Differential effects of microplastics on soil organic carbon via lignin phenols and amino sugars in soil aggregates

Abstract

Accumulation of plant- and microbial-derived carbon together determines the stability of soil organic carbon (SOC) pools. To explore the accumulation characteristics and comparative contributions of organic carbon from diverse origins within soil aggregates exposed to microplastic pollution, we conducted corn pot experiments using biodegradable (polylactic acid; PLA) and conventional microplastics (polyethylene; PE) to examine the effects of microplastic pollution on microbial and plant derived carbon in macroaggregates (0.25–2 mm) and microaggregates (< 0.25 mm). Exposure to PE and PLA microplastics diminished the microbial necromass carbon in macroaggregates and its contribution to SOC, whereas their effects on microbial necromass carbon in microaggregates fluctuated depending on microplastic concentration. Due to the increased turnover rates and structural modifications experienced by biodegradable microplastics, PLA treatments yielded superior microbial necromass carbon content than PE treatments. PE reduced plant-derived carbon and its contribution to SOC across both aggregates, whereas PLA exerted a dosage-related effect on plant-derived carbon. Remarkably, 87%–408% of additional SOC in PLA treatment was primarily derived from other carbons, possibly indicating the inclusion of microplastic derived carbon in SOC assessments, thereby inflating SOC estimates. Under microplastic pollution, plant derived carbon dominated the accumulation of SOC in macroaggregates, whereas microbial derived carbon dominated SOC accumulation in microaggregates. Furthermore, macroaggregates exhibited higher SOC concentrations than microaggregates, with PLA treatments demonstrating superiority over PE treatments. Remarkably, microplastics supported the stability of SOC in microaggregates without exerting similar effects on macroaggregates.

Graphical abstract

Keywords

Microplastic pollution / Soil organic carbon / Soil aggregate / Plant lignin / Microbial necromass

Highlight

	● Polyethylene microplastics reduced plant derived carbon and its contribution to SOC.
	● The accumulation of SOC in macroaggregates was higher than that in microaggregates.
	● The additional SOC was estimated to be microplastic derived carbon.
	● Microplastics improved SOC stability in microaggregates.
	● Microplastic type and dose governed plant and microbial derived carbon.

References

[1] BaoS D (2000). Soil Agrochemical Analysis. Beijing: China Agriculture Press

[2] Bian W, An L, Zhang S, Feng J, Sun D, Yao Y, Shen T, Yang Y, Zhang M. (2022). The long-term effects of microplastics on soil organomineral complexes and bacterial communities from controlled-release fertilizer residual coating. Journal of Environmental Management, 304: 114193

[3] Bläsing M, Amelung W. (2018). Plastics in soil: analytical methods and possible sources. Science of the Total Environment, 612: 422–435

[4] Bossio D A, Scow K M. (1998). Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microbial Ecology, 35(3): 265–278

[5] Cao S, Zhou Y, Zhou Y, Zhou X, Zhou W. (2021). Soil organic carbon and soil aggregate stability associated with aggregate fractions in a chronosequence of citrus orchards plantations. Journal of Environmental Management, 293: 112847

[6] Chen H, Wang Y, Sun X, Peng Y, Xiao L. (2020). Mixing effect of polylactic acid microplastic and straw residue on soil property and ecological function. Chemosphere, 243: 125271

[7] Chen L, Han L, Wang F, Chen Q, Huang H, Wang J, Ma C, Sun K, Rillig M C, Kuzyakov Y, Yang Z. (2025). Polylactic acid microplastics induced negative priming and improved carbon sequestration via microbial processes in different paddy soils. Soil Biology & Biochemistry, 201: 109653

[8] Chen X, Hu Y, Xia Y, Zheng S, Ma C, Rui Y, He H, Huang D, Zhang Z, Ge T. . (2021). Contrasting pathways of carbon sequestration in paddy and upland soils. Global Change Biology, 27(11): 2478–2490

[9] Cole M, Webb H, Lindeque P K, Fileman E S, Halsband C, Galloway T S. (2014). Isolation of microplastics in biota-rich seawater samples and marine organisms. Scientific Reports, 4(1): 4528

