Abstract
Purpose
The increasing soil microplastics (MPs) pollution and the dry–wet alternation caused by climate change occur widely. Emerging studies have shown their negative impacts on the structure of soil bacteria and plant physiology. However, there is limited research on the effects of MPs exposure under different water regimes, and the influence processes are inconclusive. Therefore, the impacts of MPs under different water regimes on the antioxidant activity of vegetable and the soil bacterial community were studied.
Materials and methods
A continuous water supply and a dry–wet cycle were established to compare the effects of two types of MPs (polypropylene (PP); polyethylene terephthalate (PET)) on lettuce (Lactuca sativa L. var. longifolia) growth and soil bacterial community, determined by antioxidant enzyme activity analysis, and by high-throughput sequencing analysis, respectively.
Results
The PET influenced the lettuce growth and bacterial diversity largely compared to PP. The dry–wet cycle enhanced the effects of MPs on the activity of the antioxidant enzymes in lettuce, while it reduced lettuce biomass and root activity. Proteobacteria and Actinobacteria were the dominant soil bacteria under all treatments. The addition of MPs increased the relative abundance of nutrient-related bacteria such as Proteobacteria. MPs addition increased intragroup differences in soil bacterial diversity, and the dry–wet cycle reduced intergroup differences caused by MPs.
Conclusion
The polymer type of MPs influenced the antioxidant activity of lettuce roots and leaves. The dry–wet cycle intensified the exposure risk of MPs by enhancing the stimulation of MPs on the antioxidant activity of lettuce. The dry–wet cycle significantly reduced the MPs-induced differences in bacterial communities. In short, the dry–wet cycle might alter the ecological risks in plant-soil ecosystem by shifting soil bacterial lineages related to nutrient cycling and metabolic function under MPs exposure.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data will be made available upon request.
References
Bapiri A, Bååth E, Rousk J (2010) Drying–rewetting cycles affect fungal and bacterial growth differently in an arable soil. Microb Ecol 60:419–428. https://doi.org/10.1007/s00248-010-9723-5
Cao S, Wang W, Wang F, Zhang J, Wang Z, Yang S, Xue Q (2016) Drought-tolerant Streptomyces pactum Act12 assist phytoremediation of cadmium-contaminated soil by Amaranthus hypochondriacus: great potential application in arid/semi-arid areas. Environ Sci Pollut Res 23(15):14898–14907. https://doi.org/10.1007/s11356-016-6636-y
Chen S, Zhang W, Li J, Yuan M, Zhang J, Xu F, Xu H, Zheng X, Wang L (2020) Ecotoxicological effects of sulfonamides and fluoroquinolones and their removal by a green alga (Chlorella vulgaris) and a cyanobacterium (Chrysosporum ovalisporum). Environ Pollut 263:114554. https://doi.org/10.1016/j.envpol.2020.114554
Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34(17):i884–i890. https://doi.org/10.1093/bioinformatics/bty560
Dong Y, Gao M, Song Z, Qiu W (2020) Microplastic particles increase arsenic toxicity to rice seedlings. Environ Pollut 259:113892. https://doi.org/10.1016/j.envpol.2019.113892
Duan J, Bolan N, Li Y, Ding S, Atugoda T, Vithanage M, Sarkar B, Tsang D, Kirkham MB (2021) Weathering of microplastics and interaction with other coexisting constituents in terrestrial and aquatic environments. Water Res 196:117011. https://doi.org/10.1016/j.watres.2021.117011
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998. https://doi.org/10.1038/nmeth.2604
Fan H, Liu H, Dong Y, Chen C, Wang Z, Guo J, Du S (2019) Growth inhibition and oxidative stress caused by four ionic liquids in Scenedesmus obliquus: role of cations and anions. Sci Total Environ 651:570–579. https://doi.org/10.1016/j.scitotenv.2018.09.106
Fukami T (2015) Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu Rev Ecol Evol Syst 46:1–23. https://doi.org/10.1146/annurev-ecolsys-110411-160340
Gao B, Yao H, Li Y, Zhu Y (2021a) Microplastic addition alters the microbial community structure and stimulates soil carbon dioxide emissions in vegetable-growing soil. Environ Toxicol Chem 40(2):352–365. https://doi.org/10.1002/etc.4916
