Abstract
Camellia sinensis is an important economic plant grown in southern subtropical hilly areas, especially in China, mainly for the production of tea. Soil acidification is a significant cause of the reduction of yield and quality and continuous cropping obstacles in tea plants. Therefore, chemical and microbial properties of tea growing soils were investigated and phenolic acid-degrading bacteria were isolated from a tea plantation. Chemical and ICP-AES investigations showed that the soils tested were acidic, with pH values of 4.05–5.08, and the pH negatively correlated with K (p < 0.01), Al (p < 0.05), Fe and P. Aluminum was the highest (47–584 mg/kg) nonessential element. Based on high-throughput sequencing, a total of 34 phyla and 583 genera were identified in tea plantation soils. Proteobacteria and Acidobacteria were the main dominant phyla and the highest abundance of Acidobacteria was found in three soils, with nearly 22% for the genus Gp2. Based on the functional abundance values, general function predicts the highest abundance, while the abundance of amino acids and carbon transport and metabolism were higher in soils with pH less than 5. According to Biolog Eco Plate™ assay, the soil microorganisms utilized amino acids well, followed by polymers and phenolic acids. Three strains with good phenolic acid degradation rates were obtained, and they were identified as Bacillus thuringiensis B1, Bacillus amyloliquefaciens B2 and Bacillus subtilis B3, respectively. The three strains significantly relieved the inhibition of peanut germination and growth by ferulic acid, p-coumaric acid, p-hydroxybenzoic acid, cinnamic acid, and mixed acids. Combination of the three isolates showed reduced relief of the four phenolic acids due to the antagonist of B2 against B1 and B3. The three phenolic acid degradation strains isolated from acidic soils display potential in improving the acidification and imbalance in soils of C. sinensis.
Similar content being viewed by others
Availability of data and materials
The data that support the findings of this study are available from the corresponding author, Yuhan Zhang, upon reasonable request.
References
Alekseeva T, Alekseev A, Xu RK, Zhao AZ, Kalinin P (2011) Effect of soil acidification induced by a tea plantation on chemical and mineralogical properties of Alfisols in eastern China. Environ Geochem Health 33:137–148. https://doi.org/10.1007/s10653-010-9327-5
Arafat Y et al (2020) Soil sickness in aged tea plantation is associated with a shift in microbial communities as a result of plant polyphenol accumulation in the tea gardens. Front Plant Sci 11:601. https://doi.org/10.3389/fpls.2020.00601
Aston JE et al (2016) Degradation of phenolic compounds by the lignocellulose deconstructing thermoacidophilic bacterium Alicyclobacillus acidocaldarius. J Ind Microbiol Biotechnol 43:13–23. https://doi.org/10.1007/s10295-015-1700-z
Bai Y et al (2019) Soil acidification in continuously cropped tobacco alters bacterial community structure and diversity via the accumulation of phenolic acids. Sci Rep 9:12499. https://doi.org/10.1038/s41598-019-48611-5
Bao L et al (2022) Interactions between phenolic acids and microorganisms in rhizospheric soil from continuous cropping of panax notoginseng. Front Microbiol 13:791603. https://doi.org/10.3389/fmicb.2022.791603
Belova SE et al (2022) Corrigendum: hydrolytic capabilities as a key to environmental success: chitinolytic and cellulolytic acidobacteria from acidic sub-arctic soils and boreal peatlands. Front Microbiol 13:856396. https://doi.org/10.3389/fmicb.2022.856396
Cao P, Luo S (1996) Study on the autotoxic effect of tea tree. Guang Dong Tea 2:9–11
Chai X et al (2021) Spatial variation of the soil bacterial community in major apple producing regions of China. J Appl Microbiol 130:1294–1306. https://doi.org/10.1111/jam.14878
