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The soil microbiome, which is shaped by gut-related activities of earthworms, is affected by microplastic contamination. However, the influence of microplastics on earthworm gut and cast microbiomes has been poorly explored. Here, we investigated the influence of microplastics (1% in soil, w/w) on soil physicochemical properties and bacterial communities during gut passage and cast aging of Lumbricus terrestris. Microplastics used in agricultural film production were selected, i.e., low density polyethylene, polylactic acid and polybutylene adipate terephthalate (PBAT). Different niches, including pre-ingestion soil, gut content and aged casts (from 0 to 180 days), were studied. Results showed that microplastics possibly enhanced the gut passage-derived difference between pre-ingestion soil and fresh cast in terms of pH, ammonium, nitrate and nitrite, and dissolved organic carbon. But such effects mostly faded out after 180 days of aging. The composition, as well as the alpha and beta diversity of both the total (DNA) and active (RNA) bacterial communities were decisively shaped by their niche (R2: 0.22–0.63, p < 0.001, PERMANOVA), rather than the presence/absence or the types of MPs. Nevertheless, biomarkers indicative of PBAT treatment were identified, and functional prediction for the active community showed that bacterial communities of this treatment had higher potentials for hydrocarbon degradation (4.9–7.8 times that of the microplastic-free treatment in gut and aged casts). We also identified a "Soil-related core community" and a "Gut-related core community" (contributing to 39.2%–50.2% of the cast microbiome), which possibly neutralized microplastic impacts and maintained the structure and function of bacterial communities during the soil–gut–cast transit. Our findings indicate that the tested microplastics exerted a minor influence on the bacterial communities during the cast aging process, microplastics in aged casts might not necessarily have significant additional influence on the soil microbiome when they are incorporated into soils. Future studies testing different soils, polymers, and earthworm species, under field conditions are recommended to help enhance current knowledge of the influence of microplastics on earthworm cast microbiomes. [Display omitted] • Microplastics (MPs) influence on the aging of earthworm casts was studied. • MPs affected the physicochemical properties of fresh casts but not in the long term. • PBAT MPs had minor influence on the active community (RNA). • Soil- and Gut-related core communities were likely to buffer the impacts of MPs. • MP-containing casts may not cause additional effects on the soil microbiome. [ABSTRACT FROM AUTHOR]

The accumulation of microplastics poses potential risks to soil health. Here, we did a preliminary exploration on the potential of Lumbricus terrestris (Oligochaeta) to reduce low-density polyethylene (LDPE), polylactic acid (PLA), and polybutylene adipate terephthalate (PBAT) microplastic (20–648 µm) contamination in soils. The ingestion of microplastics-contaminated soil (1% of microplastics, dw/dw) in a mesocosm system and the ingestion of pure microplastics in the Petri Dish by earthworms were studied. Results show that earthworms survived in the microplastics-contaminated soil (0% mortality in 35 days) but barely when exposed solely to microplastics (30–80% mortality in 4 days). Size-dependent ingestion of microplastics was not observed. The fragmentation of LDPE microplastics in the gizzard facilitated by soil was confirmed by the significantly increased ratio of small-sized (20–113 µm) microplastics from the bulk soil to the gut (from 8.4% to 18.8%). PLA and PBAT microplastics were fragmented by gizzard without the facilitation of soil, the ratios of small-sized (20–113 µm) PLA and PBAT microplastics in the gut were 55.5% and 108.2% higher than in respective pristine distributions. Substantial depolymerization of PLA (weight-average molar mass reduced by 17.7% with shift in molecular weight distribution) and suspected depolymerization of PBAT were observed in the worm gut, while no change in the molar mass was observed for PLA and PBAT microplastics buried in the soil for 49 days. Our results suggest that ingested microplastics could undergo fragmentation and depolymerization (for certain polymers) in the earthworm gut. Further research is needed to reveal the mechanisms of polymer depolymerization in the earthworm gut and to evaluate the feasibility of microplastic bioremediation with earthworms. [Display omitted] • Lumbricus terrestris could survive in the soil contaminated with 1% (dw/dw) of LDPE, PLA and PBAT microplastics. • The ingestion of microplastics by earthworms was not size-dependent. • Microplastics were fragmented in the earthworm gizzard with/without the help of sand grains, depending on polymer types. • Depolymerization of PLA and PBAT microplastics did not happen in the soil, but only in the earthworm's gut. • The gut-related processes inside earthworms provide potential for microplastic bioremediation in the soil. [ABSTRACT FROM AUTHOR]