Gao J, Pan S, Li P, Li P, Wang L, Hou R, Wu W, Luo J, Hou D (2021b) Vertical migration of microplastics in porous media: multiple controlling factors under wet-dry cycling. J Hazard Mater 419:126413. https://doi.org/10.1016/j.jhazmat.2021.126413
Geyer R, Jambeck JR, Law KL (2017) Production, use, and the fate of all plastics ever made. Sci Adv 3(7):e1700782. https://doi.org/10.1126/sciadv.1700782
Gill SR, Pop M, DeBoy RT, Eckburg P, Turnbaugh P, Samuel B, Gordon J, Relman D, Fraser-liggett C, Neson K (2006) Metagenomic analysis of the human distal gut microbiome. Science 312(5778):1355–1359. https://doi.org/10.1126/science.1124234
Giorgetti L, Spanò C, Muccifora S, Bottega S, Barbieri F, Bellani L, Castiglione MR (2020) Exploring the interaction between polystyrene nanoplastics and Allium cepa during germination: internalization in root cells, induction of toxicity and oxidative stress. Plant Physiol Biochem 149:170–177. https://doi.org/10.1016/j.plaphy.2020.02.014
Gkoutselis G, Rohrbach S, Harjes J, Obst M, Brachmann A, Horn MA, Rambold G (2021) Microplastics accumulate fungal pathogens in terrestrial ecosystems. Sci Rep 11(1):1–13. https://doi.org/10.1038/s41598-021-92405-7
Guo JJ, Huang XP, Xiang L, Wang YZ, Li YW, Li H, Cai QY, Mo C-H, Wong MH (2020) Source, migration and toxicology of microplastics in soil. Environ Int 137:105263. https://doi.org/10.1016/j.envint.2019.105263
He D, Luo Y, Lu S, Liu M, Song Y, Lei L (2018) Microplastics in soils: analytical methods, pollution characteristics, and ecological risks. Trends Anal Chem 109:163–172. https://doi.org/10.1016/j.trac.2018.10.006
Huang B, Sun L, Liu M, Huang H, He H, Han F, Wang X, Xu Z, Li B, Pan X (2021) Abundance and distribution characteristics of microplastic in plateau cultivated land of Yunnan Province. China Sci Pollut Res 28(2):1675–1688. https://doi.org/10.1007/s11356-020-10527-3
Huang Y, Zhao Y, Wang J, Zhang M, Jia W, Qin X (2019) LDPE microplastic films alter microbial community composition and enzymatic activities in soil. Environ Pollut 254:112983. https://doi.org/10.1016/j.envpol.2019.112983
Jiang X, Chen H, Liao Y, Ye Z, Li M, Klobučar G (2019) Ecotoxicity and genotoxicity of polystyrene microplastics on higher plant Vicia faba. Environ Pollut 250:831–838. https://doi.org/10.1016/j.envpol.2019.04.055
Karbalaei S, Hanachi P, Walker TR, Cole M (2018) Occurrence, sources, human health impacts and mitigation of microplastic pollution. Environ Sci Pollut Res 25(36):36046–36063. https://doi.org/10.1007/s11356-018-3508-7
Kim SW, Waldman WR, Kim TY, Rillig MC (2020) Effects of different microplastics on nematodes in the soil environment: tracking the extractable additives using an ecotoxicological approach. Environ Sci Technol 54(21):13868–13878. https://doi.org/10.1021/acs.est.0c04641
Li H, Lu X, Wang S, Zheng B, Xu Y (2021) Vertical migration of microplastics along soil profile under different crop root systems. Environ Pollut 278:116833. https://doi.org/10.1016/j.envpol.2021.116833
Li Z, Li Q, Li R, Zhao Y, Geng J, Wang G (2020) Physiological responses of lettuce (Lactuca sativa L.) to microplastic pollution. Environ Sci Pollut Res 27:30306–30314. https://doi.org/10.1007/s11356-020-09349-0
Liu G, Zhu Z, Yang Y, Sun Y, Yu F, Ma J (2019) Sorption behavior and mechanism of hydrophilic organic chemicals to virgin and aged microplastics in freshwater and seawater. Environ Pollut 246:26–33. https://doi.org/10.1016/j.envpol.2018.11.100
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Miao L, Wang P, Hou J, Yao Y, Liu Z, Liu S, Li T (2019) Distinct community structure and microbial functions of biofilms colonizing microplastics. Sci Total Environ 650:2395–2402. https://doi.org/10.1016/j.scitotenv.2018.09.378
Ng EL, Lwanga EH, Eldridge SM, Johnston P, Hu HW, Geissen V, Chen D (2018) An overview of microplastic and nanoplastic pollution in agroecosystems. Sci Total Environ 627:1377–1388. https://doi.org/10.1016/j.scitotenv.2018.01.341
Ng EL, Lin SY, Dungan AM, Colwell JM, Ede S, Lwanga EH, Meng K, Geissen V, Blackall LL, Chen D (2021) Microplastic pollution alters forest soil microbiome. J Hazard Mater 409:124606. https://doi.org/10.1016/j.jhazmat.2020.124606
