Abstract
As a global pollution, acid rain can significantly alter soil physicochemical and biochemical processes, but our knowledge of how acid rain affects soil enzyme activity is still limited. To quantify the overall magnitude and direction of the response of soil enzyme activity to acid rain, we conducted a linear mixed model–based meta-analysis of 40 articles. Our analysis revealed that acid rain decreased enzyme activity by an average of 4.87%. Soil dehydrogenase and protease activities were particularly sensitive to acid rain, with significant inhibitions observed. The effect of acid rain was moderated by acid rain intensity (i.e., H+ addition rate, total H+ added, and acid rain pH) and soil fraction (i.e., rhizosphere and bulk soil). Structural equation modelling further revealed that acid rain suppressed soil microbial biomass by acidifying the soil and that the reduction in microbial biomass directly led to the inhibition of enzyme activity in bulk soil. However, the enzyme activity in the rhizosphere soil was not affected by acid rain due to the rhizosphere effect, which was also not impacted by the decreased soil pH induced by acid rain in rhizosphere. Our study gives an insight into how bulk soil enzyme activity is impacted by acid rain and highlights the need to incorporate rhizosphere processes into acid rain-terrestrial ecosystem models.
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References
Adams DC, Gurevitch J, Rosenberg MS (1997) Resampling tests for meta-analysis of ecological data. Ecology 78:1277–1283. https://doi.org/10.1890/0012-9658(1997)078[1277:RTFMAO]2.0.CO;2
Ahkami AH, Allen White R, Handakumbura PP, Jansson C (2017) Rhizosphere engineering: enhancing sustainable plant ecosystem productivity. Rhizosphere 3:233–243. https://doi.org/10.1016/j.rhisph.2017.04.012
Anderson JPE, Domsch KH (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:215–221. https://doi.org/10.1016/0038-0717(78)90099-8
Aponte H, Medina J, Butler B et al (2020a) Soil quality indices for metal(loid) contamination: an enzymatic perspective. Land Degrad Dev 31:2700–2719. https://doi.org/10.1002/ldr.3630
Aponte H, Meli P, Butler B et al (2020b) Meta-analysis of heavy metal effects on soil enzyme activities. Sci Total Environ 737:139744. https://doi.org/10.1016/j.scitotenv.2020.139744
Chen X, Achal V (2020) Effect of simulated acid rain on the stability of calcium carbonate immobilized by microbial carbonate precipitation. J Environ Manage 264:110419. https://doi.org/10.1016/j.jenvman.2020.110419
Chen D, Li J, Lan Z et al (2016) Soil acidification exerts a greater control on soil respiration than soil nitrogen availability in grasslands subjected to long-term nitrogen enrichment. Funct Ecol 30:658–669. https://doi.org/10.1111/1365-2435.12525
Chen J, Luo Y, van Groenigen KJ et al (2018) A keystone microbial enzyme for nitrogen control of soil carbon storage. Sci Adv 4:eaaq1689. https://doi.org/10.1126/sciadv.aaq1689
Chen J, van Groenigen KJ, Hungate BA et al (2020a) Long-term nitrogen loading alleviates phosphorus limitation in terrestrial ecosystems. Glob Change Biol 26:5077–5086. https://doi.org/10.1111/gcb.15218
Chen S, Sun L, Zhang X et al (2020b) Contrasting effects of long-term acid rain simulation on temperature sensitivity of soil respiration and enzymatic activities in a subtropical forest. J Soils Sediments 20:412–424. https://doi.org/10.1007/s11368-019-02385-5
Dighton J (1983) Phosphatase production by mycorrhizal fungi. Plant Soil 71:455–462. https://doi.org/10.1007/BF02182686
