Estuarine Aquacultures at the Crossroads of Animal Production and Antibacterial Resistance: A Metagenomic Approach to the Resistome

SIMPLE SUMMARY: The overuse of antibiotics in human and animal health has been favoring antibiotic resistance in bacteria. Moreover, antibiotic-resistance genes can spread in microbial communities, between bacteria, either pathogenic or commensal, by mobile genetic elements. The rise of aquaculture farms, to overcome the growing demand for fresh fish, can lead to the overuse of antibiotics to control diseases and promote growth. This work presents a first snapshot of the antibiotic resistance genes that are present in the sediments of oyster-extensive and gilthead bream semi-intensive aquacultures located in estuaries of three important rivers in the north, center, and south of Portugal. The metagenomic analysis approach revealed that the most diverse categories of antibiotic resistance are macrolide, tetracycline, and oxazolidinone classes. These resistances can hamper the effective treatment of infections in humans if transmitted through the food chain. ABSTRACT: It is recognized that the spread of antibiotic resistance (AR) genes among aquatic environments, including aquaculture and the human environment, can have detrimental effects on human and animal health and the ecosystem. Thus, when transmitted to the human microbiome or pathogens, resistance genes risk human health by compromising the eventual treatment of infections with antibiotic therapy. This study aimed to define the resistance profile of aquaculture farms and their potential risk for spreading. Twenty-four sediments from oyster and gilthead sea bream aquaculture farms located in three Portuguese river estuaries (17 sediments from Sado, 4 from Aveiro, and 3 from Lima) were studied by comparative metagenomic analysis. The computation of the diversity of genes conferring resistance per antibiotic class revealed a significant increase in aminoglycosides, beta-lactams, disinfectants, quinolones, and tetracyclines counts. In all geographic locations under study, the most diverse AR genes confer resistance to the macrolides, tetracyclines and oxazolidinones classes, all of which are medically important for human and animal therapies, as well as resistance to disinfectants. The diversity of mobile genetic elements correlated with the number of AR genes such as tetracyclines, suggesting that AR could be easily mobilized among bacterial genomes and microbiomes.