Ni L, Rong S, Gu G, Hu L, Wang P, Li D, Yue F, Wang N, Wu H, Li S (2018) Inhibitory effect and mechanism of linoleic acid sustained-release microspheres on Microcystis aeruginosa at different growth phases. Chemosphere 212:654–661. https://doi.org/10.1016/j.chemosphere.2018.08.045
Ouyang Y, Li X (2013) Recent research progress on soil microbial responses to drying–rewetting cycles. Acta Ecol Sin 33(1):1–6. https://doi.org/10.1016/j.chnaes.2012.12.001
Peng X, Li J, Sun L, Gao Y, Cao M, Luo J (2022) Impacts of water deficit and post-drought irrigation on transpiration rate, root activity, and biomass yield of Festuca arundinacea during phytoextraction. Chemosphere 294:133842. https://doi.org/10.1016/j.chemosphere.2022.133842
Prince L, Verhulst N, Govaerts B, Navarro-Noya YE, Dendooven L (2020) Wet or dry sowing had a larger effect on the soil bacterial community composition than tillage practices in an arid irrigated agro-ecosystem. J Soils Sediments 20:3316–3329. https://doi.org/10.1007/s11368-020-02626-y
Ren X, Tang J, Liu X, Liu Q (2020) Effects of microplastics on greenhouse gas emissions and the microbial community in fertilized soil. Environ Pollut 256:113347. https://doi.org/10.1016/j.envpol.2019.113347
Rillig MC, Ingraffia R, de Souza Machado AA (2017) Microplastic incorporation into soil in agroecosystems. Front Plant Sci 8:1805. https://doi.org/10.3389/fpls.2017.01805
Rillig MC, de Souza Machado AA, Lehmann A, Klümper U (2018) Evolutionary implications of microplastics for soil biota. Environ Chem 16(1):3–7. https://doi.org/10.1071/EN18118
Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R, Cei FP, Borin S, Sorlini C, Zocchi G, Daffonchio D (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17(2):316–331. https://doi.org/10.1111/1462-2920.12439
Shen M, Zhang Y, Zhu Y, Song B, Zeng G, Hu D, Wen X, Ren X (2019) Recent advances in toxicological research of nanoplastics in the environment: a review. Environ Pollut 252:511–521. https://doi.org/10.1016/j.envpol.2019.05.102
Simonin M, Richaume A (2015) Impact of engineered nanoparticles on the activity, abundance, and diversity of soil microbial communities: a review. Environ Sci Pollut Res 22(18):13710–13723. https://doi.org/10.1007/s11356-015-4171-x
Song YK, Hong SH, Jang M, Han GM, Jung SW, Shim WJ (2017) Combined effects of UV exposure duration and mechanical abrasion on microplastic fragmentation by polymer type. Environ Sci Technol 51(8):4368–4443. https://doi.org/10.1021/acs.est.6b06155
Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44(4):846–849. https://doi.org/10.1099/00207713-44-4-846
Xu J, Luo X, Wang Y, Feng Y (2018) Evaluation of zinc oxide nanoparticles on lettuce (Lactuca sativa L.) growth and soil bacterial community. Environ Sci Pollut Res 25:6026–6035. https://doi.org/10.1007/s11356-017-0953-7
Yao X, Luo XS, Fan J, Zhang T, Li H, Wei Y (2022) Ecological and human health risks of atmospheric microplastics (MPs): a review. Environ Sci Atmos 2:921–942. https://doi.org/10.1039/D2EA00041E
Ye L, Wu X, Wu C, Zhang Y, Meng L, Bao E, Cao K (2022) Response of soil bacterial community to agricultural reclamation in the Tengger desert, northwestern China. Appl Soil Eco 169:104189. https://doi.org/10.1016/j.apsoil.2021.104189
Yi M, Zhou S, Zhang L, Ding S (2021) The effects of three different microplastics on enzyme activities and microbial communities in soil. Water Environ Res 93(1):24–32. https://doi.org/10.1002/wer.1327
Yu L, Zhang JD, Liu Y, Chen L, Tao S, Liu W (2021) Distribution characteristics of microplastics in agricultural soils from the largest vegetable production base in China. Sci Total Environ 756:143860. https://doi.org/10.1016/j.scitotenv.2020.143860
Wang C, Tian Y, Wang X, Geng J, Jiang J, Yu H, Wang C (2010a) Lead-contaminated soil induced oxidative stress, defense response and its indicative biomarkers in roots of Vicia faba seedlings. Ecotoxicology 19(6):1130–1139. https://doi.org/10.1007/s10646-010-0496-x
