Enhancing the biodegradability and environmental impact of microplastics utilizing Eisenia fetida earthworms with treated low-density polyethylene for sustainable plastic management
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Abstract
Low-density polyethylene (LDPE) is widely used in food packaging and agricultural mulching, but its disposal generates macro, meso and microplastics that infiltrate the food chain and carry harmful substances. The present study aimed to improve remediation strategies for soils contaminated with LDPE and enhance the survivability of Eisenia fetida. The study dissolved LDPE in trichloroethylene and treated it with starch, hydrogen peroxide, nitric acid and acetic acid, initiating thermo-oxidative reactions. The treatment decreased LDPE's crystallinity index from 48.48% to 44.06% (single treatment), 44.06% to 40.02% (double treatment) and 40.02% to 32.98% (triple treatment), achieving a 15.5% reduction in crystallinity. LDPE microplastics with 40.02% crystallinity showed lower mortality rates in Eisenia fetida earthworms compared to those with 44.06% and 32.98% crystallinity and untreated LDPE. When introduced to E. fetida, microbiota in the earthworm casts included unidentified species from Pseudomonas and Zoopagomycota, known polyethylene degraders. Microbial analysis of treated LDPE microplastics showed changes in gut microbiota, including potential degraders from Aeromonas and Malassezia restricta. XRD (X-ray diffraction techniques analyses) and FTIR(Fourier Transform Infrared Spectroscopy) analyses provided insights into distinct LDPE degradation patterns, identifying hydroxyl and carboxylic groups as functional groups. The study also investigated the ability of altered microflora with treated microplastics to degrade LDPE, favouring decreased earthworm mortality rates. The crystallinity index of treated polyethylene further reduced from 40.02% to 23.58% after 21 days of exposure to E. fetida. This research advances the understanding of oxidised plastics' ecological impacts and will help to develop environmentally sustainable and biodegradable LDPE.
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Keywords
Eisenia fetida, Low-density polyethylene, Microplastics, Thermo-oxidative reaction
References
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Atanasova, N. Stoitsova, S. Paunova-Krasteva, T. & Kambourova, M. (2021). Plastic Degradation by Extremophilic Bacteria. International Journal of Molecular Sciences, 22(11), 5610. https://doi.org/10.3390/ijms22115610
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Curlevski, N J A. Xu, Z. Anderson, I C. & Cairney, J W G. (2010). Converting Australian tropical rainforest to native Araucariaceae plantations alters soil fungal communities. Soil Biol.Biochem.,42,1,14–20,doi: https://doi.org/10.1016/j.soilbio.2009.08.001
Dang, T C H. Nguyen, D T. Thai, H. Nguyen, T C. Tran, T T H. Le, V H. Nguyen, V H. Tran, X B. Pham, T P T. & Nguyen, T G. (2018). Plastic degradation by thermophilic Bacillus sp. BCBT21 isolated from composting agricultural residual in Vietnam. Adv. Nat. Sci. Nanosci. Nanotechnol. 9:015014. doi: 10.1088/2043-6254/aaabaf
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Esmaeili, A. Pourbabaee, A A. Alikhani, H A. Shabani, F. & Esmaeili, E. (2013). Biodegradation of low-density polyethylene (LDPE) by mixed culture of Lysinibacillus xylanilyticus and Aspergillus niger in soil. PLoS ONE 8:e71720, doi: 10.1371/journal.pone.0071720.