Dong D, Du E, Sun Z et al (2017) Non-linear direct effects of acid rain on leaf photosynthetic rate of terrestrial plants. Environ Pollut 231:1442–1445. https://doi.org/10.1016/j.envpol.2017.09.005
Du E, Dong D, Zeng X et al (2017) Direct effect of acid rain on leaf chlorophyll content of terrestrial plants in China. Sci Total Environ 605–606:764–769. https://doi.org/10.1016/j.scitotenv.2017.06.044
Fan K, Weisenhorn P, Gilbert JA, Chu H (2018) Wheat rhizosphere harbors a less complex and more stable microbial co-occurrence pattern than bulk soil. Soil Biol Biochem 125:251–260. https://doi.org/10.1016/j.soilbio.2018.07.022
Ge T, Wei X, Razavi BS et al (2017) Stability and dynamics of enzyme activity patterns in the rice rhizosphere: effects of plant growth and temperature. Soil Biol Biochem 113:108–115. https://doi.org/10.1016/j.soilbio.2017.06.005
Greenfield LM, Puissant J, Jones DL (2021) Synthesis of methods used to assess soil protease activity. Soil Biol Biochem 158:108277. https://doi.org/10.1016/j.soilbio.2021.108277
Guan N, Liu L (2020) Microbial response to acid stress: mechanisms and applications. Appl Microbiol Biotechnol 104:51–65. https://doi.org/10.1007/s00253-019-10226-1
Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152. https://doi.org/10.1007/s11104-008-9885-9
Hosseini SS, Lakzian A, Razavi BS (2022) Reduction in root active zones under drought stress controls spatial distribution and catalytic efficiency of enzyme activities in rhizosphere of wheat. Rhizosphere 23:100561. https://doi.org/10.1016/j.rhisph.2022.100561
Hu Y, Chen J, Hui D et al (2022) Mycorrhizal fungi alleviate acidification-induced phosphorus limitation: evidence from a decade-long field experiment of simulated acid deposition in a tropical forest in south China. Glob Change Biol 28:3605–3619. https://doi.org/10.1111/gcb.16135
Kang H, Lee D (1998) Changes of soil enzyme activities by simulated acid and nitrogen deposition. Chem Ecol 14:123–131. https://doi.org/10.1080/02757549808035547
Katsalirou E, Deng S, Nofziger DL, Gerakis A (2010) Long-term management effects on organic C and N pools and activities of C-transforming enzymes in prairie soils. Eur J Soil Biol 46:335–341. https://doi.org/10.1016/j.ejsobi.2010.06.004
Killham K, Firestone MK, Mc Coll JG (1983) Acid rain and soil microbial activity: effects and their mechanisms. J Environ Qual 12:133–137. https://doi.org/10.2134/jeq1983.00472425001200010024x
Kotroczó Z, Veres Z, Fekete I et al (2014) Soil enzyme activity in response to long-term organic matter manipulation. Soil Biol Biochem 70:237–243. https://doi.org/10.1016/j.soilbio.2013.12.028
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest Package: tests in linear mixed effects models. J Stat Softw 82:1–26. https://doi.org/10.18637/jss.v082.i13
Kuzyakov Y, Razavi BS (2019) Rhizosphere size and shape: temporal dynamics and spatial stationarity. Soil Biol Biochem 135:343–360. https://doi.org/10.1016/j.soilbio.2019.05.011
Lefcheck JS (2015) PIECEWISESEM: Piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579. https://doi.org/10.1111/2041-210X.12512
Li C, Liu X, Meng M et al (2021a) The use of Biolog Eco microplates to compare the effects of sulfuric and nitric acid rain on the metabolic functions of soil microbial communities in a subtropical plantation within the Yangtze River Delta region. CATENA 198:105039. https://doi.org/10.1016/j.catena.2020.105039
Li J, Pei J, Liu J et al (2021b) Spatiotemporal variability of fire effects on soil carbon and nitrogen: a global meta-analysis. Glob Change Biol 27:4196–4206. https://doi.org/10.1111/gcb.15742
