Long-Term Exposure to Benzalkonium Chloride Disinfectants Results in Change of Microbial Community Structure and Increased Antimicrobial Resistance

Abstract

The effect of benzalkonium chlorides (BACs), a widely used class of quaternary ammonium disinfectants, on microbial community structure and antimicrobial resistance was investigated using three aerobic microbial communities: BACs-unexposed (DP, fed a mixture of dextrin/peptone), BACs-exposed (DPB, fed a mixture of dextrin/peptone and BACs), and BACs-enriched (B, fed only BACs). Long-term exposure to BACs reduced community diversity and resulted in the enrichment of BAC-resistant species, predominantly Pseudomonas species. Exposure of the two microbial communities to BACs significantly decreased their susceptibility to BACs as well as three clinically relevant antibiotics (penicillin G, tetracycline, ciprofloxacin). Increased resistance to BACs and penicillin G of the two BACs-exposed communities is predominantly attributed to degradation or transformation of these compounds, whereas resistance to tetracycline and ciprofloxacin is largely due to the activity of efflux pumps. Quantification of several key multidrug resistance genes showed a much higher number of copies of these genes in the DPB and B microbial communities compared to the DP community. Collectively, our findings indicate that exposure of a microbial community to BACs results in increased antibiotic resistance, which has important implications for both human and environmental health.

Microbial Community Degradation of Widely Used Quaternary Ammonium Disinfectants

“…S5A in the supplemental material). Further study indicated that these efflux pumps confer increased resistance to BACs as well as several antibiotics (7). In the present work, metatranscriptomics revealed significantly increased expression (P Ͻ 0.01 by chisquared test) of these four efflux pump systems at 0.5 h compared to results at 0, 12, and 48 h (see Fig.…”

“…Detoxification of BACs or toxic intermediates also is expected to be mediated, at least in part, by the activity of efflux pump systems on a genomic island that was shared by several non-BAC-degrading members of the community (see Fig. S5 in the supplemental material) (7). Community metatranscriptomic data, as well as metabolite analysis of cultures of isolates grown on BACs, indicated that P. nitroreducens strain B cannot metabolize BDMA and, after dealkylation of BACs, appears to generate energy by ␤-oxidation of the alkyl chain and the TCA cycle ( Fig.…”

“…The microbial community analyzed in this study was incubated in a batch-fed bioreactor under aerobic conditions for 3 years (14 days of retention time) with a mixture of BACs as the sole carbon and energy source as described previously (7,14,17). Briefly, the inoculum originated from estuarine sediment that was contaminated with metals and numerous organic pollutants (18).…”

“…Hence, BACs can be toxic to life when present in nontarget environments, such as WWTPs, freshwater ecosystems, and sediments. In addition, it has been suggested that BACs promote antibiotic resistance in microbial pathogens (7)(8)(9). Following their primary application, residual BACs typically accumulate in municipal sewage systems (10,11); therefore, BAC biodegradation (detoxification) by microorganisms within WWTPs is a desirable process that could reduce potential risks to public and environmental health.…”

Integrons: Past, Present, and Future

“…Pollution of natural environments with antibiotics and disinfectants affects community structure and leads to increased carriage of resistance genes in environmental organisms (238,239). It is now widely accepted that the natural environment is a recruitment ground for resistant organisms and potential opportunistic pathogens (121,144,213,240).…”