FTIR Functional Group Table with Search -InstaNANO.9. Retrieved 2023 Jan 29, https://instanano.com/all/ characterization/ftir/ftir-functional-group-search/
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Hakkarainen, M. & Albertsson, AC. (2004). Environmental Degradation of Polyethylene. In: Albertsson, AC. (eds) Long Term Properties of Polyolefins. Advances in Polymer Science,169. Springer, Berlin, Heidelberg. https://doi.org/10.1007/b13523
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Huerta, Lwanga E. Thapa, B. Yang, X. Gertsen, H. Salánki, T. & Geissen, V. et al., (2018). Decay of low-density polyethylene by bacteria extracted from earthworm's guts: A potential for soil restoration. Sci.Total Environ. 624, 753–757.10.1016/j.scitotenv.2017.12.144
Koutny, M.Lemaire, J. & Delort, A M. (2006). “Biodegradation of polyethylene films with prooxidant additives, Chemosphere,64,8,1243–1252, doi: https://doi.org/10.1016/j.chemosphere.2005.12.060
Koutny, M. Sancelme, M. Dabin, C. Pichon, N. Delort, A M. & Lemaire, J. (2006) Acquired biodegradability of polyethylenes containing pro-oxidant additives. Polymer Degradation and Stability,91, 7,1495-1503,https://doi:org/10.1016/j.polymdegradstab.2005.10.007.
Kumar, R. Pandit, P. Kumar, D. Patel, Z. Pandya, L. Kumar, M. Joshi, C. & Joshi, M. (2021). Landfill microbiome harbour plastic degrading genes: a metagenomic study of solid waste dumping site of Gujarat, India, Sci. Total Environ. 779 (146184) 146184, https://doi.org/10.1016/j.scitotenv.2021.146184
Kumari, A. Chaudhary, D. R. & Jha, B. (2019). Destabilization of polyethylene and polyvinylchloride structure by marine bacterial strain. Environ. Sci., Pollut. Res. Int. 26,1507–1516.10.1007/s11356-018-3465-1, https://doi.org/10.1007/s11356-018-3465-1
Lacerda, A L D F. Proietti, M C. Secchi, E R. & Taylor, J D. (2020). Diverse groups of fungi are associated with plastics in the surface waters of theWestern South Atlantic and the Antarctic Peninsula. Mole. Ecol. 2020,15444. doi: 10.1111/mec.15444
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Maroof. Lalina. Khan, M I. Yoo, H S. Kim, S, Park, H T. Ahmad, B. & Sadiq Azam, S. (2020). Identification and characterization of low density polyethylene-degrading bacteria isolated from soils of waste disposal sites. Environmental Engineering Research. https://doi.org/10.4491/eer.2020.167
Mayser, P. (2015). Medium chain fatty acid ethyl esters—activation of antimicrobial effects by Malassezia enzymes. Mycoses, 58,215–19, https://doi.org/10.1111/myc.12300
Montazer, Z. Habibi, N M B. Mohebbi, M. & Oromiehei, A. (2018). Microbial degradation of UV-pretreated low-density polyethylene films by novel polyethylene-degrading bacteria isolated from plastic-dump soil. J Polym Environ 26:3613–3625, https://doi.org/10.1007/s10924-018-1245-0
Nag, M. Lahiri, D. Dutta, B. Jadav, G. & Ray RR.(2021). Biodegradation of used polyethylene bags by a new marine strain of Alcaligenes faecalis LNDR-1. Environ. Sci. Pollut. Res. 28,41365–41379, https://doi.org/10.1007/s11356-021-13704-0
OECD ( 1984).Test No. 207: Earthworm, Acute Toxicity Tests..
Ojeda, T. et al., (2009). Abiotic and biotic degradation of oxo-biodegradable foamed polystyrene. Polym. Degrad. Stab.,94,12,2128–2133,doi: https://doi.org/10.1016/j.polymdegradstab.2009.09.012.