Li X, Wang Y, Zhang Y et al (2021c) Response of soil chemical properties and enzyme activity of four species in the Three Gorges Reservoir area to simulated acid rain. Ecotoxicol Environ Saf 208:111457. https://doi.org/10.1016/j.ecoenv.2020.111457
Liu M, Huang X, Song Y et al (2019a) Ammonia emission control in China would mitigate haze pollution and nitrogen deposition, but worsen acid rain. Proc Natl Acad Sci 116:7760–7765. https://doi.org/10.1073/pnas.1814880116
Liu Z, Yang J, Zhang J et al (2019b) A bibliometric analysis of research on acid rain. Sustainability 11:3077. https://doi.org/10.3390/su11113077
Liu X, Li C, Meng M et al (2020a) Comparative effects of the recovery from sulfuric and nitric acid rain on the soil enzyme activities and metabolic functions of soil microbial communities. Sci Total Environ 714:136788. https://doi.org/10.1016/j.scitotenv.2020.136788
Liu Z, Li D, Zhang J et al (2020b) Effect of simulated acid rain on soil CO2, CH4 and N2O emissions and microbial communities in an agricultural soil. Geoderma 366:114222. https://doi.org/10.1016/j.geoderma.2020.114222
Liu C, Song Y, Dong X et al (2021) Soil enzyme activities and their relationships with soil C, N, and P in peatlands from different types of permafrost regions, northeast china. Front Environ Sci 9:670769. https://doi.org/10.3389/fenvs.2021.670769
Liu Z, Shi Z, Wei H, Zhang J (2022) Acid rain reduces soil CO2 emission and promotes soil organic carbon accumulation in association with decreasing the biomass and biological activity of ecosystems: a meta-analysis. CATENA 208:105714. https://doi.org/10.1016/j.catena.2021.105714
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
Lv Y, Wang C, Jia Y et al (2014) Effects of sulfuric, nitric, and mixed acid rain on litter decomposition, soil microbial biomass, and enzyme activities in subtropical forests of China. Appl Soil Ecol 79:1–9. https://doi.org/10.1016/j.apsoil.2013.12.002
Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704. https://doi.org/10.1111/j.1469-8137.2011.03967.x
Meng C, Tian D, Zeng H et al (2019) Global soil acidification impacts on belowground processes. Environ Res Lett 14:74003. https://doi.org/10.1088/1748-9326/ab239c
Mark Mitchell, Baurzhan Muftakhidinov, Tobias Winchen (2019) Engauge digitizer software
Moher D, Liberati A, Tetzlaff J et al (2009) Preferred reporting Items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6:e1000097. https://doi.org/10.1371/journal.pmed.1000097
Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19. https://doi.org/10.1007/s00374-017-1245-6
Peng S, Chen HYH (2021) Global responses of fine root biomass and traits to plant species mixtures in terrestrial ecosystems. Glob Ecol Biogeogr 30:289–304. https://doi.org/10.1111/geb.13205
Pina RG, Cervantes C (1996) Microbial interactions with aluminium. BioMetals 9:311–316. https://doi.org/10.1007/BF00817932
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Schimel JP, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Front Microbiol 3:348. https://doi.org/10.3389/fmicb.2012.00348
Shi Z, Zhang J, Xiao Z et al (2021) Effects of acid rain on plant growth: a meta-analysis. J Environ Manage 297:113213. https://doi.org/10.1016/j.jenvman.2021.113213
Tarafdar JC, Yadav RS, Meena SC (2001) Comparative efficiency of acid phosphatase originated from plant and fungal sources. J Plant Nutr Soil Sci 164:279–282. https://doi.org/10.1002/1522-2624(200106)164:3%3C279::AID-JPLN279%3E3.0.CO;2-L
Tian G, Qiu H, Li D et al (2022) Little environmental adaptation and high stability of bacterial communities in rhizosphere rather than bulk soils in rice fields. Appl Soil Ecol 169:104183. https://doi.org/10.1016/j.apsoil.2021.104183