Wang F, Feng X, Liu Y, Adams C. A, Sun Y, Zhang S (2022) Micro (nano) plastics and terrestrial plants: up-to-date knowledge on uptake, translocation, and phytotoxicity. Resour Conserv Recy 185:106503. https://doi.org/10.1016/j.resconrec.2022.106503
Wang J, Huang M, Wang Q, Sun Y, Zhao Y, Huang Y (2020a) LDPE microplastics significantly alter the temporal turnover of soil microbial communities. Sci Total Environ 726:138682. https://doi.org/10.1016/j.scitotenv.2020.138682
Wang J, Liu X, Dai Y, Ren J, Li Y, Wang X, Zhang P, Peng C (2020b) Effects of co-loading of polyethylene microplastics and ciprofloxacin on the antibiotic degradation efficiency and microbial community structure in soil. Sci Total Environ 741:140463. https://doi.org/10.1016/j.scitotenv.2020.140463
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267. https://doi.org/10.1128/AEM.00062-07
Wang Y, Liu F, De Neergaard A, Jensen LS, Luxhøi J, Jensen CR (2010b) Alternate partial root-zone irrigation induced dry/wet cycles of soils stimulate N mineralization and improve N nutrition in tomatoes. Plant Soil 337(1):167–177. https://doi.org/10.1007/s11104-010-0513-0
Wiedner K, Polifka S (2020) Effects of microplastic and microglass particles on soil microbial community structure in an arable soil (Chernozem). Soil 6(2):315–324. https://doi.org/10.5194/soil-6-315-2020
Zhang GS, Liu YF (2018) The distribution of microplastics in soil aggregate fractions in southwestern China. Sci Total Environ 642:12–20. https://doi.org/10.1016/j.scitotenv.2018.06.004
Zhang X, Huang G, Bian X, Zhao Q (2013) Effects of root interaction and nitrogen fertilization on the chlorophyll content, root activity, photosynthetic characteristics of intercropped soybean and microbial quantity in the rhizosphere. Plant Soil Environ 59(2):80–88. https://doi.org/10.17221/613/2012-PSE
Zhang Y, Du N, Wang L, Zhang H, Zhao J, Sun G, Wang P (2015) Physical and chemical indices of cucumber seedling leaves under dibutyl phthalate stress. Environ Sci Pollut Res 22(5):3477–3488. https://doi.org/10.1007/s11356-014-3524-1
Zheng X, Zhang W, Yuan Y, Li Y, Liu X, Wang X, Fan Z (2021) Growth inhibition, toxin production and oxidative stress caused by three microplastics in Microcystis aeruginosa. Ecotox Environ Safe. 208:111575. https://doi.org/10.1016/j.ecoenv.2020.111575
Zhou J, Gui H, Banfield CC, Wen Y, Zang H, Dippold MA, Charlton A, Jones DL (2021) The microplastisphere: biodegradable microplastics addition alters soil microbial community structure and function. Soil Biol Biochem 156:108211. https://doi.org/10.1016/j.soilbio.2021.108211
Zhou L, Wang T, Qu G, Jia H, Zhu L (2020) Probing the aging processes and mechanisms of microplastic under simulated multiple actions generated by discharge plasma. J Hazard Mater 398:122956. https://doi.org/10.1016/j.jhazmat.2020.122956
Zhou Z, Wang C, Luo Y (2018) Response of soil microbial communities to altered precipitation: a global synthesis. Global Ecol Biogeogr 27(9):1121–1136. https://doi.org/10.1111/geb.12761
Zhu F, Zhu C, Wang C, Gu C (2019) Occurrence and ecological impacts of microplastics in soil systems: a review. B Environ Contam Tox 102:741–749. https://doi.org/10.1007/s00128-019-02623-z
Funding
This research was funded by the National Special Fund Project for Soil Pollution Prevention and Control, and the Core Area (Demonstration Base) Construction Project for the Safe Use of Contaminated Farmland in Xinyi City.
Author information
Authors and Affiliations
Contributions
Methodology, experimental design, data curation, writing—original draft: Tingting Zhang; conceptualization; writing—review and editing; supervision: Xiao-San Luo; investigation: Xuewen Yao and Jiayi Fan; methodology: Yijia Song and Yidan Mao; writing—review and editing: Jiangbing Xu, Wajid Ali Khattak, Jinshan Yang, and Junyu Pan. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Responsible editor: Hang-Wei Hu
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, T., Luo, XS., Xu, J. et al. Dry–wet cycle changes the influence of microplastics (MPs) on the antioxidant activity of lettuce and the rhizospheric bacterial community. J Soils Sediments 23, 2189–2201 (2023). https://doi.org/10.1007/s11368-023-03479-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11368-023-03479-x