Abstract
Aims
Stoichiometry of soil extracellular enzymes such as the ratios of carbon (C)‒, nitrogen (N)‒, and phosphorus (P)‒acquiring enzymes as well as their vector length and angle are used to reveal the biogeochemical equilibrium between microbial nutrient requirements and soil nutrient availability. However, the dynamics of soil extracellular enzymes activities and microbial N limitation following afforestation remain poorly understood in karst rocky desertification areas.
Methods
Soil samples were collected from Dodonaea viscosa plantations after 0, 10, 20, and 40 years of afforestation following the abandonment of croplands in a karst rocky desertification area, and a natural restored shrubland soil was served as the control. The activities of C, N, and P extracellular enzymes were measured and the stoichiometric and vector ratios of extracellular enzymes were calculated to quantify microbial nutrient limitation.
Results
The stoichiometric ratio of soil C: N:P acquisition enzymes was 0.63:1.48:1.0, with a vector angle of 34.7 in croplands, indicating high microbial N limitation. Compared to the croplands, D. viscosa afforestation significantly increased soil C‒, N‒, and P‒acquiring enzyme activities and gradually increased C: N:P stoichiometric ratio and vector angle to 0.75:1.39:1–0.76:1.17:1 and 34.9–38.2, respectively, indicating that afforestation alleviated microbial N limitation. Furthermore, gross N mineralization and gross ammonium immobilization rates increased by 140‒278% and 340‒801% following afforestation due to the increase in soil organic C and total N contents and the > 2 mm soil aggregates. The vector angle positively correlated with β‒N‒acetylglucosaminidase activity, gross N mineralization, and gross ammonium immobilization. Notably, the vector angle of extracellular enzymes following 40‒year afforestation was still 6.63% lower than that of the shrubland soil.
Conclusion
Our results suggested that afforestation could substantially increase gross N mineralization through stimulating β‒N‒acetylglucosaminidase activity and gross ammonium immobilization, thereby reducing microbial N limitation. However, this limitation persists even following long‒term afforestation in karst rocky desertification areas.
Research highlights
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Afforestation improves soil structure and increases organic matter content.
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Afforestation stimulates the activities of soil C‒, N‒, and P‒acquiring enzymes.
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Afforestation increases gross N mineralization and NH4+ immobilization rates.
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Afforestation alleviates soil microbial N limitation in subtropical karst areas.
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Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Araujo ASF, Bonifacio A, Pereira APA, Medeiros EV, Araujo FF, Mendes LW (2022) Enzymatic stoichiometry in soils from physiognomies of Brazilian Cerrado. J Soil Sci Plant Nutr 22:2735–2742. https://doi.org/10.1007/s42729-022-00840-w
Bell CW, Fricks BE, Rocca JD, Steinweg JM, McMahon SK, Wallenstein MD (2013) High–throughput fluorometric measurement of potential soil extracellular enzyme activities. J Vis Exp 81:e50961. https://doi.org/10.3791/50961
Bremner JM, Keeney DR (1966) Determination and isotope–ratio analysis of different forms of nitrogen in soils: 3. Exchangeable ammonium, nitrate, and nitrite by extraction–distillation methods. Soil Sci Soc Am J 30:577–582. https://doi.org/10.2136/sssaj1966.03615995003000050015x
Chen H, Li DJ, Xiao KC, Wang KL (2018) Soil microbial processes and resource limitation in karst and non–karst forests. Funct Ecol 32(5):1400–1409. https://doi.org/10.1111/1365-2435.13069
