The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria

Abstract

The use of antibiotics at subtherapeutic concentrations for agricultural applications is believed to be an important factor in the proliferation of antibiotic-resistant bacteria. The goal of this study was to determine if the application of manure onto agricultural land would result in the proliferation of antibiotic resistance among soil bacteria. Chlortetracycline-resistant bacteria were enumerated and characterized from soils exposed to the manure of animals fed subtherapeutic concentrations of antibiotics and compared to the chlortetracycline-resistant bacteria from soils at farms with restricted antibiotic use (dairy farms) and from non-agricultural soils. No significant differences were observed at nine different study sites with respect to the numbers and types of cultivated chlortetracycline-resistant bacteria. Genes encoding for tetracycline resistance were rarely detected in the resistant bacteria from these sites. In contrast, soils collected from a tenth farm, which allowed manure to indiscriminately accumulate outside the animal pen, had significantly higher chlortetracycline-resistance levels. These resistant bacteria frequently harbored one of 14 different genes encoding for tetracycline resistance, many of which (especially tet(A) and tet(L)) were detected in numerous different bacterial species. Subsequent bacterial enumerations at this site, following the cessation of farming activity, suggested that this farm remained a hotspot for antibiotic resistance. In conclusion, we speculate that excessive application of animal manure leads to the spread of resistance to soil bacteria (potentially by lateral gene transfer), which then serve as persistent reservoir of antibiotic resistance.

Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil

“…However, land application of animal manure or sewage sludge does not universally increase ARGs in soils (Zhou et al, 2010) and this increase is not maintained long-term (Fahrenfeld et al, 2014). For instance, manure from three dairy farms did not increase cultivable chlortetracycline-resistant bacteria when land-applied to soil (Ghosh and LaPara, 2007). Also in a microcosm study, the relative abundance of tetAP, tetX, and tetO genes decreased over time, and fell below the initial levels of the control soils during the 60d experimental periods .…”

“…This phenomenon may be due, at least partly, to potential changes in soil microbial composition including the native soil antibiotic-resistant bacteria (ARB) after the application of chemical fertilizer (Forsberg et al, 2014). Although chemical fertilizer had some effects on soil ARGs, these effects, not surprisingly, are weaker when compared with sewage sludge or chicken manure, considering that manure is rich in ARGs and ARBs , Jiang et al, 2002Ghosh and LaPara, 2007) and most ARGs are discharged from the municipal wastewater treatment process in the form of sewage sludge (Munir et al, 2011). However, land application of animal manure or sewage sludge does not universally increase ARGs in soils (Zhou et al, 2010) and this increase is not maintained long-term (Fahrenfeld et al, 2014).…”

Temporal changes of antibiotic-resistance genes and bacterial communities in two contrasting soils treated with cattle manure

“…Amendment of soils with manure from antibiotic-treated animals has been frequently reported as an important route by which ARGs enter the environment and food system (Ghosh and LaPara 2007;Heuer et al 2008). However, recent studies suggested that high frequencies of ARGs (such as β-lactamases and tetracycline-resistance genes) are encountered in manure from dairy cows receiving no administration of veterinary antibiotics (Kyselkova et al 2013;Udikovic-Kolic et al 2014).…”

“…Antibiotics are widely used in agriculture for treatments of sick animals, infectious disease prophylaxis and growth promotion, accounting for at least half of the antibiotics produced worldwide (Ghosh and LaPara 2007;Allen et al 2010;Hu, Zhou and Luo 2010). However, most of antibiotics are poorly absorbed by animals and a large proportion (30%-90%) of them can be excreted and dispersed into soils when manure is applied as fertilizer (Zhang and Zhang 2011).…”

“…To date, the environmental occurrence of antibiotics and ARGs in wastewater, reclaimed water, sludge and sediments has been documented (Auerbach, Seyfried and McMahon 2007;Ghosh and LaPara 2007;D'Costa et al 2011;Leung et al 2012;Liu et al 2012); however, evidence remains largely elusive regarding the spatial and temporal patterns of soil ARGs under anthropogenic disturbance (D'Costa et al 2006;Forsberg et al 2014). Soil is considered to be the largest environmental reservoir comprising as much as 30% of the known ARGs in public repositories , and to be one of the most complex ecosystems in terms of microbial diversity and ecological niches (Nesme and Simonet 2014).…”