Elsevier

Chemosphere

Volume 221, April 2019, Pages 132-140
Chemosphere

Antimicrobial resins with quaternary ammonium salts as a supplement to combat the antibiotic resistome in drinking water treatment plants

https://doi.org/10.1016/j.chemosphere.2019.01.047Get rights and content

Highlights

  • AMRs-QAS show potential in diminishing pathogens that resist disinfectant in DWTPs.

  • Coupling AMRs-QAS with low-dose chlorine effectively combats antibiotic resistome.

  • Co-occurrences of pathogens and ARGs account for the ARGs removal by AMRs-QAS.

  • AMRs-QAS can assist to the chlorine or UV disinfection in DWTPs.

Abstract

The increasing finding of pathogens and antibiotic resistance genes (ARGs) in drinking water has become one of the most challenging global health threats worldwide. However, conventional disinfection strategies in drinking water treatment plants (DWTPs) require further optimization in combating the antibiotic resistome. Here, we show that antimicrobial resins with quaternary ammonium salts (AMRs-QAS) exhibit great potentials in diminishing specific potential pathogens that relatively resist chlorine or UV disinfection in DWTPs, and comprehensive analyses using microscopy and fluorescence techniques revealed that the antimicrobial capacity of AMRs-QAS mainly proceed via the bacterial adsorption and cell membrane dissociation. Moreover, a total of 15 among 30 selected ARGs, as well as 4 selected potential pathogens including Pseudomonas aeruginosa, Bacillus subtilis, Escherichia coli and Staphylococcus aureus were all detected in the source water. Coupling the AMRs-QAS with 0.2 mg/L chlorine resulted in higher removal efficiencies than chlorination (2 mg/L) or UV disinfection (400 mJ cm−2) for all the detected pathogens and ARGs in drinking water and significantly decreased the relative abundances of Pseudomonas aeruginosa, Bacillus subtilis, Escherichia coli, as well as all the detected ARGs (p < 0.05). Co-occurrences of pathogens and ARGs were revealed by a correlation network and possibly accounts for the ARGs removal. This coupled disinfection strategy overcomes the limitations of individual disinfection methods, i.e. the enrichment of specific pathogens and ARGs among bacterial populations, and provides an alternative for minimizing health risks induced by the antibiotic resistome in DWTPs.

Introduction

The wide spread of antibiotic resistance in the environment has become one of the most important environmental concerns with global implications and extensive attention (Pruden et al., 2013). Specially, the increasingly excessive use of antibiotics stimulates the antibiotic resistance genes (ARGs) propagation in natural waters (Lubick, 2011), which aggravates the biological contamination of drinking water and thus threatens public health (Dhara and Tripathi, 2014; Ashbolt, 2015; Fernando et al., 2016). Recently, a broad spectrum of ARGs and potential pathogens were found in drinking water from the main metropolitan cities of China and other areas worldwide by a large-scale survey (Ma et al., 2017), demonstrating the urgent need for concern regarding this environmental problem.

Drinking water treatment plants (DWTPs) usually employ disinfection strategies involving chlorine, chloramine or ultraviolet (UV) light to inactivate both nonpathogenic and pathogenic microorganisms (Ngwenya et al., 2013). However, chlorination partially eliminates pathogens due to their cross- or co-resistance against antibiotics and chloride-type disinfectants (Xi et al., 2009; Jia et al., 2015), and it consequently enriches several potential pathogens, e.g. Pseudomonas spp. and Bacillus spp., as well as their inherent ARGs in drinking water (Shi et al., 2013). UV disinfection induces a viable but nonculturable (VBNC) state in Escherichia coli and Pseudomonas aeruginosa (Zhang et al., 2015) and also enriches Pseudomonas spp. and resistance-nodulation-division (RND) genes that they carry in wastewater (Hu et al., 2016). Moreover, a series of synthetic antimicrobial nanomaterials showed great potential for water disinfection (Li et al., 2008) and pathogens control (Lam et al., 2016), but they might promote horizontal gene transfer of multidrug resistance genes across genera due to multimode mechanisms (Qiu et al., 2012) and might exhibit nanotoxicity to human health (Li et al., 2008), which are disadvantages for their application in DWTPs.

