The widespread dissemination of integrons throughout bacterial communities in a riverine system

• Published in: The ISME Journal Vol. 12; no. 3; pp. 681 - 691
• Main Authors: Amos, Gregory C. A., Ploumakis, Semina, Zhang, Lihong, Hawkey, Peter M., Gaze, William H., Wellington, Elizabeth M. H.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.03.2018; Nature Publishing Group
• Subjects: 631/158/855; 631/326/171; 631/326/22; Ammonium; Anthropogenic factors; Anti-Bacterial Agents - pharmacology; Antibiotic resistance; Antibiotics; Antimicrobial resistance; Bacteria; Bacteria - classification; Bacteria - drug effects; Bacteria - genetics; Bacteria - isolation & purification; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Biomedical and Life Sciences; Boron; Conserved sequence; Data analysis; Data processing; Detergents; Drug resistance; Drug Resistance, Bacterial; E coli; Ecology; Environmental impact; Escherichia coli - drug effects; Escherichia coli - genetics; Evolutionary Biology; Gene Transfer, Horizontal; Genes; Human influences; Humans; Integrons; Life Sciences; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Quaternary Ammonium Compounds - metabolism; Waste Water - microbiology; Wastewater; Wastewater treatment; Wastewater treatment plants; Water treatment; Water treatment plants
• ISSN: 1751-7362; 1751-7370
• DOI: 10.1038/s41396-017-0030-8

Anthropogenic inputs increase levels of antimicrobial resistance (AMR) in the environment, however, it is unknown how these inputs create this observed increase, and if anthropogenic sources impact AMR in environmental bacteria. The aim of this study was to characterise the role of waste water treatment plants (WWTPs) in the dissemination of class 1 integrons (CL1s) in the riverine environment. Using sample sites from upstream and downstream of a WWTP, we demonstrate through isolation and culture-independent analysis that WWTP effluent significantly increases both CL1 abundance and antibiotic resistance in the riverine environment. Characterisation of CL1-bearing isolates revealed that CL1s were distributed across a diverse range of bacteria, with identical complex genetic resistance determinants isolated from both human-associated and common environmental bacteria across connected sites. Over half of sequenced CL1s lacked the 3′-conserved sequence ('atypical’ CL1s); surprisingly, bacteria carrying atypical CL1s were on average resistant to more antibiotics than bacteria carrying 3′-CS CL1s. Quaternary ammonium compound (QAC) resistance genes were observed across 75% of sequenced CL1 gene cassette arrays. Chemical data analysis indicated high levels of boron (a detergent marker) downstream of the WWTP. Subsequent phenotypic screening of CL1-bearing isolates demonstrated that ~90% were resistant to QAC detergents, with in vitro experiments demonstrating that QACs could solely select for the transfer of clinical antibiotic resistance genes to a naive Escherichia coli recipient. In conclusion, this study highlights the significant impact of WWTPs on environmental AMR, and demonstrates the widespread carriage of clinically important resistance determinants by environmentally associated bacteria.