Palanna, A P. & Sayantan, D. (2023). A primary study on the degradation of low-density polyethylene treated with select oxidizing agents and starch. Journal of Applied and Natural Science. https://doi.org/10.31018/jans.v15i2.4645
Park, S Y. & Kim, C G. (2019). Biodegradation of micro-polyethylene particles by bacterial colonization of a mixed microbial consortium isolated from a landfill site. Chemosphere, 222,527–533. https://doi.org/10.1 016/j.chemosphere.2019.01.159
Percent Crystallinity by the XRD Integration Method. Retrieved 2023 Feb 26, https://mcl.mse.utah.edu/xrd crystallinity-by-integration/
Ritz, K. McNicol, J W. Nunan, N. Grayston, S. Millard, P. Atkinson, D. Gollotte, A. Habeshaw, D. Boag, B. Clegg, C, D. Griffiths, B, S. Wheatley, R E. Glover, L A. McCaig, A E. & Prosser, J I. (2004). Spatial structure in soil chemical and microbiological properties in an upland grassland. FEMS Microbiol Ecol 49(2),191–205. https://doi.org/10.1016/j.femsec.2004.03.005
Selke, S. Auras, R. Nguyen, T A. Castro, A E. & Cheruvathur, R. Liu, Y. (2015). Evaluation of biodegradation-promoting additives for plastics. Environ Sci Technol, 49, 3769–3777, https://doi.org/10.1021/es504258u
Sivan, A. (2011), New perspectives in plastic biodegradation. Curr. Opin. Biotechnol.,422–426 doi: https://doi.org/10.1016/j.copbio.2011.01.013.
Sudhakar, M. Doble, M. Murthy, P S.& Venkatesan, R. (2008). Marine microbe-mediated biodegradation of low-and high-density polyethylenes. Int Biodeterior Biodegrad, 61, 203–213, https://doi.org/10.1016/j.ibiod.2007.07.011
Zhou, X. Liang, W. Zhang, Y. et al. (2021). Effect of earthworm Eisenia fetida epidermal mucus on the vitality and pathogenicity of Beauveria bassiana. Sci Rep., 11, 13915 https://doi.org/10.1038/s41598-021-92694-y
Albertsson, A C. & Karlsson, S. (1990). The influence of biotic and abiotic environments on the degradation of polyethylene. Prog Polym Sci , 15:177–192, https://doi.org/10.1016/0079-6700(90)90027-X
Ambika, D K. Lakshmi, B, K, M. Hemalatha, K. P. J. (2015). Degradation of low density polythene by Achromobacter denitrificans strain s1, a novel marine isolate. Int. J. Rec. Sci. Res. 6, 5454–5464.
Atanasova, N. Stoitsova, S. Paunova-Krasteva, T. & Kambourova, M. (2021). Plastic Degradation by Extremophilic Bacteria. International Journal of Molecular Sciences, 22(11), 5610. https://doi.org/10.3390/ijms22115610
Cui, W. Gao, P. Zhang, M. Wang, L. Sun, H. & Liu, C. (2022). Adverse effects of microplastics on earthworms: A critical review, Sci. Total Environ.,850,158041, 2022, doi: https://doi.org/10.1016/j.scitotenv.2022.158041
Curlevski, N J A. Xu, Z. Anderson, I C. & Cairney, J W G. (2010). Converting Australian tropical rainforest to native Araucariaceae plantations alters soil fungal communities. Soil Biol.Biochem.,42,1,14–20,doi: https://doi.org/10.1016/j.soilbio.2009.08.001
Dang, T C H. Nguyen, D T. Thai, H. Nguyen, T C. Tran, T T H. Le, V H. Nguyen, V H. Tran, X B. Pham, T P T. & Nguyen, T G. (2018). Plastic degradation by thermophilic Bacillus sp. BCBT21 isolated from composting agricultural residual in Vietnam. Adv. Nat. Sci. Nanosci. Nanotechnol. 9:015014. doi: 10.1088/2043-6254/aaabaf
Dongxing, Z. Yucui, N. Jiabin, L. et al. (2016). Effects of oxidative stress reaction for the Eisenia fetida with exposure in Cd2+ . Environ. Sci. Pollut. Res., 23, 21883–21893. https://doi.org/10.1007/s11356-016-7422-6
Ekanayaka, A H. Tibpromma, S. Dai, D. Xu, R. Suwannarach, N. Stephenson, S L. Dao, C. & Karunarathna, S C. (2022). A Review of the Fungi That Degrade Plastic. J Fungi (Basel). 8(8),772. doi: 10.3390/jof8080772. PMID: 35893140; PMCID: PMC9330918
Esmaeili, A. Pourbabaee, A A. Alikhani, H A. Shabani, F. & Esmaeili, E. (2013). Biodegradation of low-density polyethylene (LDPE) by mixed culture of Lysinibacillus xylanilyticus and Aspergillus niger in soil. PLoS ONE 8:e71720, doi: 10.1371/journal.pone.0071720.
