Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment

Abstract

The impact of human activity on the selection for antibiotic resistance in the environment is largely unknown, although considerable amounts of antibiotics are introduced through domestic wastewater and farm animal waste. Selection for resistance may occur by exposure to antibiotic residues or by co-selection for mobile genetic elements (MGEs) which carry genes of varying activity. Class 1 integrons are genetic elements that carry antibiotic and quaternary ammonium compound (QAC) resistance genes that confer resistance to detergents and biocides. This study aimed to investigate the prevalence and diversity of class 1 integron and integron-associated QAC resistance genes in bacteria associated with industrial waste, sewage sludge and pig slurry. We show that prevalence of class 1 integrons is higher in bacteria exposed to detergents and/or antibiotic residues, specifically in sewage sludge and pig slurry compared with agricultural soils to which these waste products are amended. We also show that QAC resistance genes are more prevalent in the presence of detergents. Studies of class 1 integron prevalence in sewage sludge amended soil showed measurable differences compared with controls. Insertion sequence elements were discovered in integrons from QAC contaminated sediment, acting as powerful promoters likely to upregulate cassette gene expression. On the basis of this data, 41 Â 10 19 bacteria carrying class 1 integrons enter the United Kingdom environment by disposal of sewage sludge each year.

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

“…We believe this is the first study to determine the effects from the direct application of veterinary antibiotics in the absence of manure with the resolution achievable by16S rRNA gene sequence analysis. We have shown that a decade of annual exposure to a mixture of antibiotics at 10 mg kg -1 led to a statistically significant H. Gaze, personal communication) (Gaze et al, 2011). The 0.064% observed in treatment plots was higher than that previously observed in soil that had undergone application of antibiotic amended pig slurry (0.01%) (Byrne-Bailey et al, 2011), and soil 12 months after sewage cake application (0.02%) (Gaze et al, 2011) but lower than one month after application (0.36%).…”

“…We have shown that a decade of annual exposure to a mixture of antibiotics at 10 mg kg -1 led to a statistically significant H. Gaze, personal communication) (Gaze et al, 2011). The 0.064% observed in treatment plots was higher than that previously observed in soil that had undergone application of antibiotic amended pig slurry (0.01%) (Byrne-Bailey et al, 2011), and soil 12 months after sewage cake application (0.02%) (Gaze et al, 2011) but lower than one month after application (0.36%). Integron prevalence in aquatic sediments has been shown to correlate with specific land uses (Amos et al, 2014), suggesting terrestrial inputs into river catchments and ultimately to receiving coastal waters where human exposure may occur (Leonard et al, 2015).…”

Antibiotic resistance genes in manure-amended soil and vegetables at harvest

“…In this study, it was found that intI1 gene had significantly positive correlation with sulI, sulII, tetA, tetC, tetG, and tetBP genes, indicating that intI1 gene may play certain role in the dissemination of ARGs. Previous study have demonstrated that integrons can be used by Gram-positive and Gram-negative bacteria to stockpile and express different exogenous resistance genes and are considered to play a central role in the worldwide problem of antibiotic resistance [39][40][41]. Partridge et al found that sulI gene was carried within the 3 conserved region of class 1 integron, and such an association may facilitate and enhance its persistence [42].…”

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

“…HGT could potentially enhance the accumulation and persistence of ARGs in manure/sludge-amended soil via MGEs (Gaze et al, 2011;Smalla et al, 2000). It has been demonstrated that MGEs, especially integrons can be used by bacteria to stockpile and express different exogenous resistance genes and are considered to play a central role in the worldwide problem of antibiotic resistance (Gaze et al, 2011;Gillings et al, 2008;Partridge et al, 2009). Our results indicated that MGEs had significantly positive correlation with resistance genes to beta-lactams, MLSB, sulfonamide and vancomycin, while no significant correlation with resistance genes to tetracyclines.…”

“…Land application of sewage sludge may result in the spread of ARGs in soil and to underground water (Threedeach et al, 2012). More importantly, bacteria have been shown to readily share genetic information by HGT via mobile genetic elements (MGEs) including plasmids, transposons, and integrons (Zhu et al, 2013;Pruden et al, 2006), allowing the transfer of resistance genes from sewage sludge microorganisms to indigenous environmental bacteria (Gaze et al, 2011). Sewage sludge has been shown to be a hotspot for bacteria carrying ARGs and MGEs and its application may enhance the HGT of ARGs in soil, although the bacterial populations of sewage sludge and soil may be quite distinct (Hammesfahr et al, 2008).…”