Abstract
Aims
Tree species mixing is an essential measure used to increase soil carbon (C) sinks and enhance nutrient cycling, while enzyme catalysis is the rate-limiting step of soil C mineralization and nutrient release. The study aimed to determine how mixing affects soil C and nitrogen (N) hydrolases kinetics in subtropical plantations.
Methods
The topsoil (0–15 cm) and subsoil (45–60 cm) from two monoculture coniferous plantations and two mixed plantations formed by replanting broad-leaved trees in the two coniferous plantations were collected to analyze the maximum activity (Vmax), half-saturation constant (Km) and catalytic efficiency (Vmax/Km) of four hydrolases involved in C (β-glucosidase, BG; cellobioside, CB) and N (β-N-acetylglucosaminidase, NAG; leucine aminopeptidase, LAP) cycling.
Results
Mixing decreased the Vmax of BG but increased the Vmax of NAG in the topsoil, indicating the differential response of C and N enzyme activities to mixing. The Km of NAG and LAP increased, while the Vmax/Km of CB and NAG decreased after mixing in the topsoil. Mixing decreased the Vmax of CB and NAG and the Vmax/Km of BG and CB in the subsoil. The Vmax/Km values of C and N hydrolases were negatively correlated with SOC, total N and mineral N and positively correlated with the aromatic/aliphatic compound ratio, which illustrated that the hydrolases kinetics were mediated by changes in soil quality.
Conclusion
Mixing decreased the catalytic efficiency of soil C and N hydrolases in subtropical plantations, although the mixing effect on soil hydrolase kinetic parameters depended on the enzyme type and soil depth.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The data are available from the corresponding author on reasonable request.
References
Allison SD, Romero-Olivares AL, Lu Y, Taylor JW, Treseder KK (2018) Temperature sensitivities of extracellular enzyme V. and K(m) across thermal environments. Glob Change Biol 24:2884–2897. https://doi.org/10.1111/gcb.14045
Alves RJE, Callejas IA, Marschmann GL, Mooshammer M, Singh HW, Whitney B, Torn MS, Brodie EL (2021) Kinetic properties of microbial exoenzymes vary with soil depth but havesimilar temperature sensitivities through the soil profile. Front Microbiol 12:735282. https://doi.org/10.3389/fmicb.2021.735282
Bayranvand M, Akbarinia M, Salehi Jouzani G, Gharechahi J, Baldrian P (2021) Distribution of soil extracellular enzymatic, microbial, and biological functions in the C and N-cycle pathways along a forest altitudinal gradient. Front Microbiol 12:660603. https://doi.org/10.3389/fmicb.2021.660603
Bornemann L, Welp G, Amelung W (2010) Particulate organic matter at the field scale: rapid acquisition using mid infrared spectroscopy. Soil Sci Soc Am 74:1147–1156. https://doi.org/10.2136/sssaj2009.0195
Calderón F, Haddix M, Conant R, Magrini Bair K, Paul E (2013) Diffuse reflectance Fourier transform mid infrared spectroscopy as a method of characterizing changes in soil organic matter. Soil Biol Biochem 77:1591–1600. https://doi.org/10.2136/sssaj2013.04.0131
Chen J, Sinsabaugh RL (2021) Linking microbial functional gene abundance and soil extracellular enzyme activity: implications for soil carbon dynamics. Glob Change Biol 27:1322–1325. https://doi.org/10.1111/gcb.15506
Chen FL, Zheng H, Yang BS, Ouyang ZY, Zhang K, Xiao Y, Tu NM (2011) The decomposition of coniferous and broadleaf mixed litters significantly changes the carbon metabolism diversity of soil microbial communities in subtropical area, southern China. Acta Ecol Sin 31:3027–3035
