Abstract
Triclosan (TCS) is a widely used antimicrobial agent and TCS resistance is considered to have evolved in diverse organisms with extensive use of TCS, but distribution of TCS resistance has not been well characterized. Functional screening of the soil metagenome in this study has revealed that a variety of target enoyl acyl carrier protein reductases (ENR) homologues are responsible for the majority of TCS resistance. Diverse ENRs similar to 7-α-hydroxysteroid dehydrogenase (7-α-HSDH), FabG, or the unusual YX7K-type ENR conferred extreme tolerance to TCS. The TCS-refractory 7-α HSDH-like ENR and the TCS-resistant YX7K-type ENR seem to be prevalent in human pathogenic bacteria, suggesting that a selective enrichment occurred in pathogenic bacteria in soil. Additionally, resistance to multiple antibiotics was found to be mediated by antibiotic resistance genes that co-localize with TCS resistance determinants. Further comparative analysis of ENRs from 13 different environments has revealed a huge diversity of both prototypic and metagenomic TCS-resistant ENRs, in addition to a selective enrichment of TCS-resistant specific ENRs in presumably TCS-contaminated environments with reduced ENR diversity. Our results suggest that long-term extensive use of TCS can lead to the selective emergence of TCS-resistant bacterial pathogens, possibly with additional resistance to multiple antibiotics, in natural environments.
Highlights
Various environments, including waste water treatment plants (WWTPs), sediment, surface water, sewage, sludge and soil, have been known to serve as potential reservoirs of antibiotic resistance genes (ARGs)[5]
Our results provide valuable information about the TCS resistance gene (TRG) reservoir in the natural environment at the metagenomic level
We demonstrate that novel metagenome-derived diverse enoyl acyl carrier protein reductases (ENR) variants associated with TCS resistance are abundant in natural soils and in a number of human-associated pathogenic microorganisms
Summary
Various environments, including waste water treatment plants (WWTPs), sediment, surface water, sewage, sludge and soil, have been known to serve as potential reservoirs of antibiotic resistance genes (ARGs)[5]. Exchange of ARGs by horizontal gene transfer between bacteria from natural environments and pathogenic bacteria has been reported[6]. This phenomenon reveals the importance of the environmental resistome in terms of the possible transmission and spread of selected ARGs to human pathogenic bacteria. Several mechanisms that confer resistance to this biocide are known and include: (i) overexpression of ENR17; (ii) presence of mutated and/or TCS-tolerant ENR18; (iii) changes in the outer membrane[19]; (iv) up regulation of efflux pumps[17] and (v) the presence of other potential target genes[20]. We primarily aimed to (1) investigate the TCS resistome from the soil metagenome using functional metagenomics-based screening, (2) to investigate any resistance to other antibiotics conferred by ARGs colocalized with TCS resistance determinants, (3) to perform comprehensive profiling of both prototypic and TCS-resistant metagenomic ENR diversity from different environments, and (4) to assess selective specific ENR abundance in presumably TCS-rich environments
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