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707. https://doi.org/10.1016/0038-0717(87)90052-6
Vilà M, Espinar JL, Hejda M et al (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems: ecological impacts of invasive alien plants. Ecol Lett 14:702–708. https://doi.org/10.1111/j.1461-0248.2011.01628.x
Vranova V, Rejsek K, Formanek P (2013) Proteolytic activity in soil: a review. Appl Soil Ecol 70:23–32. https://doi.org/10.1016/j.apsoil.2013.04.003
Wang C, Guo P, Han G et al (2010) Effect of simulated acid rain on the litter decomposition of Quercus acutissima and Pinus massoniana in forest soil microcosms and the relationship with soil enzyme activities. Sci Total Environ 408:2706–2713. https://doi.org/10.1016/j.scitotenv.2010.03.023
Wei H, Shan X, Wu L et al (2023) Microbial cell membrane properties and intracellular metabolism regulate individual level microbial responses to acid stress. Soil Biol Biochem 177:108883. https://doi.org/10.1016/j.soilbio.2022.108883
Wickham H (2016) ggplot2: Elegant graphics for data analysis, 2nd edn. Springer, Cham
Wu J, Liang G, Hui D et al (2016) Prolonged acid rain facilitates soil organic carbon accumulation in a mature forest in Southern China. Sci Total Environ 544:94–102. https://doi.org/10.1016/j.scitotenv.2015.11.025
Wu J, Deng Q, Hui D et al (2020) Reduced lignin decomposition and enhanced soil organic carbon stability by acid rain: evidence from 13C Isotope and 13C NMR analyses. Forests 11:1191. https://doi.org/10.3390/f11111191
Xiao W, Chen X, Jing X, Zhu B (2018) A meta-analysis of soil extracellular enzyme activities in response to global change. Soil Biol Biochem 123:21–32. https://doi.org/10.1016/j.soilbio.2018.05.001
Yang Y, Dong M, Cao Y et al (2017) Comparisons of soil properties, enzyme activities and microbial communities in heavy metal contaminated bulk and rhizosphere soils of Robinia pseudoacacia L. in the Northern foot of Qinling Mountain. Forests 8:430. https://doi.org/10.3390/f8110430
Yu Z, Chen HYH, Searle EB et al (2020) Whole soil acidification and base cation reduction across subtropical China. Geoderma 361:114107. https://doi.org/10.1016/j.geoderma.2019.114107
Zhou Y, Staver AC (2019) Enhanced activity of soil nutrient-releasing enzymes after plant invasion: a meta-analysis. Ecology 100:e02830. https://doi.org/10.1002/ecy.2830
Zhou Y, Biro A, Wong MY et al (2022) Fire decreases soil enzyme activities and reorganizes microbially mediated nutrient cycles: a meta-analysis. Ecology. 103(11):e3807. https://doi.org/10.1002/ecy.3807
Zuber SM, Villamil MB (2016) Meta-analysis approach to assess effect of tillage on microbial biomass and enzyme activities. Soil Biol Biochem 97:176–187. https://doi.org/10.1016/j.soilbio.2016.03.011
Acknowledgements
We are grateful to all the researchers whose studies were included in this meta-analysis.
Funding
This work was supported by the National Natural Science Foundation of China (grant numbers U1701236, 32071641), the Joint Project of Laboratory of Lingnan Modern Agriculture (grant number NT2021010). Science and Technology Planning Project of Guangdong Province of China (grant number 2019B030301007), and Special Funds for the Cultivation of Guangdong College Students’ Scientific and Technological Innovation (grant number pdjh 2020b0092).
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Shi, Z., Zhang, J., Zhang, H. et al. Response and driving factors of soil enzyme activity related to acid rain: a meta-analysis. Environ Sci Pollut Res 30, 105072–105083 (2023). https://doi.org/10.1007/s11356-023-29585-4
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DOI: https://doi.org/10.1007/s11356-023-29585-4