Chen S, Yu H, Zhou X, Wu F (2018) Cucumber (Cucumis sativus L.) seedling rhizosphere Trichoderma and Fusarium spp. communities altered by vanillic acid. Front Microbiol 9:2195
Conradie TA, Jacobs K (2021) Distribution patterns of Acidobacteriota in different fynbos soils. PLoS ONE 16:e0248913. https://doi.org/10.1371/journal.pone.0248913
Fritsch C, Heinrich V, Vogel RF, Toelstede S (2016) Phenolic acid degradation potential and growth behavior of lactic acid bacteria in sunflower substrates. Food Microbiol 57:178–186. https://doi.org/10.1016/j.fm.2016.03.003
Gao H, Meng T, Xiong Q, Zhang H, Qiu J (2022) Changes in physicochemical property and microbial community of Pseudostellaria heterophylla soil at different fallow ages. Chin J Appl Ecol 33:2196–2204. https://doi.org/10.13287/j.1001-9332.202208.029
Gao S et al (2021) Consecutive soybean (Glycine max) planting and covering improve acidified tea garden soil. PLoS ONE 16:e0254502. https://doi.org/10.1371/journal.pone.0254502
Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57(8):2351–2359. https://doi.org/10.1128/aem.57.8.2351-2359.1991
Han W et al (2002) The major nutritional limiting factors in tea soils and development of tea speciality fertilizer series. J Tea Sci 22:70–74
Hao J et al (2022) Tea plant roots respond to aluminum-induced mineral nutrient imbalances by transcriptional regulation of multiple cation and anion transporters. BMC Plant Biol 22:203. https://doi.org/10.1186/s12870-022-03570-4
Ji T, Shen Y, Chen S, Fu E (2017) Study on determination of exchangeable aluminum by inductively coupled plasma atomic emission spectrometry. Acta Agriculturae Zhejiangensis 29:1347–1352
Kalam S et al (2020) Recent understanding of soil acidobacteria and their ecological significance: a critical review. Front Microbiol 11:580024. https://doi.org/10.3389/fmicb.2020.580024
Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120. https://doi.org/10.1128/aem.00335-09
Li C 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 M, Zhang L, Zhang Y, Zhu J, Ma H (2019) Review on the microbial biodegradation and metabolism of autotoxic phenolic acids. Asian J Ecotoxicol 14:72–78
Li P, Wang X, Li Y, Wang H, Liang F, Dai C (2010) The contents of phenolic acids in continuous cropping peanut and their allelopathy. Acta Ecol Sin 30:2128–2134
Li P, Ye S, Liu H, Pan A, Ming F, Tang X (2018a) Cultivation of drought-tolerant and insect-resistant rice affects soil bacterial, but not fungal, abundances and community structures. Front Microbiol 9:1390. https://doi.org/10.3389/fmicb.2018.01390
Li Q, Lei W, Liu J, Zhu J, Shi L (2021b) Effects of intercropping Ophiopogon japonicus into tea plantation on its soil physicochemical properties and microbial community structure. J South Agric 52:3366–3374
Li S, Li H, Yang C, Wang Y, Xue H, Niu Y (2016) Rates of soil acidification in tea plantations and possible causes. Agric Ecosyst Environ 233:60–66. https://doi.org/10.1016/j.agee.2016.08.036
Li Y et al (2023) Effect of continuous cropping of hot pepper on soil bacterial community. Acta Microbiol Sin 63:297–318. https://doi.org/10.13343/j.cnki.wsxb.20220310
Li Z, Fu J, Zhou R, Wang D (2018b) Effects of phenolic acids from ginseng rhizosphere on soil fungi structure, richness and diversity in consecutive monoculturing of ginseng. Saudi J Biol Sci 25:1788–1794. https://doi.org/10.1016/j.sjbs.2018.07.007
Li Z, Liu G, Wei J, Lu R (2000) Quick determination of effective phosphor in soil. J Changchun Univ Sci Technol 30:307–309. https://doi.org/10.13278/j.cnki.jjuese.2000.03.025
Ling G, Shi B, Huang Y, Li Y, Yu Y, Li X (2010) Secretion of organic acid anions and potassium from root apices under Al stress in Secale cereale L. Plant Nutr Fertil Sci 16:893–898