Cui Y, Fang L, Guo X, Wang X, Zhang Y, Li P, Zhang X (2018) Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern Loess Plateau, China. Soil Biol Biochem 116:11–21. https://doi.org/10.1016/j.soilbio.2017.09.025
Dietterich LH, Bouskill NJ, Brown M, Castro B, Chacon SS, Colburn L, Cordeiro AL, García EH, Gordon AA, Gordon E, Dietterich LH, Bouskill NJ, Brown M, Castro B, Chacon SS, Colburn L, Cordeiro AL, García EH, Gordon AA, Gordon E, Hedgpeth A, Konwent W, Oppler G, Reu J, Tsiames C, Valdes E, Zeko A, Cusack DF (2022) Effects of experimental and seasonal drying on soil microbial biomass and nutrient cycling in four lowland tropical forests. Biogeochemistry 161:227–250. https://doi.org/10.1007/s10533-022-00980-2
Dove NC, Arogyaswamy K, Billings SA, Botthoff JK, Carey CJ, Cisco C, DeForest JL, Fairbanks D, Fierer N, Gallery RE, Kaye JP, Lohse KA, Maltz MR, Mayorga E, Pett-Ridge J, Yang WH, Hart SC, Aronson EL (2020) Continental-scale patterns of extracellular enzyme activity in the subsoil: an overlooked reservoir of microbial activity. Environ Res Lett 15:1040a1. https://doi.org/10.1088/1748-9326/abb0b3
Dove NC, Torn MS, Hart SC, Taş N (2021) Metabolic capabilities mute positive response to direct and indirect impacts of warming throughout the soil profile. Nat Commun 12:2089. https://doi.org/10.1038/s41467-021-22408-5
Dungait JA, Hopkins DW, Gregory AS, Whitmore AP (2012) Soil organic matter turnover is governed by accessibility not recalcitrance. Glob Change Biol 18:1781–1796. https://doi.org/10.1111/j.1365-2486.2012.02665.x
Fang XM, Chen FS, Wan SZ, Yang QP, Shi JM (2015) Topsoil and deep soil organic carbon concentration and stability vary with aggregate size and vegetation type in subtropical China. PLoS ONE 10:e0139380. https://doi.org/10.1371/journal.pone.0139380
Feng J, Wei K, Chen Z, Lü X, Tian J, Wang C, Chen L (2019) Coupling and decoupling of soil carbon and nutrient cycles across an aridity gradient in the drylands of northern China: evidence from ecoenzymatic stoichiometry. Global Biogeochem Cy 33:559–569. https://doi.org/10.1029/2018gb006112
Garau G, Morillas L, Roales J, Castaldi P, Mangia NP, Spano D, Mereu S (2019) Effect of monospecific and mixed Mediterranean tree plantations on soil microbial community and biochemical functioning. Appl Soil Ecol 140:78–88. https://doi.org/10.1016/j.apsoil.2019.04.005
Gillespie LM, Hättenschwiler S, Milcu A, Wambsganss J, Shihan A, Fromin N (2021) Tree species mixing affects soil microbial functioning indirectly via root and litter traits and soil parameters in european forests. Funct Ecol 35:2190–2204. https://doi.org/10.1111/1365-2435.13877
Guo J, Feng H, McNie P, Liu Q, Xu X, Pan C, Yan K, Feng L, Adehanom Goitom E, Yu Y (2023) Species mixing improves soil properties and enzymatic activities in chinese fir plantations: a meta-analysis. CATENA 220:106723. https://doi.org/10.1016/j.catena.2022.106723
Huang YX, Wu ZJ, Zong YY, Li WQ, Chen FS, Wang GG, Li JJ, Fang XM (2022) Mixing with coniferous tree species alleviates rhizosphere soil phosphorus limitation of broad-leaved trees in subtropical plantations. Soil Biol Biochem 175:108853. https://doi.org/10.1016/j.soilbio.2022.108853
Karhu K, Hilasvuori E, Fritze H, Biasi C, Nykänen H, Liski J, Vanhala P, Heinonsalo J, Pumpanen J (2016) Priming effect increases with depth in a boreal forest soil. Soil Biol Biochem 99:104–107. https://doi.org/10.1016/j.soilbio.2016.05.001
