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[Display omitted] • Sucralose can be completely degraded by the enriched consortia within 4 days. • Five biotransformation products were detected and a degradation pathway was proposed. • The enrichments were characterized by combining Illumina and Nanopore technologies. • The function of sucralose biodegradation was driven by novel species. Sucralose has been regarded as an emerging pollutant with growing concerns owing to its environmental persistence and potential risks to ecosystems and human health. However, limited information is currently available regarding its biodegradability and degradation pathway in the environment. In this study, complete and efficient sucralose biodegradation was achieved by enriched consortia seeded with activated sludge. In the enrichments with sucralose as the sole carbon source, 73 % of the total organic carbon was removed with a maximum degradation rate of 3.87 mg sucralose/g VSS·h−1, coupling with the release of three chloride ions of sucralose. Additionally, five biotransformation products, namely TP-409N, TP-373N, TP-357N, TP-455N, and TP-393N, were determined by UPLC-QTOF-MS, and an aerobic sucralose-degrading pathway was proposed. Then, Illumina and Nanopore sequencing were employed to provide a genome-centric resolution of microbial communities, demonstrating that the enriched consortia were dominated by Proteobacteria , Bacteroidota , Chloroflexota , and Planctomycetota. At the species level, over half of metagenome-assembled genomes were potentially affiliated with new lineages, implying that the function of sucralose biodegradation was driven by some novel species (at the genus level). Combined with the network analysis, species from UBA11579 and Polyangiaceae were suspected to be involved in the biodegradation of sucralose. This research evidenced the bacterial biodegradability of sucralose and first demonstrated the sucralose-biodegrading pathway and microbial communities, providing novel insights into sucralose biodegradation in the environment. [ABSTRACT FROM AUTHOR]