Class 1 integron carrying qacEΔ1 gene confers resistance to disinfectant and antibiotics in Salmonella

Shujuan Chen; Jingxia Fu; Ke Zhao; Shengzhi Yang; Chun Li; Petri Penttinen; Xiaolin Ao; Aiping Liu; Kaidi Hu; Jianlong Li; Yong Yang; Shuliang Liu; Li Bai; Likou Zou

doi:10.1016/j.ijfoodmicro.2023.110319

Class 1 integron carrying qacEΔ1 gene confers resistance to disinfectant and antibiotics in Salmonella

Int J Food Microbiol. 2023 Nov 2:404:110319. doi: 10.1016/j.ijfoodmicro.2023.110319. Epub 2023 Jul 13.

Authors

Shujuan Chen¹, Jingxia Fu², Ke Zhao³, Shengzhi Yang³, Chun Li⁴, Petri Penttinen³, Xiaolin Ao¹, Aiping Liu¹, Kaidi Hu¹, Jianlong Li¹, Yong Yang¹, Shuliang Liu¹, Li Bai⁵, Likou Zou⁶

Affiliations

¹ College of Food Science, Sichuan Agricultural University, Ya'an, Sichuan, China.
² College of Resource, Sichuan Agricultural University, Chengdu, Sichuan, China; College of Environment, Sichuan Agricultural University, Chengdu, Sichuan, China.
³ College of Resource, Sichuan Agricultural University, Chengdu, Sichuan, China.
⁴ Sichuan Province Center for Animal Disease Prevention and Control, Chengdu, Sichuan, China.
⁵ National Health Commission Key Laboratory of Food Safety Risk Assessment, Food Safety Research Unit (2019RU014) of Chinese Academy of Medical Science, China National Center for Food Safety Risk Assessment, Beijing, China. Electronic address: baili@cfsa.net.cn.
⁶ College of Resource, Sichuan Agricultural University, Chengdu, Sichuan, China. Electronic address: zoulikou@sicau.edu.cn.

PMID: 37473468
DOI: 10.1016/j.ijfoodmicro.2023.110319

Abstract

Salmonella has presented increasingly alarming rates of antimicrobial resistance believed to be a result of a high prevalence of integrons. It is speculated that disinfectant-resistant isolates are due to the expression of qacEΔ1, an efflux pump located in the 3' conserved sequence (3'CS) of class 1 integrons. With this concern, we tested the antibiotic and disinfectant resistance of 581 Salmonella strains collected from different sources, and characterized their integron structures. Gene expression and induction experiments were also performed. Results showed that Salmonella have high resistance to antimicrobials, especially to sulfonamides (SAs, 78.83 %), tetracyclines (TCs, 75.04 %) and benzalkonium chloride (BC, 87.26 %). The multi-drug resistance (MDR) frequency reached up to 63.17 %, and the prevalence of intI1 was 45.78 %. Molecular characterization of class 1 integrons exhibited nine different gene cassette arrays, of these, dfrA12-orf-aadA2 (n = 75), EstX (n = 25) and aadA2 (n = 14) were the most frequent. Importantly, 74.06 % of intI1-positive isolates were carrying qacEΔ1-sul1 genes in the 3'CS. This study also demonstrated that phenotypic resistance to both antibiotics and disinfectants was significantly correlated with the emergence of intI1 (p < 0.05). 91.37 % of qacEΔ1-sul1 positive Salmonella were found with disinfectant resistance. Additionally, expression of qacEΔ1 gene in Escherichia coli confirmed qacEΔ1 is predominantly involved in conferring disinfectant resistance. Disinfectant induction experiments further implicated qacEΔ1 in disinfectant resistance. RT-qPCR revealed a disinfectant-mediated increase in the relative expression of antibiotic-resistant genes (ARGs), aadA2 and dfrA12 on the integron, and efflux pump genes (mdtH and acrD) indicating that disinfectant could trigger co or cross-resistance. Therefore, our study confirmed that using disinfectant could provide selection pressure for strains with acquired resistance to antibiotics, providing new insights into the public health impact of Salmonella and guide continued efforts in antimicrobial stewardship and prevention of antibiotic resistance.

Keywords: Class 1 integron; Disinfectant resistance; Salmonella; qacEΔ1 gene.

MeSH terms

Anti-Bacterial Agents / pharmacology
Disinfectants* / pharmacology
Drug Resistance, Bacterial / genetics
Drug Resistance, Multiple, Bacterial / genetics
Escherichia coli
Integrons* / genetics
Microbial Sensitivity Tests
Salmonella

Substances

Anti-Bacterial Agents
Disinfectants