Effects of the coexistence of polystyrene microplastics and imidacloprid on nitrogen and phosphorus transformation in soil

Abstract

Microplastics have received increasing attention in soil ecosystems, and their potential impacts on soil properties have raised concerns. Pesticides are the most prevalent pollutants in soil, but their combined effects with microplastics on the soil environment have not been elucidated. In this study, polystyrene microplastics (PS MPs) and imidacloprid (IMI) were added to the soil to investigate their combined effects on soil physicochemical characteristics, nitrogen and phosphorus contents, related transformation activities, and the composition of nitrogen- and phosphorus-transforming microorganisms. The results revealed that the coexistence of PS MPs and IMI led to a significantly higher soil pH level and lower water-stable aggregate (WSA) content. Additionally, it increased the relative abundance of nitrogen- and phosphorus-transforming microorganisms, including ammonia-oxidizing archaea and bacteria, nitrite-oxidizing bacteria, heterotrophic denitrifying bacteria, phosphate-solubilizing bacteria. PS MPs increased the soil potential denitrification rate by 14.53% owing to a significantly higher pH level. However, this promotion disappeared when they combined with IMI. The coexistence of PS MPs and IMI caused a significant decrease in WSA content, thereby improving soil aeration and increasing the relative abundance of phosphate-solubilizing bacteria, which led to a 14.54% and 44.79% increase in soil phosphatase activity and Olsen-P content, respectively. Variance partitioning analysis revealed that the coexistence of PS MPs and IMI mainly influenced nitrogen and phosphorus transformations by altering soil pH and WSA content. These results reveal the combined effects of PS MPs and IMI on soil nitrogen and phosphorus transformations and elucidate soil environmental risks associated with microplastics and pesticides.

Graphical abstract

Keywords

Polystyrene microplastics / Imidacloprid / Nitrogen transformation activities / Olsen-P / Microorganisms

Highlight

	● The addition of microplastics increased the soil potential denitrification rate.
	● The coexistence of PS MPs and IMI led to a higher Olsen-P content.
	● The relative abundance of N- and P-transforming microorganisms was increased.
	● PS MPs and IMI affected N and P transformation by altering soil pH and WSA content.

References

[1] Baćmaga M, Kucharski J, Wyszkowska J. (2015). Microbial and enzymatic activity of soil contaminated with azoxystrobin. Environmental Monitoring and Assessment, 187(10): 615

[2] Bai N, Zhang H, Zhou S, Sun H, Zhao Y, Zheng X, Li S, Zhang J, Lv W. (2020). Long-term effects of straw return and straw-derived biochar amendment on bacterial communities in soil aggregates. Scientific Reports, 10(1): 7891

[3] Bonmatin J M, Giorio C, Girolami V, Goulson D, Kreutzweiser D P, Krupke C, Liess M, Long E, Marzaro M, Mitchell E D A. . (2015). Environmental fate and exposure: neonicotinoids and fipronil. Environmental Science and Pollution Research International, 22(1): 35–67

[4] Burger M, Jackson L E. (2003). Microbial immobilization of ammonium and nitrate in relation to ammonification and nitrification rates in organic and conventional cropping systems. Soil Biology & Biochemistry, 35(1): 29–36

[5] Čuhel J, Simek M, Laughlin R J, Bru D, Cheneby D, Watson C J, Philippot L. (2010). Insights into the effect of soil pH on N₂O and N₂ emissions and denitrifier community size and activity. Applied and Environmental Microbiology, 76(6): 1870–1878

[6] Cycoń M, Piotrowska-Seget Z. (2015a). Biochemical and microbial soil functioning after application of the insecticide imidacloprid. Journal of Environmental Sciences, 27: 147–158

[7] Cycoń M, Piotrowska-Seget Z. (2015b). Community structure of ammonia-oxidizing archaea and ammonia-oxidizing bacteria in soil treated with the insecticide imidacloprid. BioMed Research International, 2015: 582938

[8] Dai H H, Gao J F, Wang Z Q, Zhao Y F, Zhang D. (2020). Behavior of nitrogen, phosphorus and antibiotic resistance genes under polyvinyl chloride microplastics pressures in an aerobic granular sludge system. Journal of Cleaner Production, 256: 120402

[9] Das A C, Mukherjee D. (2000). Soil application of insecticides influences microorganisms and plant nutrients. Applied Soil Ecology, 14(1): 55–62

[10] Das S, Wang W, Reeves S, Dalal R C, Dang Y P, Gonzalez A, Kopittke P M. (2022). Non-target impacts of pesticides on soil N transformations, abundances of nitrifying and denitrifying genes, and nitrous oxide emissions. Science of the Total Environment, 844: 157043