[10] Collignon A, Hecq J H, Galgani F, Collard F, Goffart A. (2014). Annual variation in neustonic micro- and meso-plastic particles and zooplankton in the Bay of Calvi (Mediterranean–Corsica). Marine Pollution Bulletin, 79(1−2): 293–298

[11] Cotrufo M F, Ranalli M G, Haddix M L, Six J, Lugato E. (2019). Soil carbon storage informed by particulate and mineral-associated organic matter. Nature Geoscience, 12(12): 989–994

[12] de Souza Machado A A, Lau C W, Kloas W, Bergmann J, Bachelier J B, Faltin E, Becker R, Gorlich A S, Rillig M C. (2019). Microplastics can change soil properties and affect plant performance. Environmental Science & Technology, 53(10): 6044–6052

[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] DrisR, Gasperi J, SaadM, MirandeC, TassinB (2016). Synthetic fibers in atmospheric fallout: a source of microplastics in the environment? Marine Pollution Bulletin, 104(1–1): 290–293

[15] Fang Z, Sallach J B, Hodson M E. (2024). Size- and concentration-dependent effects of microplastics on soil aggregate formation and properties. Journal of Hazardous Materials, 465: 133395

[16] Fojt J, David J, Prikryl R, Rezacova V, Kucerik J. (2020). A critical review of the overlooked challenge of determining micro-bioplastics in soil. Science of the Total Environment, 745: 140975

[17] Hammesfahr U, Heuer H, Manzke B, Smalla K, Thiele-Bruh S. (2008). Impact of the antibiotic sulfadiazine and pig manure on the microbial community structure in agricultural soils. Soil Biology & Biochemistry, 40(7): 1583–1591

[18] Hidalgo-Ruz V, Gutow L, Thompson R C, Thiel M. (2012). Microplastics in the marine environment: a review of the methods used for identification and quantification. Environmental Science & Technology, 46(6): 3060–3075

[19] Hou J, Xu X, Yu H, Xi B, Tan W. (2021). Comparing the long-term responses of soil microbial structures and diversities to polyethylene microplastics in different aggregate fractions. Environment International, 149: 106398

[20] Ihenetu S C, Enyoh C E, Wang C, Li G. (2024). Sustainable urbanization and microplastic management: implications for human health and the environment. Urban Science, 8: 252

[21] Jiang Y, Jin C, Sun B. (2014). Soil aggregate stratification of nematodes and ammonia oxidizers affects nitrification in an acid soil. Environmental Microbiology, 16(10): 3083–3094

[22] Jiang Y, Liu M, Zhang J, Chen Y, Chen X, Chen L, Li H, Zhang X, Sun B. (2017). Nematode grazing promotes bacterial community dynamics in soil at the aggregate level. ISME Journal, 11(12): 2705–2717

[23] Ju T, Yang K, Chang L, Zhang K, Wang X, Zhang J, Xu B, Li Y. (2023). Microplastics sequestered in the soil affect the turnover and stability of soil aggregates: a review. Science of the Total Environment, 904: 166776

[24] Karamanlioglu M, Preziosi R, Robson G D. (2017). Abiotic and biotic environmental degradation of the bioplastic polymer poly (lactic acid): a review. Polymer Degradation & Stability, 137: 122–130

[25] Khan I, Tariq M, Alabbosh K F, Rehman A, Jalal A, Khan A A, Farooq M, Li G, Iqbal B, Ahmad N. . (2024). Soil microplastics: impacts on greenhouse gasses emissions, carbon cycling, microbial diversity, and soil characteristics. Applied Soil Ecology, 197: 105343

[26] Lehmann J, Bossio D A, Kogel-Knabner I, Rillig M C. (2020). The concept and future prospects of soil health. Nature Reviews. Earth & Environment, 1(10): 544–553

[27] Li H Z, Zhu D, Lindhardt J H, Lin S M, Ke X, Cui L. (2021). Long-term fertilization history alters effects of microplastics on soil properties, microbial communities, and functions in diverse farmland ecosystem. Environmental Science & Technology, 55(8): 4658–4668

