Accelerated Biodegradation of Veterinary Antibiotics in Agricultural Soil following Long-Term Exposure, and Isolation of a Sulfamethazine-degrading Microbacterium sp.

Abstract

The World Health Organization has identified antibiotic resistance as one of the top three threats to global health. There is concern that the use of antibiotics as growth promoting agents in livestock production contributes to the increasingly problematic development of antibiotic resistance. Many antibiotics are excreted at high rates, and the land application of animal manures represents a significant source of environmental exposure to these agents. To evaluate the long-term effects of antibiotic exposure on soil microbial populations, a series of field plots were established in 1999 that have since received annual applications of a mixture of sulfamethazine (SMZ), tylosin (TYL), and chlortetracycline (CTC). During the first 6 yr (1999-2004) soils were treated at concentrations of 0, 0.01 0.1, and 1.0 mg kg soil, in subsequent years at concentrations of 0, 0.1, 1.0, and 10 mg kg soil. The lower end of this concentration range is within that which would result from an annual application of manure from medicated swine. Following ten annual applications, the fate of the drugs in the soil was evaluated. Residues of SMZ and TYL, but not CTC were removed much more rapidly in soil with a history of exposure to 10 mg/kg drugs than in untreated control soil. Residues of C-SMZ were rapidly and thoroughly mineralized to CO in the historically treated soils, but not in the untreated soil. A SMZ-degrading sp. was isolated from the treated soil. Overall, these results indicate that soil bacteria adapt to long-term exposure to some veterinary antibiotics resulting in sharply reduced persistence. Accelerated biodegradation of antibiotics in matrices exposed to agricultural, wastewater, or pharmaceutical manufacturing effluents would attenuate environmental exposure to antibiotics, and merits investigation in the context of assessing potential risks of antibiotic resistance development in environmental matrices.

Long-term antibiotic exposure in soil is associated with changes in microbial community structure and prevalence of class 1 integrons

“…Only one OTU was shown to increase significantly, belonging to the Cyanobacteria (Table 1). This is an unexpected finding given the known sensitivity of members of this Class, which have seen their use in antibiotic environmental toxicity bioassays ( Van der Grinten et al, 2010).…”

“…Details on the field site, soil management and cropping are provided in Topp et al (2013). Briefly, a series of 2 m 2 plots were established isolated by means of an open fibreglass box (inserted to a depth of ~ 50 cm) with 1 m grassed strips between plots.…”

“…To characterise in situ selection for antibiotic resistance a long-term field study was initiated in 1999 in London Ontario, Canada to evaluate the impact of veterinary antibiotics on soil microbial populations (Topp et al, 2013). This study was designed such that the introduction of bacteria from manure, although a more realistic source of antibiotic residues, is avoided thereby facilitating interpretation of the direct selective effects of antibiotics on soil microbiota.…”

Agriculture and Agri-Food Canada’s research program on antimicrobial resistance

“…The ecology of antimicrobial-resistant enteric bacteria in crop production systems fertilized with manure is being investigated to assess the potential increase in AMR burden on crops at harvest (7,8). The fate of antimicrobials in soil and their potential impacts on soil microorganisms is of interest (9,10). Overall, the objective is to understand the dynamics of AMR development in animal and crop production systems and the potential transmission through the food processing chain into agroecosystems receiving the agricultural waste.…”

An effective bioremediation approach for enhanced microbial degradation of the veterinary antibiotic sulfamethazine in an agricultural soil

“…The only study showing a metabolic SMZ degradation conducted by indigenous soil microbes was done by Topp et al [30]. High SMZ degradation by indigenous soil microbes was observed in laboratory experiments after long-term application of SMZ to the field (one time per year for 10 years).…”