[11] de Gannes V, Eudoxie G, Hickey W J. (2014). Impacts of edaphic factors on communities of ammonia-oxidizing archaea, ammonia-oxidizing bacteria and nitrification in tropical soils. PLoS One, 9(2): e89568

[12] Ding L, Zhang S, Wang X, Yang X, Zhang C, Qi Y, Guo X. (2020). The occurrence and distribution characteristics of microplastics in the agricultural soils of Shaanxi Province, in North-western China. Science of the Total Environment, 720: 137525

[13] Dong Y, Gao M, Qiu W, Song Z. (2021). Effect of microplastics and arsenic on nutrients and microorganisms in rice rhizosphere soil. Ecotoxicology and Environmental Safety, 211: 111899

[14] Dong Y, Gao M, Qiu W, Xiao L, Cheng Z, Peng H, Song Z. (2024). Investigating the impact of microplastics on sulfur mineralization in different soil types: a mechanism study. Journal of Hazardous Materials, 464: 132942

[15] Dong Y, Gao M, Song Z, Qiu W. (2020). As(III) adsorption onto different-sized polystyrene microplastic particles and its mechanism. Chemosphere, 239: 124792

[16] Du P, Wu X, Xu J, Dong F, Liu X, Zheng Y. (2018). Effects of trifluralin on the soil microbial community and functional groups involved in nitrogen cycling. Journal of Hazardous Materials, 353: 204–213

[17] Erguder T H, Boon N, Wittebolle L, Marzorati M, Verstraete W. (2009). Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiology Reviews, 33(5): 855–869

[18] Gao G F, Li P F, Zhong J X, Shen Z J, Chen J, Li Y T, Isabwe A, Zhu X Y, Ding Q S, Zhang S. . (2019). Spartina alterniflora invasion alters soil bacterial communities and enhances soil N₂O emissions by stimulating soil denitrification in mangrove wetland. Science of the Total Environment, 653: 231–240

[19] Horton A A, Walton A, Spurgeon D J, Lahive E, Svendsen C. (2017). Microplastics in freshwater and terrestrial environments: evaluating the current understanding to identify the knowledge gaps and future research priorities. Science of the Total Environment, 586: 127–141

[20] Hou X, Nan H, Chen X, Ge F, Liu Y, Li F, Zhang D, Tian J. (2023). Slow release of attapulgite based nano-enabled glyphosate improves soil phosphatase activity, organic P-pool and proliferation of dominant bacterial community. Environmental Pollution, 336: 122408

[21] Hu J, Xie Z, Zuo J. (2024). Single and combined effects of secondary polyethylene microplastic on the growth of Pak choi and the soil microbiome composition. Frontiers of Environmental Science & Engineering, 18(5): 53

[22] Huang Y, Liu Q, Jia W, Yan C, Wang J. (2020). Agricultural plastic mulching as a source of microplastics in the terrestrial environment. Environmental Pollution, 260: 114096

[23] Jiao K, Yang B, Wang H, Xu W, Zhang C, Gao Y, Sun W, Li F, Ji D. (2022). The individual and combined effects of polystyrene and silver nanoparticles on nitrogen transformation and bacterial communities in an agricultural soil. Science of the Total Environment, 820: 153358

[24] Khan A, Jilani G, Akhtar M S, Naqvi S M S, Rasheed M. (2009). Phosphorus solubilizing bacteria: occurrence, mechanisms and their role in crop production. Journal of Agricultural and Biological Science, 1(1): 48–58

[25] Kravchenko A N, Guber A K. (2017). Soil pores and their contributions to soil carbon processes. Geoderma, 287: 31–39

[26] Lehmann A, Zheng W, Rillig M C. (2017). Soil biota contributions to soil aggregation. Nature Ecology & Evolution, 1(12): 1828–1835

[27] Liu B, Mørkved P T, Frostegård Å, Bakken L R. (2010). Denitrification gene pools, transcription and kinetics of NO, N₂O and N₂ production as affected by soil pH. FEMS Microbiology Ecology, 72(3): 407–417

[28] Liu H, Yang X, Liu G, Liang C, Xue S, Chen H, Ritsema C J, Geissen V. (2017). Response of soil dissolved organic matter to microplastic addition in Chinese loess soil. Chemosphere, 185: 907–917

[29] Liu J L, Liao W H, Zhang Z X, Zhang H T, Wang X J, Meng N. (2007). Effect of phopshate fertilizer and manure on crop yield, soil P accumulation, and the environmental risk assessment. Agricultural Sciences in China, 6(9): 1107–1114