Li WQ, Huang YX, Chen FS, Liu YQ, Lin XF, Zong YY, Wu GY, Yu ZR, Fang XM (2021) Mixing with broad leaved trees shapes the rhizosphere soil fungal communities of coniferous tree species in subtropical forests. For Ecol Manag 480:118664. https://doi.org/10.1016/j.foreco.2020.118664
Li WQ, Wu ZJ, Zong YY, Wang GG, Chen FS, Liu YQ, Li JJ, Fang XM (2022) Tree species mixing enhances rhizosphere soil organic carbon mineralization of conifers in subtropical plantations. For Ecol Manag 516:120238. https://doi.org/10.1016/j.foreco.2022.120238
Liu W, Tian R, Peng Z, Yang S, X Liu, Yang Y, Zhang W, Liu L (2020) Nonlinear responses of the Vmax and Km of hydrolytic and polyphenol oxidative enzymes to nitrogen enrichment. Soil Biol Biochem 141:107656. https://doi.org/10.1016/j.soilbio.2019.107656
Loeppmann S, Blagodatskaya E, Pausch J, Kuzyakov Y (2016) Enzyme properties down the soil profile A matter of substrate quality in rhizosphere and detritusphere. Soil Biol Biochem 103:274–283. https://doi.org/10.1016/j.soilbio.2016.08.023
Margenot AJ, Calderón FJ, Bowles TM, Parikh SJ, Jackson LE (2015) Soil organic matter functional group composition in relation to organic carbon, nitrogen, and phosphorus fractions in organically managed tomato fields. Soil Sci Soc Am J 79:772–782. https://doi.org/10.2136/sssaj2015.02.0070
Margenot AJ, Calderón FJ, Parikh SJ (2016) Limitations and potential of spectral subtractions in Fourier transform infrared spectroscopy of soil samples. Soil Sci Soc Am J 80:10–26. https://doi.org/10.2136/sssaj2015.06.0228
Maxwell TL, Augusto L, Bon L, Courbineau A, Altinalmazis-Kondylis A, Milin S, Bakker MR, Jactel H, Fanin N (2020) Effect of a tree mixture and water availability on soil nutrients and extracellular enzyme activities along the soil profile in an experimental forest. Soil Biol Biochem 148:107864. https://doi.org/10.1016/j.soilbio.2020.107864
Mayer M, Prescott CE, Abaker WEA, Augusto L, Cécillon L, Ferreira GWD, James J, Jandl R, Katzensteiner K, Laclau J-P, Laganière J, Nouvellon Y, Paré D, Stanturf JA, Vanguelova EI, Vesterdal L (2020) Influence of forest management activities on soil organic carbon stocks: a knowledge synthesis. For Ecol Manag 466:118127. https://doi.org/10.1016/j.foreco.2020.118127
Mori T, Aoyagi R, Kitayama K, Mo J (2021) Does the ratio of β-1,4-glucosidase to β-1,4-N-acetylglucosaminidase indicate the relative resource allocation of soil microbes to C and N acquisition? Soil Biol Biochem 160:108363. https://doi.org/10.1016/j.soilbio.2021.108363
Ni X, Ning C, Yan W, Liu Z, Chen Y, Ning X (2017) Soil nutrients status of masson pine and slash pine plantations in Guizhou Longli forest farm. J Cent South Univ For Technol 37:49–56. https://doi.org/10.14067/j.cnki.1673-923x.2017.09.009
Paul KI, Polglase PJ, Nyakuengama JG, Khanna PK (2002) Change in soil carbon following afforestation. For Ecol Manag 168:241–257. https://doi.org/10.1016/j.soilbio.2021.108363
Rai P, Shukla G, Manohar KA, Bhat JA, Kumar A, Kumar M, Cabral Pinto M, Chakravarty S (2021) Carbon storage of single tree and mixed tree dominant species stands in a reserve forest case study of the eastern sub Himalayan Region of India. Land 10:435. https://doi.org/10.3390/land10040435
Salome C, Nunan N, Pouteau V, Lerch TZ, Chenu C (2010) Carbon dynamics in topsoil and in subsoil may be controlled by different regulatory mechanisms. Glob Change Biol 16:416–426. https://doi.org/10.1111/j.1365-2486.2009.01884.x