FTIR Functional Group Table with Search -InstaNANO.9. Retrieved 2023 Jan 29, https://instanano.com/all/ characterization/ftir/ftir-functional-group-search/
Hadad, D. Geresh, S. & Sivan, A. (2005). Biodegradation of polyethylene by the thermophilic bacterium Brevibacillus borstelensis. J Appl Microbiol., 98,1093–1100, https://doi.org/10.1111/j.1365-2672.2005.02553.x
Hakkarainen, M. & Albertsson, AC. (2004). Environmental Degradation of Polyethylene. In: Albertsson, AC. (eds) Long Term Properties of Polyolefins. Advances in Polymer Science,169. Springer, Berlin, Heidelberg. https://doi.org/10.1007/b13523
Hannah, R. Veronika, S. & Max, R (2023). Plastic Pollution. Published online at OurWorldInData.org. Retrieved from: https://ourworldindata.org/plastic-pollution [Online Resource]
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, Sci. TotalEnviron.,586,127–141,doi:https://doi.org/10.1016/j.scitotenv.2017.01.190
Huerta, Lwanga E. Thapa, B. Yang, X. Gertsen, H. Salánki, T. & Geissen, V. et al., (2018). Decay of low-density polyethylene by bacteria extracted from earthworm's guts: A potential for soil restoration. Sci.Total Environ. 624, 753–757.10.1016/j.scitotenv.2017.12.144
Koutny, M.Lemaire, J. & Delort, A M. (2006). “Biodegradation of polyethylene films with prooxidant additives, Chemosphere,64,8,1243–1252, doi: https://doi.org/10.1016/j.chemosphere.2005.12.060
Koutny, M. Sancelme, M. Dabin, C. Pichon, N. Delort, A M. & Lemaire, J. (2006) Acquired biodegradability of polyethylenes containing pro-oxidant additives. Polymer Degradation and Stability,91, 7,1495-1503,https://doi:org/10.1016/j.polymdegradstab.2005.10.007.
Kumar, R. Pandit, P. Kumar, D. Patel, Z. Pandya, L. Kumar, M. Joshi, C. & Joshi, M. (2021). Landfill microbiome harbour plastic degrading genes: a metagenomic study of solid waste dumping site of Gujarat, India, Sci. Total Environ. 779 (146184) 146184, https://doi.org/10.1016/j.scitotenv.2021.146184
Kumari, A. Chaudhary, D. R. & Jha, B. (2019). Destabilization of polyethylene and polyvinylchloride structure by marine bacterial strain. Environ. Sci., Pollut. Res. Int. 26,1507–1516.10.1007/s11356-018-3465-1, https://doi.org/10.1007/s11356-018-3465-1
Lacerda, A L D F. Proietti, M C. Secchi, E R. & Taylor, J D. (2020). Diverse groups of fungi are associated with plastics in the surface waters of theWestern South Atlantic and the Antarctic Peninsula. Mole. Ecol. 2020,15444. doi: 10.1111/mec.15444
Linnaeus, C. (1758). Systema naturae per regna tria naturae: secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Stockholm, Sweden: Laurentii Salvii (in Latin), https://doi.org/10.5962/bhl.title.542
Maroof. Lalina. Khan, M I. Yoo, H S. Kim, S, Park, H T. Ahmad, B. & Sadiq Azam, S. (2020). Identification and characterization of low density polyethylene-degrading bacteria isolated from soils of waste disposal sites. Environmental Engineering Research. https://doi.org/10.4491/eer.2020.167
Mayser, P. (2015). Medium chain fatty acid ethyl esters—activation of antimicrobial effects by Malassezia enzymes. Mycoses, 58,215–19, https://doi.org/10.1111/myc.12300
Montazer, Z. Habibi, N M B. Mohebbi, M. & Oromiehei, A. (2018). Microbial degradation of UV-pretreated low-density polyethylene films by novel polyethylene-degrading bacteria isolated from plastic-dump soil. J Polym Environ 26:3613–3625, https://doi.org/10.1007/s10924-018-1245-0
Nag, M. Lahiri, D. Dutta, B. Jadav, G. & Ray RR.(2021). Biodegradation of used polyethylene bags by a new marine strain of Alcaligenes faecalis LNDR-1. Environ. Sci. Pollut. Res. 28,41365–41379, https://doi.org/10.1007/s11356-021-13704-0
OECD ( 1984).Test No. 207: Earthworm, Acute Toxicity Tests..