[30] Liu W, Pan T, Liu H, Jiang M, Zhang T. (2023). Adsorption behavior of imidacloprid pesticide on polar microplastics under environmental conditions: critical role of photo-aging. Frontiers of Environmental Science & Engineering, 17(4): 41

[31] Mahon A M, O’Connell B, Healy M G, O’Connor I, Officer R, Nash R, Morrison L. (2017). Microplastics in sewage sludge: Effects of treatment. Environmental Science & Technology, 51(2): 810–818

[32] Mangalassery S, Sjögersten S, Sparkes D L, Sturrock C J, Mooney S J. (2013). The effect of soil aggregate size on pore structure and its consequence on emission of greenhouse gases. Soil & Tillage Research, 132: 39–46

[33] MarschnerB, Brodowski S, DrevesA, GleixnerG, GudeA, GrootesP M, Hamer U, HeimA, JandlG, JiR, et al. (2008). How relevant is recalcitrance for the stabilization of organic matter in soils? Journal of Plant Nutrition and Soil Science, 171(1): 91–110

[34] Mikutta R, Zang U, Chorover J, Haumaier L, Kalbitz K. (2011). Stabilization of extracellular polymeric substances (Bacillus subtilis) by adsorption to and coprecipitation with Al forms. Geochimica et Cosmochimica Acta, 75(11): 3135–3154

[35] NizzettoL, Futter M, LangaasS (2016). Are agricultural soils dumps for microplastics of urban origin? Environmental Science & Technology, 50(20): 10777–10779

[36] Nugnes R, Russo C, Lavorgna M, Orlo E, Kundi M, Isidori M. (2022). Polystyrene microplastic particles in combination with pesticides and antiviral drugs: toxicity and genotoxicity in Ceriodaphnia dubia. Environmental Pollution, 313: 120088

[37] O'Brien S L, Jastrow J D. (2013). Physical and chemical protection in hierarchical soil aggregates regulates soil carbon and nitrogen recovery in restored perennial grasslands. Soil Biology & Biochemistry, 61: 1–13

[38] Qu H, Diao H, Han J, Wang B, Yu G. (2023). Understanding and addressing the environmental risk of microplastics. Frontiers of Environmental Science & Engineering, 17(1): 12

[39] Salehi M H, Beni O H, Harchegani H B, Borujeni I E, Motaghian H R. (2011). Refining soil organic matter determination by loss-on-ignition. Pedosphere, 21(4): 473–482

[40] Sharma S B, Sayyed R Z, Trivedi M H, Gobi T A. (2013). Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus, 2(1): 587

[41] Shi J, Wang J, Lv J, Wang Z, Peng Y, Wang X. (2022). Microplastic presence significantly alters soil nitrogen transformation and decreases nitrogen bioavailability under contrasting temperatures. Journal of Environmental Management, 317: 115473

[42] Singh S, Gupta R, Kumari M, Sharma S. (2015). Nontarget effects of chemical pesticides and biological pesticide on rhizospheric microbial community structure and function in Vigna radiata. Environmental Science and Pollution Research International, 22(15): 11290–11300

[43] Song C, Cao X, Zhou Y, Azzaro M, Monticelli L S, Leonardi M, La Ferla R, Caruso G. (2018). Different pathways of nitrogen and phosphorus regeneration mediated by extracellular enzymes in temperate lakes under various trophic state. Environmental Science and Pollution Research International, 25(31): 31603–31615

[44] Stevens R J, Laughlin R J, Malone J P. (1998). Soil pH affects the processes reducing nitrate to nitrous oxide and di-nitrogen. Soil Biology & Biochemistry, 30(8−9): 1119–1126

[45] Šunta U, Prosenc F, Trebse P, Bulc T G, Kralj M B. (2020). Adsorption of acetamiprid, chlorantraniliprole and flubendiamide on different type of microplastics present in alluvial soil. Chemosphere, 261: 127762

[46] Tan H, Xu M, Li X, Zhang H, Zhang C. (2013). Effects of chlorimuron-ethyl application with or without urea fertilization on soil ammonia-oxidizing bacteria and archaea. Journal of Hazardous Materials, 260: 368–374

[47] Tiwari S, Tripathi P, Mohan D, Singh R S. (2022). Imidacloprid biodegradation using novel bacteria Tepidibacillus decaturensis strain ST1 in batch and in situ microcosm study. Environmental Science and Pollution Research International, 30(22): 61562–61572

