J S, MAO R. Effects of carbon and nutrient addition on soil enzyme activities and their stoichiometry in subtropical paddy soils. Soils and Crops, 2020, 9(3): 231-239. (in Chinese)
[11]
XIE Y N, OUYANG Y, HAN S, SE J, TANG S, YANG Y F, MA Q X, WU L H. Crop rotation stage has a greater effect than fertilisation on soil microbiome assembly and enzymatic stoichiometry. Science of the Total Environment, 2022, 815: 152956.
[12]
ZHU Z K, GE , LUO Y, LIU S L, XU X L, TONG C L, SHIBISTOVA O, GUGGENBERGER G, WU J S. Microbial stoichiometric flexibility regulates rice straw mineralization and its priming effect in paddy soil. Soil Biology and Biochemistry, 2018, 121: 67-76.
[13]
LIU Y L, DONG Y Q, GE , HUSSAIN Q, WANG P, WANG J K, LI Y, GUGGENBERGER G, WU J S. Impact of prolonged rice cultivation on coupling relationship among C, Fe, and Fe-reducing bacteria over a 1000-year paddy soil chronosequence. Biology and Fertility of Soils, 2019, 55(6): 589-602.
[14]
MOORHEAD D L, SINSABAUGH R L, HILL B H, WEINTRAUB M N. Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biology and Biochemistry, 2016, 93: 1-7.
[15]
SINSABAUGH R L, FOLLSTAD SHAH J J. Ecoenzymatic stoichiometry and ecological theory. Annual Review of Ecology, Evolution, and Systematics, 2012, 43: 313-343.
[16]
张露, 张水清, 任科宇, 李俊杰, 段英华, 徐明岗. 不同肥力潮土的酶活计量比特征及其与微生物量的关系. 中国农业科学, 2020, 53(20): 4226-4236. doi: 10.3864/j.issn.0578-1752.2020.20.011.
ZHANG L, ZHANG S Q, REN K Y, LI J J, DUAN Y H, XU M G. Soil ecoenzymatic stoichiometry and relationship with microbial biomass in fluvo-aquic soils with various fertilities. Scientia Agricultura Sinica, 2020, 53(20): 4226-4236. doi: 10.3864/j.issn.0578-z1752.2020.20.011. (in Chinese)
[17]
WU L P, MA H, ZHAO Q L, ZHANG S R, WEI W L, DING X D. Changes in soil bacterial community and enzyme activity under five years straw returning in paddy soil. European Journal of Soil Biology, 2020, 100: 103215.
[18]
吕波, 王宇函, 夏浩, 姚子涵, 姜存仓. 不同改良剂对黄棕壤和红壤上白菜生长及土壤肥力影响的差异. 中国农业科学, 2018, 51(22): 4306-4315. doi: 10.3864/j.issn.0578-1752.2018.22.009.
B, WANG Y H, XIA H, YAO Z H, JIANG C C. Effects of biochar and other amendments on the cabbage growth and soil fertility in yellow-brown soil and red soil. Scientia Agricultura Sinica, 2018, 51(22): 4306-4315. doi: 10.3864/j.issn.0578-1752.2018.22.009. (in Chinese)
[19]
刘彦伶, 李渝, 张雅蓉, 黄兴成, 朱华清, 杨叶华, 张萌, 蒋太明, 张文安. 长期施肥对黄壤稻田和旱地土壤磷酸酶活性的影响. 土壤通报, 2022, 53(4): 948-955.
LIU Y L, LI Y, ZHANG Y R, HUANG X C, ZHU H Q, YANG Y H, ZHANG M, JIANG T M, ZHANG W A. Effects of long-term fertilization on phosphatase activities in paddy and dryland of yellow soil. Chinese Journal of Soil Science, 2022, 53(4): 948-955. (in Chinese)
[20]
DAI X L, ZHOU W, LIU G R, LIANG G Q, HE P, LIU Z B. Soil C/N and pH together as a comprehensive indicator for evaluating the effects of organic substitution management in subtropical paddy fields after application of high-quality amendments. Geoderma, 2019, 337: 1116-1125.
