Abstract
Irrigation with wastewater releases pharmaceuticals, pathogenic bacteria, and resistance genes, but little is known about the accumulation of these contaminants in the environment when wastewater is applied for decades. We sampled a chronosequence of soils that were variously irrigated with wastewater from zero up to 100 years in the Mezquital Valley, Mexico, and investigated the accumulation of ciprofloxacin, enrofloxacin, sulfamethoxazole, trimethoprim, clarithromycin, carbamazepine, bezafibrate, naproxen, diclofenac, as well as the occurrence of Enterococcus spp., and sul and qnr resistance genes. Total concentrations of ciprofloxacin, sulfamethoxazole, and carbamazepine increased with irrigation duration reaching 95% of their upper limit of 1.4 µg/kg (ciprofloxacin), 4.3 µg/kg (sulfamethoxazole), and 5.4 µg/kg (carbamazepine) in soils irrigated for 19–28 years. Accumulation was soil-type-specific, with largest accumulation rates in Leptosols and no time-trend in Vertisols. Acidic pharmaceuticals (diclofenac, naproxen, bezafibrate) were not retained and thus did not accumulate in soils. We did not detect qnrA genes, but qnrS and qnrB genes were found in two of the irrigated soils. Relative concentrations of sul1 genes in irrigated soils were two orders of magnitude larger (3.15×10−3±0.22×10−3 copies/16S rDNA) than in non-irrigated soils (4.35×10−5±1.00×10−5 copies/16S rDNA), while those of sul2 exceeded the ones in non-irrigated soils still by a factor of 22 (6.61×10–4±0.59×10−4 versus 2.99×10−5±0.26×10−5 copies/16S rDNA). Absolute numbers of sul genes continued to increase with prolonging irrigation together with Enterococcus spp. 23S rDNA and total 16S rDNA contents. Increasing total concentrations of antibiotics in soil are not accompanied by increasing relative abundances of resistance genes. Nevertheless, wastewater irrigation enlarges the absolute concentration of resistance genes in soils due to a long-term increase in total microbial biomass.
Highlights
The coexistence of antibiotics, pathogenic bacteria, and resistance determinants in the environment raises concerns that antibiotic resistance genes are mobilized from and disseminated into the environmental resistome and transferred to bacteria that are potentially pathogenic to humans [1,2,3]
These risks might be high for agricultural fields that are irrigated with wastewater, which receive regular inputs of antibiotics, bacteria, and resistance genes similar to manured soils (e.g., [4])
One of the largest wastewater irrigation areas worldwide can be found in the Mezquital Valley receiving wastewater from the Mexico City Metropolitan Area (MCMA) [11]
Summary
The coexistence of antibiotics, pathogenic bacteria, and resistance determinants in the environment raises concerns that antibiotic resistance genes are mobilized from and disseminated into the environmental resistome and transferred to bacteria that are potentially pathogenic to humans [1,2,3]. These risks might be high for agricultural fields that are irrigated with wastewater, which receive regular inputs of antibiotics, bacteria, and resistance genes similar to manured soils (e.g., [4]). Reports on the occurrence of pharmaceuticals in wastewater-irrigated soils in Colorado, USA [16], Braunschweig, Germany [17], Hebei, China [18], and the metropolitan area of Paris, France [19] illustrate that the contamination of soils with wastewater-derived pharmaceuticals is not limited to Mexico, but a global phenomenon
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