Co-occurrence of qacEΔ1 disinfectant resistance gene and ARGs among Salmonella Indiana and its correlation with resistance to sodium hypochlorite

Abstract

Sodium hypochlorite (SHC) is the most commonly utilized carcass and equipment disinfectant in the poultry industry. However, prolonged exposure to SHC can result in the development of bacterial tolerance and exert co-selection on antimicrobial resistance. This study investigated the co-resistance to SHC and multiple antimicrobial agents among Salmonella enterica serovar Indiana (S. Indiana), with a specific focus on the co-occurrence of disinfectant resistance gene qacEΔ1 and the antimicrobial resistance genes (ARGs) revealed by whole genome sequencing (WGS). Additionally, the study examined the transcriptional response of qacEΔ1 and its closely associated ARGs under SHC pressure. Moreover, the study determined the optimal SHC concentration for the decontamination of multidrug-resistant (MDR) S. Indiana on chicken. The results indicated that S. Indiana exhibited a resistance rate of 73.31 % to SHC, and varying levels of resistance to 13 antimicrobial agents. Furthermore, the analysis revealed a significant correlation between the qacEΔ1 gene and ARGs, including catB3, sul1, arr-3 and bla_OXA-1. The genetic contexts surrounding the qacEΔ1 gene demonstrated a high degree of homology, allowing for the categorization into 11 distinct genetic context types, among which the gene cluster aacA4-bla_OXA-1-catB3-arr-3-qacEΔ1-sul1 was the most prevalent. Further analysis of the MDR IndS97 strain using PacBio SMRT sequencing revealed that the qacEΔ1 gene was located on plasmid pLKQY01, with IS26 and ISRle7 positioned at the flanks of the composite transposon aacA4-bla_OXA-1-catB3-arr-3-qacEΔ1-sul1. The transcription levels of qacEΔ1, arr-3 and sul1 genes in response to SHC stress initially increased, followed by a decline as SHC concentrations rose. At an SHC concentration of 0.5 MIC, the transcription levels of these genes were notably low, and the results indicated a decontamination efficacy of 86.51 % against Salmonella contamination while relatively preserving the freshness of the chicken. This study enhanced the understanding of disinfectant effects on the antimicrobial resistance of S. Indiana and provided evidence to support the regulated use of disinfectants.