[21]
HODGE A, CAMPBELL C D, FITTER A H. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature, 2001, 413(6853): 297-299.
[22]
吴金水, 葛体达, 胡亚军. 稻田土壤关键元素的生物地球化学耦合过程及其微生物调控机制. 生态学报, 2015, 35(20): 6626-6634.
WU J S, GE , HU Y J. A review on the coupling of bio- geochemical process for key elements and microbial regulation mechanisms in paddy rice ecosystems. Acta Ecologica Sinica, 2015, 35(20): 6626-6634. (in Chinese)
[23]
PENG X Q, WANG W. Stoichiometry of soil extracellular enzyme activity along a climatic transect in temperate grasslands of northern China. Soil Biology and Biochemistry, 2016, 98: 74-84.
[24]
ALLISON S D, VITOUSEK P M. Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biology and Biochemistry, 2005, 37(5): 937-944.
[25]
YANG Y, LIANG C, WANG Y Q, CHENG H, AN S S, CHANG S X. Soil extracellular enzyme stoichiometry reflects the shift from P- to N-limitation of microorganisms with grassland restoration. Soil Biology and Biochemistry, 2020, 149: 107928.
[26]
胡琛, 贺云龙, 黄金莲, 雷静品, 崔鸿侠, 唐万鹏, 马国飞. 神农架4种典型针叶人工林土壤酶活性及其生态化学计量特征. 林业科学研究, 2020, 33(4): 143-150.
HU C, HE Y L, HUANG J L, LEI J P, CUI H X, TANG W P, MA G F. Soil enzyme activity and its ecological stoichiometry in four typical coniferous planted forests in Shennongjia national nature reserve, China. Forest Research, 2020, 33(4): 143-150. (in Chinese)
[27]
吴际友, 叶道碧, 王旭军. 长沙市城郊森林土壤酶活性及其与土壤理化性质的相关性. 东北林业大学学报, 2010, 38(3): 97-99.
WU J Y, YE D B, WANG X J. Soil enzyme activity and its correlation with soil physical and chemical properties in suburban forests in Changsha City. Journal of Northeast Forestry University, 2010, 38(3): 97-99. (in Chinese)
[28]
HE Q Q, WU Y H, BING H J, ZHOU J, WANG J P. Vegetation type rather than climate modulates the variation in soil enzyme activities and stoichiometry in subalpine forests in the eastern Tibetan Plateau. Geoderma, 2020, 374: 114424.
[29]
董秀, 张燕, MUNYAMPIRWA Tito, 陶海宁, 沈禹颖. 长期保护性耕作对黄土高原旱作农田土壤碳含量及转化酶活性的影响. 中国农业科学, 2023, 56(5): 907-919. doi: 10.3864/j.issn.0578-1752.2023.05.008.
DONG X, ZHANG Y, MUNYAMPIRWA T, TAO H N, SHEN Y Y. Effects of long-term conservation tillage on soil carbon content and invertase activity in dry farmland on the Loess Plateau. Scientia Agricultura Sinica, 2023, 56(5): 907-919. doi: 10.3864/j.issn.0578-1752.2023.05.008. (in Chinese)
[30]
张海鑫, 曾全超, 安韶山, 王宝荣, 白雪娟. 子午岭典型植被凋落叶-土壤养分与酶活性特征. 生态学报, 2018, 38(7): 2262-2270.
ZHANG H X, ZENG Q C, AN S S, WANG B R, BAI X J. Soil enzyme activities, soil and leaf litter nutrients of typical vegetation in Ziwuling Mountain. Acta Ecologica Sinica, 2018, 38(7): 2262-2270. (in Chinese)
[31]
LI J J, ZHENG Y M, YAN J X, LI H J, HE J Z. Succession of plant and soil microbial communities with restoration of abandoned land in the Loess Plateau, China. Journal of Soils and Sediments, 2013, 13(4): 760-769.
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