Crosstalk between gut metabolomics, bioaccumulation, and microbial enrichment in earthworms for effective remediation of toxic metals: Insights from green waste-based vermicomposting systems

The knowledge on earthworm gut metabolomic variations in metal-enriched green waste (GW)-based vermicomposting systems is scarce. Earthworm's gut metabolite-metal accumulation interactions have also not been studied earlier. Therefore, GW-based Eisenia fetida-mediated vermicomposting and aerobic composting systems were spiked with Pb-Cr-Cu (1:1:1)-mixed solutions. While earthworm reproduction, body weight, and gut microbial growth were slightly lower in metal-spiked GW-vermibeds compared to unspiked vermibeds, the temporal increase in N-P-K enrichment, feedstock microbial counts, and microbial biomass-C&N were significantly more in metal-spiked vermicomposts than in metal-spiked composts. Interestingly, the metal removal efficiency was ∼1.2–3.0 times higher in metal-spiked vermibeds than in unspiked vermibeds and composting beds. Furthermore, the degree of bioaccumulation for Pb (spiked - 1.64 mg kg⁻¹ versus unspiked - 0.22 mg kg⁻¹), Cr (spiked - 0.92 mg kg⁻¹ versus unspiked - 0.40 mg kg⁻¹), and Cu (spiked – 1.54 mg kg⁻¹ versus unspiked - 0.79 mg kg⁻¹) was significantly higher in earthworms grown in spiked than in unspiked GW feedstocks. The LC-QTOF-MS-mediated earthworm-gut metabolomic profiling revealed that 655 biomolecules were significantly up or down-regulated due to metal spiking. Interestingly, compounds known for stress-ameliorating roles (e.g., methylcitisine and trans-anethole) have increased most dramatically in metal-spiked vermibed-borne earthworms. A KEGG-database analysis revealed that the phenylpropanoid pathway metabolites augment in metal-rich feedstock-borne earthworms. Finally, the correlation statistics clarified that earthworm gut metabolite distribution meaningfully alters to enhance the detoxification of non-essential toxic metals (Pb and Cr) more than essential micronutrient metals (Cu) in waste-based vermicomposting systems.