Abstract
Natural waters are contaminated globally with pharmaceuticals including many antibiotics. In this study, we assessed the acquisition of antimicrobial resistance in the culturable intestinal microbiota of rainbow trout (Oncorhynchus mykiss) exposed for 6 months to sub-inhibitory concentrations of sulfamethoxazole (SMX), one of the most prevalent antibiotics in natural waters. SMX was tested at three concentrations: 3000 µg/L, a concentration that had no observed effect (NOEC) on the in vitro growth of fish intestinal microbiota; 3 µg/L, a theoretical predicted no effect concentration (PNEC) for long-term studies in natural environments; and 0.3 µg/L, a concentration detected in many surveys of surface waters from various countries including the USA. In two independent experiments, the emergence of phenotypic resistance and an increased prevalence of bacteria carrying a sulfonamide-resistance gene (sul1) were observed in SMX-exposed fish. The emergence of phenotypic resistance to1000 mg/L SMX was significant in fish exposed to 3 µg/L SMX and was in large part independent of sul resistance genes. The prevalence of bacteria carrying the sul1 resistance gene increased significantly in the culturable intestinal microbiota of SMX-exposed fish, but the sul1-positive population was in large part susceptible to 1000 mg/L SMX, suggesting that the gene confers a lower resistance level or a growth advantage. The increased prevalence of sul1 bacteria was observed in all groups of SMX-exposed fish. Overall, this study suggests that fish exposed long-term to waters contaminated with low levels of antibiotics serve as reservoir of antimicrobial resistant genes and of resistant bacteria, a potential threat to public health.
Highlights
Natural waters are frequently contaminated with antibiotics all around the world (Batt et al 2016; Fatta-Kassinos et al 2011; Fram and Belitz 2011; Kolpin et al 2002; Kummerer 2009; Pochodylo and Helbling 2017)
Each row was supplemented with 2- fold serial dilutions of SMX from 1000 to 1 mg/L, with a no antibiotic control well, and each well was inoculated with ≈ 4 x 10e4 CFU from trout intestinal microbiota
This study shows the emergence of phenotypic resistance to SMX in the microbiota of fish exposed long-term to sub-inhibitory concentrations of this antibiotic
Summary
Natural waters are frequently contaminated with antibiotics all around the world (Batt et al 2016; Fatta-Kassinos et al 2011; Fram and Belitz 2011; Kolpin et al 2002; Kummerer 2009; Pochodylo and Helbling 2017). Sub-inhibitory concentrations of antibiotics cause mutagenesis, horizontal gene transfer, as well as modulating bacterial metabolism and virulence, including promoting biofilm formation (Andersson and Hughes 2014; Bernier and Surette 2013; Froehner et al.2000; Knudsen et al 2016; Laureti et al 2013). As these observations were derived from in vitro systems, it seems imperative to test the consequences of long-term exposure to sub-inhibitory levels of antibiotics in live aquatic systems
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