Anthropogenic influences on coastal bacteriomes and antibiotic resistomes : from environment to cultured fish

Abstract

Anthropogenic influences on coastal bacteriomes and resistomes can promote the proliferation of human pathogens and antibiotic resistance genes (ARGs) in coastal environments and their dissemination into marine organisms. These impacts are likely amplified in intensively managed mariculture systems, raising critical concerns about seafood safety. However, the extent and mechanisms of anthropogenic influences on coastal bacteriomes and resistomes, as well as the resulting seafood contamination, remain poorly characterized, particularly in mariculture contexts. This poses significant threats to environmental and human health. To address these issues, we provide metagenomic insights into alterations in the characteristics of coastal bacteriomes and resistomes under varying anthropogenic influence across different seasons in two megacities, using minimally impacted oceanic ecosystems as global baselines, and identified key drivers. Then, we assessed the link between environmental alterations and the emergence of human pathogens and antimicrobial resistance at a mariculture site using metagenomic and culture-based methods. Relative to oceanic baselines, coastal bacteriomes showed a marked decline in biodiversity, a significant rise in human pathogen abundance, and a notable shift in core bacterial species, while coastal resistomes exhibited greater diversity, abundance, mobility, and co-occurrence with human pathogens. These biological groups showed more obvious seasonal variations than regional fluctuations from diversity to composition. Bacterial diversity peaked in winter, accompanied by a decline in human pathogen abundance. The diversity, abundance, mobility, and host range of ARGs were elevated in winter, particularly in Hong Kong coastal waters. These patterns involved increased levels of human-associated bacteria and ARGs, underscoring the profound influences of anthropogenic activities on coastal bacteriomes and resistomes. Mechanistic analyses revealed that coastal bacteriomes and resistomes were shaped by a combination of environmental and anthropogenic factors. However, biodiversity loss, shifts in core bacterial species, human pathogen proliferation, and resistome emergence were more influenced by anthropogenic factors, including antibiotic selection pressure, human fecal contamination, and anthropogenically enhanced ARG transfer. The elevated stress from these factors during winter, particularly in Hong Kong coastal waters, largely contributed to the proliferation of human-associated bacteria and ARGs in coastal waters, thereby driving the adverse shifts in coastal bacteriomes and resistomes. Wastewater treatment plant discharge and contaminated riverine runoff were primary origins of these drivers. Critically, these alterations in coastal bacteriomes and resistomes have amplified health risks for coastal populations through increasing exposure to multidrug-resistant human pathogens. Further metagenomic investigations into the link between environmental alterations and seafood contamination at the contaminated mariculture site unveiled that mariculture-induced environmental changes promoted the enrichment of emerging and foodborne pathogens (e.g., Staphylococcus aureus, Klebsiella pneumoniae, and Escherichia coli) and typical ARGs conferring resistance to vancomycin, macrolide–lincosamide–streptogramin antibiotics, trimethoprim, and chloramphenicol in cultured fishes. Shifts in source dynamics and the enhancement of ARG transferability further amplified this enrichment. The isolation of methicillin-resistant S. aureus in edible fish tissues provides phenotypic evidence for these findings and highlights the health risks of processing and consuming such contaminated seafood. Collectively, this systematic study offers comparatively systematic insights into the anthropogenic impacts on coastal bacteriomes and resistomes in both environmental and cultured seafood contexts. The findings advance our understanding of bacterial and ARG contamination and its associated health risks to coastal ecosystems and resident communities, ultimately supporting the urgency of developing effective strategies to address the growing threats of coastal antimicrobial resistance and pathogen proliferation at the local and global scales.