Liu P et al (2012) Iinteractive effects of three kinds of phenolic acids on peanut germination and soil microbes. Acta Agriculturae Jiangxi 24:85–87. https://doi.org/10.19386/j.cnki.jxnyxb.2012.08.026
Liu T, Gao H, Wan X, Zhang Z (2011) Impacts of aluminum on root cell membrane permeability and organic acids in root exudates of tea plant. J Tea Sci 31:458–462. https://doi.org/10.13305/j.cnki.jts.2011.05.015
Liu Y, Huang Y, Zeng Q (2016) Soil bacterial communities under different vegetation types in the loess plateau. Environ Sci 37:3931–3938
Min K, Freeman C, Kang H, Choi SU (2015) The regulation by phenolic compounds of soil organic matter dynamics under a changing environment. Biomed Res Int 2015:825098. https://doi.org/10.1155/2015/825098
Mo X, Hu Y, Liu H, Zhang Q, Yi W (2016) Study on potential risk and prevention and control measures on soil over-acidification at tea plantation in mountainous tea garden of Guizhou. Tillage Cultiv 56–59. https://doi.org/10.13605/j.cnki.52-1065/s.2016.04.025
Mu Y, Yuan D, Lan Y, Tian W, Zhang J, Wang C (2016a) Effects of tea planting age on soil pH value, contents of organic matter and phenolic acids. Soil Fertil Sci China 4:44–48
Mu Y, Yuan D, Lan Y, Tian W, Zhang J, Wang C (2016b) Effects of tea polyphenol concentration on soil pH value, phenolic acid content and transformation of iron and aluminum. Chin J Soil Sci 47:954–958. https://doi.org/10.19336/j.cnki.trtb.2016.04.28
Peng Y et al (2020) Soil acidification in Chinese tea plantations. Sci Total Environ 715:136963. https://doi.org/10.1016/j.scitotenv.2020.136963
Qu XH, Wang JG (2008) Effect of amendments with different phenolic acids on soil microbial biomass, activity, and community diversity. Appl Soil Ecol 39:172–179. https://doi.org/10.1016/j.apsoil.2007.12.007
Shetty R, Vidya CS, Prakash NB, Lux A, Vaculík M (2021) Aluminum toxicity in plants and its possible mitigation in acid soils by biochar: a review. Sci Total Environ 765:142744. https://doi.org/10.1016/j.scitotenv.2020.142744
Shi J, Ding R, Liu Y, Sun Y (1999) Acidification of soil by urea and fallen tea leaves. J Tea Sci 19:7–12
Sun Q, Ni W, Yang X (2002) Role of organic acid in detoxification of aluminum in higher plants and its mechanisms. Chin Bull Bot 19:496–503
Sun X, Wang X, Wei M, Wang F, Shi Q, Zhou B (2014) Screening and identification of cinnamic acid-degrading fungis and the effect of degradation liquid on the cucumber germination. Acta Horticulturae Sinica 41:765–772. https://doi.org/10.16420/j.issn.0513-353x.2014.04.018
Tian P et al (2023) Effects of vanillic acid on growth and yield components of peanut and its rhizosphere soil. Chin J Oil Crop Sci 45:1–10. https://doi.org/10.19802/j.issn.1007-9084.2022188
Tian T, Wei J, Chen Y, Wei C, Chen H (2016) A review of aluminum, selenium and calcium nutrition and interactions in tea trees. Jiangsu Agric Sci 44:29–33. https://doi.org/10.15889/j.issn.1002-1302.2016.12.007
Wang F et al (2022a) Effects of planting patterns and slope positions on soil bacterial community structure and functional groups in tea gardens. Acta Ecol Sin 42:8435–8452
Wang J et al (2022b) Screening, identification and antimicrobial activity of microbial strains degrading autotoxic phenolic acids in the rhizosphere of vanilla. J Trop Biol 13:595–604. https://doi.org/10.15886/j.cnki.rdswxb.2022.06.009
Wang X, Zhang T, Dai C (2010) Advance in mechanism and countermeasures of peanut succession monocropping obstacles. Soils 42:505–512. https://doi.org/10.13758/j.cnki.tr.2010.04.021
Wang Y, Liao W, Su Y, Zhang Y, Sun L (2012) Investigation of content of water-soluble phenolic acids and complex phenolic acids in tea garden soil. J Anhui Agric Sci 40:14256–14258. https://doi.org/10.13989/j.cnki.0517-6611.2012.29.266
Wang Y, Zhang W, Zhang Z, Wang W, Xu S, He X (2021) Isolation, identification and characterization of phenolic acid-degrading bacteria from soil. J Appl Microbiol 131:208–220. https://doi.org/10.1111/jam.14956