Schnecker J, Wild B, Takriti M, Eloy Alves RJ, Gentsch N, Gittel A, Hofer A, Klaus K, Knoltsch A, Lashchinskiy N, Mikutta R, Richter A (2015) Microbial community composition shapes enzyme patterns in topsoil and subsoil horizons along a latitudinal transect in western Siberia. Soil Biol Biochem 83:106–115. https://doi.org/10.1016/j.soilbio.2015.01.016
Sinsabaugh RL, Belnap J, Findlay SG, Shah JJF, Hill BH, Kuehn KA, Kuske CR, Litvak ME, Martinez NG, Moorhead DL, Warnock DD (2014) Extracellular enzyme kinetics scale with resource availability. Biogeochemistry 121:287–304. https://doi.org/10.1007/s10533-014-0030-y
Stone M, DeForest J, Plante A (2014) Changes in extracellular enzyme activity and microbial community structure with soil depth at the Luquillo critical zone observatory. Soil Biol Biochem 75:237–247. https://doi.org/10.1016/j.soilbio.2014.04.017
Stone MM, Kan J, Plante AF (2015) Parent material and vegetation influence bacterial community structure and nitrogen functional genes along deep tropical soil profiles at the Luquillo critical zone observatory. Soil Biol Biochem 80:273–282. https://doi.org/10.1016/j.soilbio.2014.10.019
Stone MM, Plante AF (2014) Changes in phosphatase kinetics with soil depth across a variable tropical landscape. Soil Biol Biochem 71:61–67. https://doi.org/10.1016/j.soilbio.2014.01.006
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. Glob Change Biol 18:1173–1184. https://doi.org/10.1111/j.1365-2486.2011.02545.x
Tan X, Machmuller MB, Huang F, He J, Chen J, Cotrufo MF, Shen W (2020) Temperature sensitivity of ecoenzyme kinetics driving litter decomposition: the effects of nitrogen enrichment, litter chemistry, and decomposer community. Soil Biol Biochem 148:107878. https://doi.org/10.1016/j.soilbio.2020.107878
Tang J, Riley WJ (2019) Competitor and substrate sizes and diffusion together define enzymatic depolymerization and microbial substrate uptake rates. Soil Biol Biochem 139:107624. https://doi.org/10.1016/j.soilbio.2019.107624
Tang Z, Sun X, Luo Z, He N, Sun OJ (2018) Effects of temperature, soil substrate, and microbial community on carbon mineralization across three climatically contrasting forest sites. Ecol Evol 8:879–891. https://doi.org/10.1002/ece3.3708
Tian D, Xiang W, Yan W (2004) Comparison of bimass dynamic and nutrient cycling between pinus massoniman plataion and Pinus elliottin plantation. Acta Ecol Sin 24:2207–2210
Tischer A, Blagodatskaya E, Hamer U (2015) Microbial community structure and resource availability drive the catalytic efficiency of soil enzymes under land use change conditions. Soil Biol Biochem 89:226–237. https://doi.org/10.1016/j.soilbio.2015.07.011
Tischer A, Sehl L, Meyer U-N, Kleinebecker T, Klaus V, Hamer U (2019) Land use intensity shapes kinetics of extracellular enzymes in rhizosphere soil of agricultural grassland plant species. Plant Soil 437:215–239. https://doi.org/10.1007/s11104-019-03970-w
Waldrop MP, Zak DR, Sinsabaugh RL, Gallo M, Lauber C (2004) Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecol Appl 14:1172–1177. https://doi.org/10.1890/03-5120
Wang B, Allison SD (2019) Emergent properties of organic matter decomposition by soil enzymes. Soil Biol Biochem 136:107522. https://doi.org/10.1016/j.soilbio.2019.107522
Wang J, Wu Y, Li J, He Q, Bing H (2021) Soil enzyme stoichiometry is tightly linked to microbial community composition in successional ecosystems after glacier retreat. Soil Biol Biochem 162:108429. https://doi.org/10.1016/j.soilbio.2021.108429
Wang B, Xue S, Liu GB, Zhang GH, Li G, Ren ZP (2012) Changes in soil nutrient and enzyme activities under different vegetations in the Loess Plateau area, Northwest China. CATENA 92:186–195. https://doi.org/10.1016/j.catena.2011.12.004