Cui YX, Moorhead DL, Guo XB, Peng SS, Wang YQ, Zhang XC, Fang LC (2021) Stoichiometric models of microbial metabolic limitation in soil systems. Global Ecol Biogeogr 30:2297–2311. https://doi.org/10.1111/geb.13378
Darby BA, Goodale CL, Chin NA, Fuss CB, Lang AK, Ollinger SV, Lovett GM (2020) Depth patterns and connections between gross nitrogen cycling and soil exoenzyme activities in three northern hardwood forests. Soil Biol Biochem 147:107836. https://doi.org/10.1016/j.soilbio.2020.107836
Elrys AS, Ali A, Zhang HM, Cheng Y, Zhang JB, Cai ZC, Müller C, Chang SX (2021a) Patterns and drivers of global gross nitrogen mineralization in soils. Glob Change Biol 27(22):5950–5962. https://doi.org/10.1111/gcb.15851
Elrys AS, Wang J, Metwally MAS, Cheng Y, Zhang JB, Cai ZC, Chang SX, Müller C (2021b) Global gross nitrification rates are dominantly driven by soil carbon–to–nitrogen stoichiometry and total nitrogen. Glob Change Biol 27(24):6512–6524. https://doi.org/10.1111/gcb.15883
Feng J, Wu JJ, Zhang Q, Zhang DD, Li QX, Long CY, Yang F, Chen Q, Cheng XL (2018) Stimulation of nitrogen–hydrolyzing enzymes in soil aggregates mitigates nitrogen constraint for carbon sequestration following afforestation in subtropical China. Soil Biol Biochem 123:136–144. https://doi.org/10.1016/j.soilbio.2018.05.013
Feyissa A, Gurmesa GA, Yang F, Long CY, Zhang Q, Cheng XL (2022) Soil enzyme activity and stoichiometry in secondary grasslands along a climatic gradient of subtropical China. Sci Total Environ 825:154019. https://doi.org/10.1016/j.scitotenv.2022.154019
Feyissa A, Yang F, Wu JJ, Chen Q, Zhang DD, Cheng XL (2021) Soil nitrogen dynamics at a regional scale along a precipitation gradient in secondary grassland of China. Sci Total Environ 781:146736. https://doi.org/10.1016/j.scitotenv.2021.146736
Filho ADC, Inda AV, Fink JR, Curi N (2015) Iron oxides in soils of different lithological origins in Ferriferous Quadrilateral (Minas Gerais, Brazil). Appl Clay Sci 118:1–7. https://doi.org/10.1016/j.clay.2015.08.037
Gao L, Smith AR, Jones DL, Guo YF, Liu BD, Guo ZL, Fan CN, Zheng JP, Cui XY, Hill PW (2023) How do tree species with different successional stages affect soil organic nitrogen transformations? Geoderma 430:116319. https://doi.org/10.1016/j.geoderma.2022.116319
Garousi F, Shan ZJ, Ni K, Yang H, Shan J, Cao JH, Jiang ZC, Yang JL, Zhu TB, Müller C (2021) Decreased inorganic N supply capacity and turnover in calcareous soil under degraded rubber plantation in the tropical karst region. Geoderma 381:114754. https://doi.org/10.1016/j.geoderma.2020.114754
Geisseler D, Horwath WR, Joergensen RG, Ludwig B (2010) Pathways of nitrogen utilization by soil microorganisms–A review. Soil Biol Biochem 42(12):2058–2067. https://doi.org/10.1016/j.soilbio.2010.08.021
Giller KE, Witter E, Mcgrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414. https://doi.org/10.1016/S0038-0717(97)00270-8
Goldscheider N, Chen Z, Auler AS, Bakalowicz M, Broda S, Drew D, Hartmann J, Jiang GH, Moosdorf N, Stevanovic Z (2020) Global distribution of carbonate rocks and karst water resources. Hydrogeol J 28:1661–1677. https://doi.org/10.1007/s10040-020-02139-5
Green SM, Dungait JA, Tu CL, Buss HL, Sanderson N, Hawkes SJ, Xing KX, Yue FJ, Hussey VL, Peng J (2019) Soil functions and ecosystem services research in the Chinese karst critical zone. Chem Geol 527:119107. https://doi.org/10.1016/j.chemgeo.2019.03.018
Guan HL, Fan JW, Lu X (2022) Soil specific enzyme stoichiometry reflects nitrogen limitation of microorganisms under different types of vegetation restoration in the karst areas. Appl Soil Ecol 169:104253. https://doi.org/10.1016/j.apsoil.2021.104253
Guo ZM, Zhang XY, Green SM, Dungait JAJ, Wen XF, Quine TA (2019) Soil enzyme activity and stoichiometry along a gradient of vegetation restoration at the Karst Critical Zone Observatory in Southwest China. Land Degrad Dev 30(16):1916–1927. https://doi.org/10.1002/ldr.3389
