Integron Involvement in Environmental Spread of Antibiotic Resistance

Abstract

The spread of antibiotic-resistant bacteria is a growing problem and a public health issue. In recent decades, various genetic mechanisms involved in the spread of resistance genes among bacteria have been identified. Integrons – genetic elements that acquire, exchange, and express genes embedded within gene cassettes (GC) – are one of these mechanisms. Integrons are widely distributed, especially in Gram-negative bacteria; they are carried by mobile genetic elements, plasmids, and transposons, which promote their spread within bacterial communities. Initially studied mainly in the clinical setting for their involvement in antibiotic resistance, their role in the environment is now an increasing focus of attention. The aim of this review is to provide an in-depth analysis of recent studies of antibiotic-resistance integrons in the environment, highlighting their potential involvement in antibiotic-resistance outside the clinical context. We will focus particularly on the impact of human activities (agriculture, industries, wastewater treatment, etc.).

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

“…Recent functional metagenomic studies suggested that soil microbial phylogenetic and taxonomic structure is the primary determinant of ARG profile across various soil types, and no positive correlation was found between the soil ARGs and mobility elements suggesting that the horizontal gene transfer between soil bacteria is very low (Forsberg et al 2014). In fact, integrons are just one of the many types of mobile genetic elements involved in the adaptation of bacteria (Stalder et al 2012), and we did not find any positive effect of manure application on the transposase gene tnpA. Therefore, although the acquisition of ARGs by lateral gene transfer is considered as the most probable route of ARGs emergence in clinical environments (Nesme and Simonet 2014), such mechanism is pending more investigations in soil environments.…”

“…Integrons possess a site specific recombination system that could capture and express mobile gene cassettes (Heuer, Schmitt and Smalla 2011a), and they were reported to often localize in broad-host-range IncP-1ε plasmids with a wide distribution in agricultural systems that further facilitates their mobility potential (Heuer et al 2012;Jechalke et al 2014c;Wolters et al 2015). The critical roles of integrons in the dissemination of ARGs in environments have been highlighted by cultivation methods and metagenomics approaches (Hardwick et al 2008;Stalder et al 2012;Gillings et al 2015). Class 1 integrons have been extensively studied due to their widespread distribution in Gram-negative bacteria of clinical importance (Stalder et al 2012), and the intI1 genes were reported to be very common in soils and related ecosystems (Gillings et al 2008;Jechalke et al 2014c).…”

“…The critical roles of integrons in the dissemination of ARGs in environments have been highlighted by cultivation methods and metagenomics approaches (Hardwick et al 2008;Stalder et al 2012;Gillings et al 2015). Class 1 integrons have been extensively studied due to their widespread distribution in Gram-negative bacteria of clinical importance (Stalder et al 2012), and the intI1 genes were reported to be very common in soils and related ecosystems (Gillings et al 2008;Jechalke et al 2014c).…”

Quaternary ammonium compounds in soil: implications for antibiotic resistance development

“…The qac genes are commonly found on class 1 integrons, for example from clinical isolates (Gillings et al 2009;Stalder et al 2012). Class 1 integrons are able to accumulate, exchange, and express gene cassettes, which are known to carry resistance genes for almost all antibiotic families (Stalder et al 2012). These integrons are also widespread in the environment such as agricultural soils (Gillings et al 2014;Jechalke et al 2014).…”

Effects of electron acceptors on removal of antibiotic resistant Escherichia coli, resistance genes and class 1 integrons under anaerobic conditions

“…Bacterial pathogens carrying ARGs can survive in the presence of antibiotics through several mechanisms (Wright, 2012), thereby enriching resistant strains and lowering drug efficacy. A major concern is that ARGs can be shared among different species through horizontal gene transfer (Stokes and Gillings, 2011), which appears to be a rare, but important event in the spread of antibiotic resistance (Durso et al, 2012;Forsberg et al, 2014;Stalder et al, 2012). The rise in percentages of resistant bacteria has steadily followed the rise in antibiotic use in humans and agriculture.…”