Wei X, Li Q, Liu Y, Liu S, Guo X, Zhang L, Niu D, Zhang W (2013) Restoring ecosystem carbon sequestration through afforestation: a sub tropic restoration case study. For Ecol Manag 300:60–67. https://doi.org/10.1016/j.foreco.2012.06.018
Wu ZJ, Duan XQ, Li WQ, Chen FS, Liu YQ, Fang XM (2022a) Effects of tree mixture on rhizosphere soil nitrogen mineralization and microbial characteristics of coniferous trees in subtropical plantations. Acta Ecol Sin 42:8414–8424. https://doi.org/10.5846/stxb202110072766
Wu Y, Zhou H, Sun W, Zhao Q, Liang M, Chen W, Guo Z, Jiang Y, Jiang Y, Liu G, Xue S (2022b) Temperature sensitivity of soil enzyme kinetics under N and P fertilization in an alpine grassland, China. Sci Total Environ 838:156042. https://doi.org/10.1016/j.scitotenv.2022.156042
Xiang Y, Li Y, Luo X, Liu Y, Huang P, Yao B, Zhang L, Li W, Xue J, Gao H, Xiang Y, Li Y, Luo X, Liu Y, Huang P, Yao B, Zhang L, Li W, Xue J, Gao H, Li Y, Zhang W (2022) Mixed plantations enhance more soil organic carbon stocks than monocultures across China: implication for optimizing afforestation/reforestation strategies. Sci Total Environ 821:153449. https://doi.org/10.1016/j.scitotenv.2022.153449
Yan H, Kou L, Wang H, Fu X, Dai X, Li S (2019) Contrasting root foraging strategies of two subtropical coniferous forests under an increased diversity of understory species. Plant Soil 436:427–438. https://doi.org/10.1007/s11104-019-03936-y
Yuan Z, Ali A, Wang S, Gazol A, Freckleton R, Wang X, Lin F, Ye J, Zhou L, Hao Z, Yuan Z, Ali A, Wang S, Gazol A, Freckleton R, Wang X, Lin F, Ye Ji, Zhou Li, Hao Z, Loreau M (2018) Abiotic and biotic determinants of coarse woody productivity in temperate mixed forests. Sci Total Environ 630:422–431. https://doi.org/10.1016/j.scitotenv.2018.02.125
Zhang X, Yang Y, Zhang C, Niu S, Yang H, Yu G, Wang H, Blagodatskaya E, Kuzyakov Y, Tian D, Zhang X, Yang Y, Zhang C, Niu S, Yang H, Yu G, Wang H, Blagodatskaya E, Kuzyakov Y, Tian D, Tang Y, Liu S, Sun X (2018) Contrasting responses of phosphatase kinetic parameters to nitrogen and phosphorus additions in forest soils. Funct Ecol 32:106–116. https://doi.org/10.1111/1365-2435.12936
Acknowledgements
The authors thank Wen-Qing Li and Zi-Jun Wu for their help with the investigations and sample analysis. We are grateful to Ling Zhang for his comments on the manuscript.
Funding
This work was supported by the National Natural Science Foundation of China (32260379), the Jiangxi Provincial Science Fund for Distinguished Young Scholars (20224ACB215005) and the Jiangxi “Double Thousand Plan” (jxsq2019201080).
Author information
Authors and Affiliations
Contributions
Xiang-Min Fang, Rong Mao, Zhong-Liang Li and Fu-Sheng Chen contributed to the study conception and design. Zhong-Liang Li and Yu-Xin Huang collected the samples. Xue-Li Jiang, Bin Xu, Jin He and Yu-Xin Huang ran analyses. Xue-Li Jiang wrote the first draft of the manuscript. Xiang-Min Fang provided edits to the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Responsible Editor: Timothy J. Fahey.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 52.7 KB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Jiang, XL., Mao, R., Li, ZL. et al. Tree species mixture effect on extracellular enzyme kinetics varies with enzyme type and soil depth in subtropical plantations. Plant Soil 493, 267–282 (2023). https://doi.org/10.1007/s11104-023-06229-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-023-06229-7