Antimicrobial resins with quaternary ammonium salt (AMRs-QAS) moieties harbor complex macromolecular and micrometer-scale architectures that are unable to penetrate cell membranes but interact with bacterial membranes through electrostatic attractions, which may physically damage the bacterial morphology (Carmona–Ribeiro and Carrasco, 2013). Their unique bactericidal mechanism may render bacteria less likely to develop resistance to the AMRs-QAS and thus provides an alternative for combating the antibiotic resistome in drinking water through the preferred removal of highly negatively charged bacteria (e.g., Pseudomonas aeruginosa and Bacillus subtilis), which are relatively resistant to chlorine or UV disinfection (Wilson et al., 2001; Horka et al., 2006). Numerous studies have evidenced the excellent bactericidal effects of many AMRs-QAS such as epoxy-amine resins (Adam et al., 2014) and antimicrobial resins containing quaternarized N-halamine (Jie et al., 2013) or QAS groups (Jie et al., 2014). However, the cross-resistance of bacteria to these materials and antibiotics, as well as the mechanism of action by which ARG change, has not been investigated yet. Quaternary ammonium compounds (QACs) enhance the co-selection and spread of antibiotic resistance among skin-colonizing and also environmental bacteria (Buffet–Bataillon et al., 2012; Bragg et al., 2014), resulting in the necessity of unraveling the AMRs-QAS effects on the antibiotic resistome in drinking water.

Magnetic anion exchange resins (MAERs) are a type of AMRs-QAS with advantages of adjustable structure, renewable use and large water yield that have realized engineering application, and sufficient studies have proven their excellent performance on normal organic matters (NOMs) (Bhatnagar and Sillanpää, 2017), disinfection byproducts (DBPs) control and toxicity reduction in DWTPs (Shi et al., 2015). However, the degerming and ARGs control capacities of MAERs in DWTPs were seldom reported in previous studies. We therefore aimed to investigate the bacteria-eliminating effectiveness and ARGs changes caused by two types of commercially-available AMRs-QAS in DWTPs, and their effects on antibiotic resistance using flow cytometry, scanning electron microscope (SEM), excitation-emission matrix (EEM) spectroscopy and high-throughput quantitative real-time PCR (HT-qPCR) approaches. Finally, a microbial control strategy coupling the AMRs-QAS and conventional disinfection methods was proposed to minimize the pathogenic and antibiotic-resistant risks in DWTPs. This study provides us novel insights into controlling potential pathogens that relatively resist chlorine or UV disinfection and combating the antibiotic resistome in DWTPs.

Section snippets

Preparation of AMRs-QAS and bacterial suspensions

Two types of MAERs, i.e. MIEX and NDMP, were selected in this study and generously provided by the Guochuang New Material Company (Jiangsu, China), respectively. These two MAERs are typical AMRs-QAS with polyacrylic acid matrixes and QAS groups, and their physiochemical parameters were reported in our previous study (Shuang et al., 2012) and summarized in Table S1. In addition, two strains of gram-negative bacteria, including Escherichia coli (ATCC55124) and Pseudomonas aeruginosa

AMRs-QAS elimination of bacteria in bacterial suspensions

The removal efficiencies of NDMP and MIEX against four bacterial strains increased from 40 to 99% with increasing dosage (Fig. S3), and NDMP showed a much better antimicrobial performance than MIEX, exhibiting the highest removal efficiency of 99% against Bacillus subtilis. The results indicated that the AMRs-QAS efficiently eliminated all the tested bacteria irrespective of the gram-negative or gram-positive, implying the broad-spectrum effect of the materials on bacterium removal. This

Discussion

In this study, disinfection via the AMRs-QAS eliminated potential pathogens well and effectively combated the antibiotic resistome in drinking water when coupled with a low dose of chlorine disinfectant. The adsorption-dissociation of the AMRs-QAS was proven to be the underlying bactericidal mechanism that determined their unique ability to remove pathogens and ARGs. Preferred removal of Pseudomonas aeruginosa and Bacillus subtilis by the AMRs-QAS well compensated for the conventional

Acknowledgements

This study was financially supported by National Natural Science Foundation of China (Grant No. 51608253), Natural Science Foundation of Jiangsu Province, China (BK20160656), Environmental Protection Research Project of Jiangsu Province (No. 2016014) and the Fundamental Research Funds for the Central Universities.

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