[48] Tomkiel M, Baćmaga M, Borowik A, Kucharski J, Wyszkowska J. (2019). Effect of a mixture of flufenacet and isoxaflutole on population numbers of soil-dwelling microorganisms, enzymatic activity of soil, and maize yield. Journal of Environmental Science and Health. Part B, Pesticides, Food Contaminants, and Agricultural Wastes, 54(10): 832–842

[49] Toosi E R, Kravchenko A N, Guber A K, Rivers M L. (2017). Pore characteristics regulate priming and fate of carbon from plant residue. Soil Biology & Biochemistry, 113: 219–230

[50] Wang R, Yang L, Guo M, Lin X, Wang R, Guo S. (2024). Effects of microplastic properties and dissolved organic matter on phosphorus availability in soil and aqueous mediums. Environmental Pollution, 340: 122784

[51] WeilR, Brady N (2017). The Nature and Properties of Soils. 15th edition. New Jersey: Pearson Press Ltd.

[52] Wu C, Pan S, Shan Y, Ma Y, Wang D, Song X, Hu H, Ren X, Ma X, Cui J. . (2022). Microplastics mulch film affects the environmental behavior of adsorption and degradation of pesticide residues in soil. Environmental Research, 214: 114133

[53] Yan Y, Chen Z, Zhu F, Zhu C, Wang C, Gu C. (2021). Effect of polyvinyl chloride microplastics on bacterial community and nutrient status in two agricultural soils. Bulletin of Environmental Contamination and Toxicology, 107(4): 602–609

[54] YangL, Zhu G, JuX, LiuR (2021). How nitrification-related N₂O is associated with soil ammonia oxidizers in two contrasting soils in China? Science of the Total Environment, 770: 143212

[55] Yao H, Gao Y, Nicol G W, Campbell C D, Prosser J I, Zhang L, Han W, Singh B K. (2011). Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Applied and Environmental Microbiology, 77(13): 4618–4625

[56] Yu Y, Battu A K, Varga T, Denny A C, Zahid T M, Chowdhury I, Flury M. (2023). Minimal impacts of microplastics on soil physical properties under environmentally relevant concentrations. Environmental Science & Technology, 57(13): 5296–5304

[57] Zhang C, Lei Y, Qian J, Qiao Y, Liu J, Li S, Dai L, Sun K, Guo H, Sui G. . (2021a). Sorption of organochlorine pesticides on polyethylene microplastics in soil suspension. Ecotoxicology and Environmental Safety, 223: 112591

[58] Zhang G S, Liu Y F. (2018). The distribution of microplastics in soil aggregate fractions in southwestern China. Science of the Total Environment, 642: 12–20

[59] Zhang K, Shi H, Peng J, Wang Y, Xiong X, Wu C, Lam P K S. (2018). Microplastic pollution in China’s inland water systems: a review of findings, methods, characteristics, effects, and management. Science of the Total Environment, 630: 1641–1653

[60] Zhang L, Zhang L X, Xu D Y. (2022). Application of low-intensity ultrasound to enhance simultaneous nitrification/iron-based autotrophic denitrification. Biotechnology Letters, 44(8): 1001–1010

[61] Zhang M, Zhao Y, Qin X, Jia W, Chai L, Huang M, Huang Y. (2019). Microplastics from mulching film is a distinct habitat for bacteria in farmland soil. Science of the Total Environment, 688: 470–478

[62] Zhang Q, Xue C, Wang C. (2015). Effects of imidacloprid on soil microbial communities in different saline soils. Environmental Science and Pollution Research International, 22(24): 19667–19675

[63] Zhang S, Liu X, Hao X, Wang J, Zhang Y. (2020). Distribution of low-density microplastics in the mollisol farmlands of northeast China. Science of the Total Environment, 708: 135091

[64] Zhang X, Li Y, Ouyang D, Lei J, Tan Q, Xie L, Li Z, Liu T, Xiao Y, Farooq T H. . (2021b). Systematical review of interactions between microplastics and microorganisms in the soil environment. Journal of Hazardous Materials, 418: 126288

[65] Zhao T, Lozano Y M, Rillig M C. (2021). Microplastics increase soil pH and secrease microbial activities as a function of microplastic shape, polymer type, and exposure time. Frontiers in Environmental Science, 9: 675803

[66] Zheng Y, Hou L, Newell S, Liu M, Zhou J, Zhao H, You L, Cheng X. (2014). Community dynamics and activity of ammonia-oxidizing prokaryotes in intertidal sediments of the Yangtze estuary. Applied and Environmental Microbiology, 80(1): 408–419

[67] Zhou J, Xu H, Xiang Y, Wu J. (2024). Effects of microplastics pollution on plant and soil phosphorus: a meta-analysis. Journal of Hazardous Materials, 461: 132705

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