Hao TX, Zhang YY, Zhang JB, Müller C, Li KH, Zhang KP, Chu HY, Stevens C, Liu XJ (2020) Chronic nitrogen addition differentially affects gross nitrogen transformations in alpine and temperate grassland soils. Soil Biol Biochem 149:107962. https://doi.org/10.1016/j.soilbio.2020.107962
İlay R, Kavdir Y (2018) Impact of land cover types on soil aggregate stability and erodibility. Environ Monit Assess 190:1–14. https://doi.org/10.1007/s10661-018-6847-4
IUSS Working Group WRB (2014) World reference base for soil resources 2014. International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106. FAO, Rome. http://www.fao.org/soils-portal/soil-survey/soil-classification/world-reference-base/en/
Jiang ZC, Lian YQ, Qin XQ (2014) Rocky desertification in Southwest China: impacts, causes, and restoration. Earth Sci Rev 132:1–12. https://doi.org/10.1016/j.earscirev.2014.01.005
Jiang XJ, Xin XP, Li SW, Zhou JC, Zhu TB, Müller C, Cai ZC, Wright AL (2015) Effects of Fe oxide on N transformations in subtropical acid soils. Sci Rep 5:8615. https://doi.org/10.1038/srep08615
Kaiser K, Guggenberger G (2003) Mineral surfaces and soil organic matter. Eur J Soil Sci 54:219–236. https://doi.org/10.1046/j.1365-2389.2003.00544.x
Lasota J, Małek S, Jasik M, Błońska E (2021) Effect of planting method on C:N:P stoichiometry in soils, young silver fir (Abies alba Mill.) And stone pine (Pinus cembra L.) in the upper mountain zone of Karpaty Mountains. Ecol Indic 129:107905. https://doi.org/10.1016/j.ecolind.2021.107905
Li DJ, Liu J, Chen H, Zheng L, Wang KL (2018) Soil gross nitrogen transformations in responses to land use conversion in a subtropical karst region. J Environ Manage 212:1–7. https://doi.org/10.1016/j.jenvman.2018.01.084
Li DJ, Yang Y, Chen H, Xiao KC, Song TQ, Wang KL (2017) Soil gross nitrogen transformations in typical karst and nonkarst forests, southwest China. J Geophys Res Biogeo 122:2831–2840. https://doi.org/10.1002/2017JG003850
Lu C, Zhu Q, Qiu MH, Fan XH, Luo J, Liang YH, Ma Y (2023) Effects of different soil water holding capacities on vegetable residue return and its microbiological mechanism. Front Microbiol 14. https://doi.org/10.3389/fmicb.2023.1257258
Mason RE, Craine JM, Lany NK, Jonard M, Ollinger SV, Groffman PM, Fulweiler RW, Angerer J, Read QD, Reich PB (2022) Evidence, causes, and consequences of declining nitrogen availability in terrestrial ecosystems. Science 376:eabh3767. https://doi.org/10.1126/science.abh3767
Moorhead DL, Rinkes ZL, Sinsabaugh RL, Weintraub MN (2013) Dynamic relationships between microbial biomass, respiration, inorganic nutrients and enzyme activities: informing enzyme–based decomposition models. Front Microbiol 4:223. https://doi.org/10.3389/fmicb.2013.00223
Moorhead DL, Sinsabaugh RL, Hill BH, Weintraub MN (2016) Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biol Biochem 93:1–7. https://doi.org/10.1016/j.soilbio.2015.10.019
Müeller C, Rütting T, Kattge J, Laughlin RJ, Stevens RJ (2007) Estimation of parameters in complex 15N tracing models by Monte Carlo sampling. Soil Biol Biochem 39(3):715–726. https://doi.org/10.1016/j.soilbio.2006.09.021
Müller C, Clough TJ (2013) Advances in understanding nitrogen flows and transformations: gaps and research pathways. J Agr Sci 152:34–44. https://doi.org/10.1017/S0021859613000610
Parsapour MK, Kooch Y, Hosseini SM, Alavi SJ (2018) C and N cycle monitoring under Quercus Castaneifolia plantation. For Ecol Manag 427:26–36. https://doi.org/10.1016/j.foreco.2018.05.060
Priha O, Smolander A (1999) Nitrogen transformations in soil under Pinus sylvestris, Picea abies and Betula pendula at two forest sites. Soil Biol Biochem 31(7):965–977. https://doi.org/10.1016/S0038-0717(99)00006-1
Rani MS, Pippalla RS, Mohan K (2009) Dodonaea viscosa Linn.–an overview. Asian J Pharm Res He 1:97–112
Rosinger C, Rousk J, Sandén H (2019) Can enzymatic stoichiometry be used to determine growth–limiting nutrients for microorganisms? A critical assessment in two subtropical soils. Soil Biol Biochem 128:115–126. https://doi.org/10.1016/j.soilbio.2018.10.011