Ward NL et al (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056. https://doi.org/10.1128/aem.02294-08
Whitehead DC (1964) Identification of p-hydroxybenzoic, vanillic, p-coumaric and ferulic acids in soils. Nature 202:417–418. https://doi.org/10.1038/202417a0
Wu F et al (2021) Plant metabolomics integrated with transcriptomics and rhizospheric bacterial community indicates the mitigation effects of Klebsiella oxytoca P620 on p-hydroxybenzoic acid stress in cucumber. J Hazard Mater 415:125756. https://doi.org/10.1016/j.jhazmat.2021.125756
Wu F, Huang C, Deng X (2007) Allelopathy effects of phenolic acid substances on nutrinets absorption of cucumber seedlings. J Inner Mongolia Agric Univ 28:131–133
Wu X, Chen H, Sun Y (2017) Study on the determination of total phosphorus, total potassium and fluoride in soil through sodium hydroxide fusion method. Ningxia J Agric for Sci Technol 58:44–45
Xie S et al (2021) Organic fertilizer reduced carbon and nitrogen in runoff and buffered soil acidification in tea plantations: evidence in nutrient contents and isotope fractionations. Sci Total Environ 762:143059. https://doi.org/10.1016/j.scitotenv.2020.143059
Xie Z, Fang C, Sun W, Chen Z, Yin B (2007) Effects of interaction of citric acid-aluminum-fluoride on the adsorption characteristics and distribution of fluoride in tea garden soil. J Agro-Environ Sci 26:2271–2276
Xu HJ, Wang XH, Li H, Yao HY, Su JQ, Zhu YG (2014) Biochar impacts soil microbial community composition and nitrogen cycling in an acidic soil planted with rape. Environ Sci Technol 48:9391–9399. https://doi.org/10.1021/es5021058
Ye J et al (2016) Autotoxicity of the soil of consecutively cultured tea plantations on tea (Camellia sinensis) seedlings. Acta Physiol Plant 38:195–204
Ye J et al (2022) Improvement of soil acidification in tea plantations by long-term use of organic fertilizers and its effect on tea yield and quality. Front Plant Sci 13:1055900. https://doi.org/10.3389/fpls.2022.1055900
Zhu B et al (2023) Improvement of phenolic acid autotoxicity in tea plantations by Pseudomonas fluorescens ZL22. J Hazard Mater 458:131957. https://doi.org/10.1016/j.jhazmat.2023.131957
Zou L (2005) Autotoxic effect of watermelon root secretions on the growth of watermelon plants. Fujian Agric Sci Technol 20:30–31
Acknowledgements
We thank the Key Research and Development Project of Zhejiang (2021C02039, 2020C02030) Province, Shanxi (2019TSLSF02-01-01) Provinces, the Open Project of Zhejiang Provincial Key Laboratory of Agricultural Green Biomanufacturing Core Strain Improvement (2020KFKT09), and the Scientific Research Fund of Zhejiang Sci-tech University (20042221-Y) for funding.
Funding
This study was funded by the Key Research and Development Project of Zhejiang and Shanxi Provinces (2021C02039, 2020C02030, 2019TSLSF02-01-01), the Open Project of Zhejiang Provincial Key Laboratory of Agricultural Green Biomanufacturing Core Strain Improvement (2020KFKT09), and Scientific Research Fund of Zhejiang Sci-tech University (20042221-Y).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Yuhan Zhang, Binjie Wang, Guiwei Wang, Zhisheng Zheng, Ying Chen, and Ou Li. Yulong Peng provided technical support and Xiufang Hu provided fund support. The first draft of the manuscript was written by Yuhan Zhang and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Communicated by Yusuf Akhter.
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.
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
Zhang, Y., Wang, B., Wang, G. et al. Acidification induce chemical and microbial variation in tea plantation soils and bacterial degradation of the key acidifying phenolic acids. Arch Microbiol 206, 239 (2024). https://doi.org/10.1007/s00203-024-03858-z
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-024-03858-z