[28] Lian J, Liu W, Meng L, Wu J, Zeb A, Cheng L, Lian Y, Sun H. (2021). Effects of microplastics derived from polymer-coated fertilizer on maize growth, rhizosphere, and soil properties. Journal of Cleaner Production, 318: 128571

[29] Liang C, Amelung W, Lehmann J, Kastner M. (2019). Quantitative assessment of microbial necromass contribution to soil organic matter. Global Change Biology, 25(11): 3578–3590

[30] Liang C, Fujinuma R, Balser T C. (2008). Comparing PLFA and amino sugars for microbial analysis in an Upper Michigan old growth forest. Soil Biology & Biochemistry, 40(8): 2063–2065

[31] 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

[32] Liu Y, Huang Q, Hu W, Qin J, Zheng Y, Wang J, Wang Q, Xu Y, Guo G, Hu S, Xu L. (2021). Effects of plastic mulch film residues on soil-microbe-plant systems under different soil pH conditions. Chemosphere, 267: 128901

[33] Ma T, Yang Z, Shi B, Gao W, Li Y, Zhu J, He J S. (2023). Phosphorus supply suppressed microbial necromass but stimulated plant lignin phenols accumulation in soils of alpine grassland on the Tibetan Plateau. Geoderma, 431: 116376

[34] MengFYang XRiksenMGeissenV (2022). Effect of different polymers of microplastics on soil organic carbon and nitrogen: a mesocosm experiment. Environmental Research, 204(Pt A): 111938

[35] Murugan R, Djukic I, Keiblinger K, Zehetner F, Bierbaumer M, Zechmeister-Bolternstern S, Joergernsen R G. (2019). Spatial distribution of microbial biomass and residues across soil aggregate fractions at different elevations in the Central Austrian Alps. Geoderma, 341: 249

[36] Otto A, Shunthirasingham C, Simpson M J. (2005). A comparison of plant and microbial biomarkers in grassland soils from the Prairie Ecozone of Canada. Organic Geochemistry, 36(3): 425–448

[37] Qi Y, Yang X, Pelaez A M, Huerta Lwanga E, Beriot N, Gertsen H, Garbeva P, Geissen V. (2018). Macro- and micro-plastics in soil-plant system: effects of plastic mulch film residues on wheat (Triticum aestivum) growth. Science of the Total Environment, 645: 1048–1056

[38] Rillig M C. (2018). Microplastic disguising as soil carbon storage. Environmental Science & Technology, 52(11): 6079–6080

[39] Shao S, Zhao Y, Zhang W, Hu G, Xie H, Yan J, Han S, He H, Zhang X. (2017). Linkage of microbial residue dynamics with soil organic carbon accumulation during subtropical forest succession. Soil Biology & Biochemistry, 114: 114–120

[40] Sheridan E A, Fonvielle J A, Cottingham S, Zhang Y, Dittmar T, Aldridge D C, Tanentzap A J. (2022). Plastic pollution fosters more microbial growth in lakes than natural organic matter. Nature Communications, 13(1): 4175

[41] Shi J, Deng L, Gunina A, Alharbi S, Wang K, Li J, Liu Y, Shangguan Z, Kuzyakov Y. (2023). Carbon stabilization pathways in soil aggregates during long-term forest succession: implications from δ13C signatures. Soil Biology & Biochemistry, 180: 108988

[42] Shi J, Tanentzap A J, Sun Y, Wang J, Xing B, Rillig M C, Li C, Jin L, Wang F, Adyel T M. . (2025). Microplastics generate less mineral protection of soil carbon and more CO₂ emissions. Advanced Science, 12(7): 2409585

[43] Shruti V C, Kutralam-Muniasamy G. (2019). Bioplastics: missing link in the era of microplastics. Science of the Total Environment, 697: 134139

[44] Six J, Bossuyt H, Degryze S, Denef K. (2004). A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil & Tillage Research, 79(1): 7–31

[45] Sun Y, Li X, Cao N, Duan C, Ding C, Huang Y, Wang J. (2022). Biodegradable microplastics enhance soil microbial network complexity and ecological stochasticity. Journal of Hazardous Materials, 439: 129610