Ross DS, Ketterings Q (1995) Recommended methods for determining soil cation exchange capacity. Recommended soil test procedures Northeastern United States 493:62
Rowley MC, Grand S, Verrecchia ÉP (2018) Calcium–mediated stabilisation of soil organic carbon. Biogeochemistry 137:27–49. https://doi.org/10.1007/s10533-017-0410-1
Rütting T, Cizungu Ntaboba L, Roobroeck D, Bauters M, Huygens D, Boeckx P (2015) Leaky nitrogen cycle in pristine African montane rainforest soil. Global Biogeochem Cy 29:1754–1762. https://doi.org/10.1002/2015GB005144
Shabtai IA, Wilhelm RC, Schweizer SA, Höschen C, Buckley DH, Lehmann J (2023) Calcium promotes persistent soil organic matter by altering microbial transformation of plant litter. Nat Commun 14:6609. https://doi.org/10.1038/s41467-023-42291-6
Siebielec S, Siebielec G, Klimkowicz–Pawlas A, Gałązka A, Grządziel J, Stuczyński T (2020) Impact of water stress on microbial community and activity in sandy and loamy soils. Agronomy 10:1429. https://doi.org/10.3390/agronomy10091429
Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798. https://doi.org/10.1038/nature08632
Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11(11):1252–1264. https://doi.org/10.1111/j.1461-0248.2008.01245.x
Six J, Elliott ET, Paustian K, Doran JW (1998) Aggregation and soil organic matter accumulation in cultivated and native grassland soils. Soil Sci Soc Am J 62(5):1367–1377. https://doi.org/10.2136/sssaj1998.03615995006200050032x
Song M, He TG, Chen H, Wang KL, Li DJ (2019) Dynamics of soil gross nitrogen transformations during post–agricultural succession in a subtropical karst region. Geoderma 341:1–9. https://doi.org/10.1016/j.geoderma.2019.01.034
Tisdall JM, Oades JM (1982) Organic matter and water–stable aggregates in soils. Eur J Soil Sci 33:141–163. https://doi.org/10.1111/j.1365-2389.1982.tb01755.x
Tong XW, Brandt M, Yue YM, Ciais P, Jepsen MR, Penuelas J, Wigneron JP, Xiao XX, Song XP, Horion S, Rasmussen K, Saatchi S, Fan L, Wang KL, Zhang B, Chen ZC, Wang YH, Li XJ, Fensholt R (2020) Forest management in southern China generates short term extensive carbon sequestration. Nat Commun 11:129. https://doi.org/10.1038/s41467-019-13798-8
Tong XW, Brandt M, Yue YM, Horion S, Wang KL, Keersmaecker WD, Tian F, Schurgers G, Xiao XM, Luo YQ (2018) Increased vegetation growth and carbon stock in China karst via ecological engineering. Nat Sustain 1:44–50. https://doi.org/10.1038/s41893-017-0004-x
Varsadiya M, Liebmann P, Petters S, Hugelius G, Urich T, Guggenberger G, Bárta J (2022) Extracellular enzyme ratios reveal locality and horizon–specific carbon, nitrogen, and phosphorus limitations in Arctic permafrost soils. Biogeochemistry 161:101–117. https://doi.org/10.1007/s10533-022-00967-z
Wang GZ, Tang GY, Pang DB, Liu YG, Wan L, Zhou JX (2021a) Plant interactions control the carbon distribution of Dodonaea viscosa in karst regions. PLoS ONE 16:e0260337. https://doi.org/10.1371/journal.pone.0260337
Wang QT, Chen LY, Xu H, Ren KX, Xu ZG, Tang Y, Xiao J (2021b) The effects of warming on root exudation and associated soil N transformation depend on soil nutrient availability. Rhizosphere 17:100263. https://doi.org/10.1016/j.rhisph.2020.100263
Wang KL, Zhang CH, Chen HS, Yue YM, Zhang W, Zhang MY, Qi XK, Fu ZY (2019) Karst landscapes of China: patterns, ecosystem processes and services. Landsc Ecol 34:2743–2763. https://doi.org/10.1007/s10980-019-00912-w
Waring BG, Weintraub SR, Sinsabaugh RL (2014) Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117:101–113. https://doi.org/10.1007/s10533-013-9849-x
Wei XR, Li XZ, Jia XX, Shao MG (2013) Accumulation of soil organic carbon in aggregates after afforestation on abandoned farmland. Biol Fert Soils 49:637–646. https://doi.org/10.1007/s00374-012-0754-6
