Integrated microbiota and multi-omics analysis reveal the differential responses of earthworm to conventional and biodegradable microplastics in soil under biogas slurry irrigation

Abstract

As one of the promising alternatives of conventional plastic mulching film (C-PMF), biodegradable plastic mulching films (B-PMF) were employed in agronomy production to alleviate the environmental burden of C-PMF. However, information regarding the potential toxicity effects of biodegradable microplastics (MPs) in soil still in scarcity, and the available findings were found to be controversial. Additionally, little is known about the molecular toxicity effects of conventional and biodegradable MPs on terrestrial organisms. Thus, 5 % (w/w) biodegradable (polylactic acid, PLA) and conventional (polyvinylchloride, PVC; low-density polyvinylchloride, LDPE) MPs were employed to assess the toxicity effects on Eisenia fetida in agricultural soil with biogas slurry irrigation. In the present study, transcriptomic, metabolomic profiles and individual indexes were selected to reveal the toxicity mechanisms from molecular level to the individual response. Furthermore, dysbiosis of bacterial community in gut was also investigated for obtaining comprehensive knowledge on the MPs toxicity. At the end of the exposure, the number of survival earthworms after MPs exposure was significantly reduced. Compared with the initial body weight, PLA and LDPE increased the biomass of earthworms after MPs exposure, while no significant influence on the biomass was observed in PVC treatment. Microbacterium, Klebsiella and Chryseobacterium were significantly enriched in earthworm gut after PLA, PVC and LDPE exposure, respectively (p < 0.05). Transcriptomic and metabolomic analysis revealed that PLA exposure induced neurotransmission disorder and high energetic expenditure in earthworms. However, PVC and LDPE inhibited the nutrient absorption efficiency and activated the innate immunity responses of earthworms. The PLS-SEM results showed that the effects of MPs were dominated by the polymer types, and hence, significantly and directly influence the gut bacterial community of earthworms. This study provides a better understanding of the similarities and discrepancies in toxicity effects of biodegradable and conventional MPs from the perspectives of individual, gut bacterial community, transcriptome and metabolome.