Vermicomposting preferably alters fungal communities in wasted activated sludge and promotes the production of plant growth-promoting biostimulants in the vermicompost

Waste activated sludge (WAS) is the main by-product of wastewater treatment plants. Vermicomposting integrated earthworms and reconstructive microbes to achieve WAS stabilization, with the mature composts enriched with plant hormones and humic substances (HS) forming supramolecular forces to protect hormone activity. However, how vermicomposting changes sludge microbial community, transforms sludge-derived organics into various plant biostimulants and promotes hormones-HS interaction remain elusive. Here we used multi-omics approaches to demonstrate how reconstructed microbes transformed sludge-derived organics into plant biostimulants, and molecular dynamics (MD) simulation to explore the force details of hormone-HS aggregations. Additionally, plant growth phenotype treated by the vermicompost was accessed. Our results showed that earthworm (Eisenia fetida) selectively altered fungal communities in sludge matrices, promoting the growth of phyla Mucoromycota, Ascomycota, and Cryptomycota. Reconstructed fungal communities then dominated the transformation of nitrogenous organics, accelerating the degradation rate of proteins and the production rate of plant biostimulants, including humic substances (HS, especially fulvic acid), indoleacetic acid (IAA), jasmonic acid (JA), and salicylic acid (SA). In detail, indole acted as the exclusive precursor for IAA biosynthesis (2.77 mg/kg-TS) via tryptophan metabolism. Unsaturated fatty acids generated from the citrate cycle were responsible for JA production (2.19 mg/kg-TS) via β-oxidation, while phenylalanine contributed to SA production (4.52 μg/kg-TS) via deaminase coenzyme and phenylalanine-4-hydroxylase. The results of MD simulation exhibited a stronger supramolecular force in the IAA-HS assemblage (−46.7 KJ/mol) than the SA-HS pair and JA-HS pair, thus protecting the structure and bioavailability of IAA and promoting the auxin-like activity in the vermicompost. Plant growth experiments further confirmed that vermicompost promoted plant root elongation. This work is believed to deepen the understanding of vermicomposting for sustainable management of sludge.