[46] ThompsonR C, Olsen Y, MitchellR P, DavisA, Rowland S J, JohnA W G, McGonigleD, Russell A E (2004). Lost at sea: where is all the plastic? Science, 304(5672): 838

[47] Wang F, Wang Q, Adams C A, Sun Y, Zhang S. (2022). Effects of microplastics on soil properties: current knowledge and future perspectives. Journal of Hazardous Materials, 424: 127531

[48] Wang J, Song M, Lu M, Wang C, Zhu C, Dou X. (2024). Insights into effects of conventional and biodegradable microplastics on organic carbon decomposition in different soil aggregates. Environmental Pollution, 359: 124751

[49] Wang R, Dorodnikov M, Yang S, Zhang Y, Filley T R, Turco R F, Zhang Y, Xu Z, Li H, Jiang Y. (2015). Responses of enzymatic activities within soil aggregates to 9-year nitrogen and water addition in a semi-arid grassland. Soil Biology & Biochemistry, 81: 159–167

[50] Wang X, Tian Q, Li Q, Liao C, He M, Liu F. (2018). Lignin characteristics in soil profiles in different plant communities in a subtropical mixed forest. Journal of Plant Ecology, 11(4): 560–568

[51] Wei X F, Bohlén M, Lindblad C, Hedenqvist M, Hakonen A. (2021). Microplastics generated from a biodegradable plastic in freshwater and seawater. Water Research, 198: 117123

[52] Xiang Y, Rillig M C, Peñuelas J, Sardans J, Liu Y, Yao B, Li Y. (2024). Global responses of soil carbon dynamics to microplastic exposure: a data synthesis of laboratory studies. Environmental Science & Technology, 58(13): 5821–5831

[53] Yang L, Zhang Y, Kang S, Wang Z, Wu C. (2021). Microplastics in soil: a review on methods, occurrence, sources, and potential risk. Science of the Total Environment, 801: 149616

[54] Yang Y, Dou Y, Wang B, Wang Y, Liang C, An S, Soromotin A, Kuzyakov Y. (2022). Increasing contribution of microbial residues to soil organic carbon in grassland restoration chronosequence. Soil Biology & Biochemistry, 170: 108688

[55] Yu H, Liu H, Yang K, Xi B, Tan W. (2024). Differential carbon accumulation of microbial necromass and plant lignin by pollution of polyethylene and polylactic acid microplastics in soil. Environmental Pollution, 358: 124504

[56] Yu H, Zhang Z, Zhang Y, Song Q, Fan P, Xi B, Tan W. (2021). Effects of microplastics on soil organic carbon and greenhouse gas emissions in the context of straw incorporation: a comparison with different types of soil. Environmental Pollution, 288: 117733

[57] Yu Y, Zhang Z, Zhang Y, Jia H, Li Y, Yao H. (2023). Abundances of agricultural microplastics and their contribution to the soil organic carbon pool in plastic film mulching fields of Xinjiang, China. Chemosphere, 316: 137837

[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 H, Huang Y, Shen J, Xu F, Hou H, Xie C, Wang B, An S. (2024). Mechanism of polyethylene and biodegradable microplastic aging effects on soil organic carbon fractions in different land-use types. Science of the Total Environment, 912: 168961

[60] Zhang Q, Li X, Liu J, Han L, Wang X, Liu H, Xu M, Yang G, Ren C, Han X. (2023). The contribution of microbial necromass carbon to soil organic carbon in soil aggregates. Applied Soil Ecology, 190: 104985

[61] Zhang X, Amelung W. (1996). Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils. Soil Biology & Biochemistry, 28(9): 1201–1206

[62] Zhou J, Feng W, Brown R W, Yang H, Shao G, Shi L, Gui H, Xu J, Li F M, Jones D L. . (2024). Microplastic contamination accelerates soil carbon loss through positive priming. Science of the Total Environment, 954: 176273

[63] Zhou J, Jia R, Brown R W, Yang Y, Zeng Z, Jones D L, Zang H. (2023). The long-term uncertainty of biodegradable mulch film residues and associated microplastics pollution on plant-soil health. Journal of Hazardous Materials, 442: 130055

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