Ojeda, T. et al., (2009). Abiotic and biotic degradation of oxo-biodegradable foamed polystyrene. Polym. Degrad. Stab.,94,12,2128–2133,doi: https://doi.org/10.1016/j.polymdegradstab.2009.09.012.
Palanna, A P. & Sayantan, D. (2023). A primary study on the degradation of low-density polyethylene treated with select oxidizing agents and starch. Journal of Applied and Natural Science. https://doi.org/10.31018/jans.v15i2.4645
Park, S Y. & Kim, C G. (2019). Biodegradation of micro-polyethylene particles by bacterial colonization of a mixed microbial consortium isolated from a landfill site. Chemosphere, 222,527–533. https://doi.org/10.1 016/j.chemosphere.2019.01.159
Percent Crystallinity by the XRD Integration Method. Retrieved 2023 Feb 26, https://mcl.mse.utah.edu/xrd crystallinity-by-integration/
Ritz, K. McNicol, J W. Nunan, N. Grayston, S. Millard, P. Atkinson, D. Gollotte, A. Habeshaw, D. Boag, B. Clegg, C, D. Griffiths, B, S. Wheatley, R E. Glover, L A. McCaig, A E. & Prosser, J I. (2004). Spatial structure in soil chemical and microbiological properties in an upland grassland. FEMS Microbiol Ecol 49(2),191–205. https://doi.org/10.1016/j.femsec.2004.03.005
Selke, S. Auras, R. Nguyen, T A. Castro, A E. & Cheruvathur, R. Liu, Y. (2015). Evaluation of biodegradation-promoting additives for plastics. Environ Sci Technol, 49, 3769–3777, https://doi.org/10.1021/es504258u
Sivan, A. (2011), New perspectives in plastic biodegradation. Curr. Opin. Biotechnol.,422–426 doi: https://doi.org/10.1016/j.copbio.2011.01.013.
Sudhakar, M. Doble, M. Murthy, P S.& Venkatesan, R. (2008). Marine microbe-mediated biodegradation of low-and high-density polyethylenes. Int Biodeterior Biodegrad, 61, 203–213, https://doi.org/10.1016/j.ibiod.2007.07.011
Zhou, X. Liang, W. Zhang, Y. et al. (2021). Effect of earthworm Eisenia fetida epidermal mucus on the vitality and pathogenicity of Beauveria bassiana. Sci Rep., 11, 13915 https://doi.org/10.1038/s41598-021-92694-y
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Enhancing the biodegradability and environmental impact of microplastics utilizing Eisenia fetida earthworms with treated low-density polyethylene for sustainable plastic management. (2024). Journal of Applied and Natural Science, 16(3), 1202-1212. https://doi.org/10.31018/jans.v16i3.5771
