Accumulation of Pharmaceuticals, Enterococcus, and Resistance Genes in Soils Irrigated with Wastewater for Zero to 100 Years in Central Mexico

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.

Occurrence and distribution of antibiotics in urban soil in Beijing and Shanghai, China

“…As for MLs, much lower concentration and detection frequency than SAs in the urban soil was observed, and ROX was detected with maximum detection frequency of 26 % and average concentration of 0.06 μg kg −1 dw. The concentrations of SMX and ROX in our study were higher than those in the agriculture soil after long-term wastewater irrigation in Paris (Tamtam et al 2011) and in the agriculture soil fertilized with poultry or cattle manure (Karcı and Balcıoğlu 2009), but lower than the SMX concentration of 4 μg kg −1 determined in peri-urban agricultural soil after approximately 20 years irrigation with untreated wastewater in Mexico City (Dalkmann et al 2012). In contrast, (Ostermann et al 2014) have found a maximum SMZ concentration of 110 μg kg −1 in peri-urban agricultural soil from Beijing, while SMZ was only detected with the maximum concentration of 2.8 μg kg −1 in urban soil from Beijing and Shanghai in our study.…”

“…NOR revealed the highest average concentration of 94.6 μg kg −1 (dry weight, dw), which was followed by OFL and CIP with the average concentrations of 36.6 and 9.44 μg kg −1 dw, respectively. These concentrations were lower than those in the sludge-treated soil in Switzerland (Golet et al 2002), but higher than those detected at organic vegetable bases and suburban areas in Tianjin, China (Hu et al 2010), as well as higher than those in peri-urban agricultural soil after longterm wastewater irrigation in Tianjin, China , Paris (Tamtam et al 2011), and Mexico City (Dalkmann et al 2012). In addition, Ostermann et al (2014) have detected the maximum ENR concentration of 63 μg kg −1 in peri-urban agricultural soil from Beijing, which was also lower than that of 128 μg kg −1 in our study.…”

“…However, to some extent, such management may result in negative consequences such as organic or inorganic contamination of soil. Several studies have been conducted to explore the occurrence and fate of antibiotics in the agricultural soil after long-term wastewater irrigation or fertilization using animal manure (Dalkmann et al 2012;Hamscher et al 2002;Hu et al 2010;Karcı and Balcıoğlu 2009;Kinney et al 2006;Ostermann et al 2014;Shi et al 2012;Siemens et al 2010;Tamtam et al 2011;Ternes et al 2007). However, the studies on the occurrence and distribution of antibiotics in urban soil are still less reported.…”

Wastewater reuse in irrigation: A microbiological perspective on implications in soil fertility and human and environmental health

“…The fate and effect of these compounds in soils will depend on several key factors, which go far behind the chemical properties of each one or of the soil characteristics. Compounds with low mobility, such as the antimicrobials ciprofloxacin, sulfamethoxazole, and carbamazepine, were shown to accumulate in soils with the irrigation period (0-100 years), in contrast with others highly mobile (diclofenac, naproxen, bezafibrate) (Chefetz et al, 2008;Dalkmann et al, 2012;Gibson et al, 2010;Kinney et al, 2006).…”

“…Although it is still very difficult to predict what may be the effect of the naked DNA in the soil, it was possible to demonstrate that antibiotic resistance genes (from both intra-and extracellular DNA) could be detected in soil in high doses by quantitative PCR after 16 months of environmental exposure (Hong et al, 2013;Selvam et al, 2012). These arguments show that even if immediate impacts are not observed, long term effects of accumulation of resistant bacteria, resistance genes and antibiotic residues should not be ignored (Dalkmann et al, 2012).…”