320 / 2024-09-14 09:45:05

Deciphering resistome structuring mechanism and increased health risk from Qiantang River Basin via estuary to Hangzhou Bay

antibiotic resistance gene,resistome structure,estuarine ecosystem,metagenomics,anthropogenic disturbance

Environmental microbiome harbors diverse antibiotic resistance genes (ARGs) which are exchangeable with human and animal resistomes. Considered as one of the most vulnerable ecosystems, coastal estuaries are threatened by growing anthropogenic pollution and have recently been reported as a pivotal reservoir for the propagation and dissemination of ARGs. Despite global concerns about the continental-scale contamination of estuaries with ARGs, the resistome structuring mechanism, key drivers, and health risks in such anthropogenically impacted brackish coastal water ecosystems are unknown.

This study leveraged metagenomics to comprehensively investigate the sediment resistome structure along a representative estuary in the Yangtze River Delta, covering the upstream freshwater rivers as Hangzhou city’s drinking water source and the downstream brackish-water bay (Hangzhou Bay), unraveled the spatial dynamics and driving factors of the interconnected resistome. The result showed that the resistome structure significantly shifted from Qiantang river basin via its estuary to Hangzhou Bay, driven most by microbial community (i.e., microbiota) and mobile genetic elements, followed by pharmaceutical and personal care products, and water physiochemistry, suggesting a role of both vertical transmission and environmental selection of ARGs along the river-coastal water continuum. Moreover, clinically important and mobile ARGs of beta-lactam (e.g., LAP-2, CMY-100, and KPC-2) and two synthetic antibiotics commonly used in veterinary medicine (e.g., florfenicol-resistant floR and sulfonamide-resistant sul1) were significantly enriched in Hangzhou Bay, greatly contributing to the identified elevation in the resistome risks. Notably, our first discovery of clinically important macrolide-resistant macB and extended-spectrum β-lactamase TEM-116 in uncultured indigenous members of Nitrospirota implicated priorly unperceived integration of clinically important ARGs into coastal environmental resistomes.

Identifying clinically relevant ARGs enriched in the environmental reservoirs, as demonstrated in this study, is the cornerstone for inspecting and controlling the transmission of high-risk antimicrobial resistance to animals and humans under the One Health framework. The results of this study co-emphasize a prominent role of anthropogenic pollution in shaping resistome structure and health risks of coastal ecosystem. This study also provides a new perspective for the monitoring, tracking, and managing ARG pollution in Hangzhou Bay and inspires future in-depth global examination of the evolution and spread of antibiotic resistance in anthropogenically impacted coastal estuaries and ecosystem.