Wen L, Li DJ, Yang LQ, Luo P, Chen H, Xiao KC, Song TQ, Zhang W, He XY, Chen HS (2016) Rapid recuperation of soil nitrogen following agricultural abandonment in a karst area, southwest China. Biogeochemistry 129:341–354. https://doi.org/10.1007/s10533-016-0235-3
Wu Y, Chen WJ, Li Q, Guo ZQ, Li YZ, Zhao ZW, Zhai JY, Liu GB, Xue S (2021) Ecoenzymatic stoichiometry and nutrient limitation under a natural secondary succession of vegetation on the Loess Plateau, China. Land Degrad Dev 32(1):399–409. https://doi.org/10.1002/ldr.3723
Xie Y, Yang L, Zhu TB, Yang H, Zhang JB, Yang JL, Cao JH, Bai B, Jiang ZC, Liang YM (2018) Rapid recovery of nitrogen retention capacity in a subtropical acidic soil following afforestation. Soil Biol Biochem 120:171–180. https://doi.org/10.1016/j.soilbio.2018.02.008
Yang ST, Yang L, Wen DN, Liu LJ, Ni K, Cao JH, Zhu TB, Müller C (2023) Soil calcium constrains nitrogen mineralization and nitrification rates in subtropical karst regions. Soil Biol Biochem 186:109176. https://doi.org/10.1016/j.soilbio.2023.109176
Zhang JB, Cai ZC, Zhu TB, Yang WY, Müller C (2013) Mechanisms for the retention of inorganic N in acidic forest soils of southern China. Sci Rep 3:2342. https://doi.org/10.1038/srep02342
Zhang CH, Qi XK, Wang KL, Zhang MY, Yue YM (2017) The application of geospatial techniques in monitoring karst vegetation recovery in southwest China: a review. Prog Phys Geog 41(4):450–477. https://doi.org/10.1177/0309133317714246
Zhu ZH, Du H, Gao K, Fang YT, Wang KL, Zhu TB, Zhu J, Cheng Y, Li DJ (2023) Plant species diversity enhances soil gross nitrogen transformations in a subtropical forest, southwest China. J Appl Ecol. https://doi.org/10.1111/1365-2664.14407
Zhu TB, Zeng SM, Qin HL, Zhou KX, Yang H, Lan FN, Huang F, Cao JH, Müller C (2016) Low nitrate retention capacity in calcareous soil under woodland in the karst region of southwestern China. Soil Biol Biochem 97:99–101. https://doi.org/10.1016/j.soilbio.2016.03.001
Zuccarini P, Asensio D, Ogaya R, Sardans J, Peñuelas J (2020) Effects of seasonal and decadal warming on soil enzymatic activity in a P–deficient Mediterranean shrubland. Glob Change Biol 26(6):3698–3714. https://doi.org/10.1111/gcb.15077
Acknowledgements
We extend our appreciation to the reviewers for their time in reviewing our manuscript and providing clear and insightful suggestions, as well as their valuable contribution to improving the scientific quality of our manuscript.
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This research was supported by the National Natural Science Foundation of China (42177243), the Guangxi Science and Technology Planning Project, China (2023GXNSFFA026010), the Guilin Scientific Research and Technology Development Project, China (2020010905), the Natural Resource Science and Technology Strategic Research Project, China (2023-ZL-03), the Geological Survey Project, China (DD20240095) and the Guangxi Bagui Scholarship Program to Dejun Li.
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Lijun Liu: Writing‒original draft, Investigation, Formal analysis. Qilin Zhu: Software, Writing‒review & editing. Dongni Wen: Investigation. Lin Yang: Investigation. Kang Ni: Investigation. Xingliang Xu: Writing‒review & editing. Jianhua Cao: Investigation, Methodology. Lei Meng: Investigation, Methodology. Jinling Yang: Investigation, Methodology. Jinxing Zhou: Investigation, Methodology. Tongbin Zhu: Conceptualization, Writing‒review & editing, Funding acquisition. Christoph Müller: Methodology.
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Liu, L., Zhu, Q., Wen, D. et al. Stimulation of organic N mineralization by N‒acquiring enzyme activity alleviates soil microbial N limitation following afforestation in subtropical karst areas. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06668-w
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DOI: https://doi.org/10.1007/s11104-024-06668-w