Chlorine disinfection facilitates natural transformation through ROS-mediated oxidative stress

Abstract

The bacterial infection that involves antimicrobial resistance is a rising global threat to public health. Chlorine-based water disinfection processes can inactivate antibiotic resistant bacteria. However, at the same time, these processes may cause the release of antibiotic resistance genes into the water as free DNA, and consequently increase the risk to disseminate antibiotic resistance via natural transformation. Presently, little is known about the contribution of residual chlorine affecting the transformation of extracellular antibiotic resistance genes (ARGs). This study investigates whether chloramine and free chlorine promote the transformation of ARGs and how this may occur. We reveal that both chloramine and free chlorine, at practically relevant concentrations, significantly stimulated the transformation of plasmid-encoded ARGs by the recipient Acinetobacter baylyi ADP1, by up to a 10-fold increase. The underlying mechanisms underpinning the increased transformations were revealed. Disinfectant exposure induced a series of cell responses, including increased levels of reactive oxygen species (ROS), bacterial membrane damage, ROS-mediated DNA damage, and increased stress response. These effects thus culminated in the enhanced transformation of ARGs. This promoted transformation was observed when exposing disinfectant-pretreated A. baylyi to free plasmid. In contrast, after pretreating free plasmid with disinfectants, the transformation of ARGs decreased due to the damage of plasmid integrity. These findings provide important insight on the roles of disinfectants affecting the horizontal transfer of ARGs, which could be crucial in the management of antibiotic resistance in our water systems.

Artificial sweeteners stimulate horizontal transfer of extracellular antibiotic resistance genes through natural transformation

“…Previous studies have reported that antibiotics can damage cell envelope or block cell membrane synthesis to increase cell envelope permeability and then promote gene transfer by transformation [49,50]. Recent studies also ascribed the increased transformation frequency to the increased cell envelope permeability by disinfectant chlorine [41,51].…”

Characteristics of Antibiotic Resistance Genes and Antibiotic-Resistant Bacteria in Full-Scale Drinking Water Treatment System Using Metagenomics and Culturing

“…Additionally, multidrug (multidrug_transporter, mex E, sme B, sme C, sme D, sme E, and sme F), aminoglycoside [ aad A, aph (6)-1, aph (3’)-IIb], beta-lactam (metallo-beta-lactamase, TEM -1, TEM -117, TEM -157, TEM -187, TEM -205, TEM -75, TEM -91, and TEM -118), and rifamycin (rifampin monooxygenase) were enriched. With respect to the phenomenon that some ARGs increased after chlorine disinfection, some researchers have pointed out that free chlorine could promote the transformation of ARGs through a series of cell responses, for example, raising levels of reactive oxygen species (ROS), ROS-mediated DNA damage, and bacterial membrane damage ( Zhang et al, 2021 ). Our results indicated that chlorination reduced the diversity of the ARG types.…”

Transcriptomic Responses of Salmonella enterica Serovars Enteritidis in Sodium Hypochlorite

“…In Table 2 , DEGs encoding outer ( sthB , invG , yohG , apeE , yaiU ) and inner membranes ( ydgK , yddG , yeiH , yhjD ) were upregulated. This may be due to the cellular response induced by NaClO stress on Salmonella leading to cell membrane disruption and thus stimulating the expression of genes associated with cell membrane proteins ( Zhang et al., 2021 ). Xiao et al.…”