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Coresistance to Benzalkonium Chloride Disinfectant and Heavy Metal Ions in Listeria monocytogenes and Listeria innocua Swine Isolates from China.

Abstract

The development of coresistance to disinfectants and heavy metals contributes to the fitness of Listeria spp. in foods or food processing environments, where life-threatening Listeria monocytogenes coexist and coevolve with other Listeria spp. Despite extensive research on L. monocytogenes, coresistance to disinfectants and heavy metals is less documented for other Listeria spp. In this study, we screened 30 L. monocytogenes and 27 Listeria innocua isolates recovered from 273 swine samples for resistance to quaternary ammonium compound benzalkonium chloride (BC) and to heavy metals cadmium (Cd) and arsenic (As). Moreover, we evaluated the potential mechanisms of resistance by detecting the efflux pump activity in BC resistance and the presence of resistance determinants. The average minimum inhibitory concentrations of BC in L. innocua (10.7 ± 2.0) were significantly higher than that in L. monocytogenes (6.9 ± 3.7) (p < 0.05). Resistance to BC and heavy metals was correlated, where all BC-resistant L. innocua and As-resistant L. monocytogenes isolates were coresistant to BC and Cd. Twenty percent and 66.7% of BC resistance in L. monocytogenes and L. innocua were related to reserpine-associated efflux pumps, whereas all cases of BC resistance were related to carbonyl cyanide 3-chlorophenylhydrazone-associated efflux pumps. The cadA1 and cadA2 genes were present in Cd-resistant isolates but not in Cd-sensitive isolates, and cadA3 was undetectable in all isolates examined. cadA4 conferring lower level of Cd resistance was copresent with arsA1 and arsA2 in the Cd-resistant and As-susceptible L. monocytogenes isolate LM3. Our findings suggest that swine serves as a reservoir for developing resistance to disinfectant and heavy metals in L. monocytogenes and L. innocua, which share common resistance mechanisms such as efflux pumps and resistance genes. This work provides new insight into the coresistance events of other Listeria as a potential contributor of the resistance in L. monocytogenes.

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  • Authors+Show Affiliations

    ,

    1 School of Food Science and Technology, South China University of Technology, Guangzhou, China.

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    2 State Key Testing Laboratory of Aquatic Products, Guangzhou Airport Entry-Exit Inspection and Quarantine Bureau, Guangzhou, China.

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    1 School of Food Science and Technology, South China University of Technology, Guangzhou, China.

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    3 Institute of Food Safety and Nutrition, Jinan University, Guangzhou, China. 4 State Key Laboratory of Food Safety Technology for Meat Products, Fujian, China.

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    2 State Key Testing Laboratory of Aquatic Products, Guangzhou Airport Entry-Exit Inspection and Quarantine Bureau, Guangzhou, China.

    1 School of Food Science and Technology, South China University of Technology, Guangzhou, China.

    Source

    Pub Type(s)

    Journal Article

    Language

    eng

    PubMed ID

    31120347

    Citation

    Xu, Dongyang, et al. "Coresistance to Benzalkonium Chloride Disinfectant and Heavy Metal Ions in Listeria Monocytogenes and Listeria Innocua Swine Isolates From China." Foodborne Pathogens and Disease, 2019.
    Xu D, Deng Y, Fan R, et al. Coresistance to Benzalkonium Chloride Disinfectant and Heavy Metal Ions in Listeria monocytogenes and Listeria innocua Swine Isolates from China. Foodborne Pathog Dis. 2019.
    Xu, D., Deng, Y., Fan, R., Shi, L., Bai, J., & Yan, H. (2019). Coresistance to Benzalkonium Chloride Disinfectant and Heavy Metal Ions in Listeria monocytogenes and Listeria innocua Swine Isolates from China. Foodborne Pathogens and Disease, doi:10.1089/fpd.2018.2608.
    Xu D, et al. Coresistance to Benzalkonium Chloride Disinfectant and Heavy Metal Ions in Listeria Monocytogenes and Listeria Innocua Swine Isolates From China. Foodborne Pathog Dis. 2019 May 22; PubMed PMID: 31120347.
    * Article titles in AMA citation format should be in sentence-case
    TY - JOUR T1 - Coresistance to Benzalkonium Chloride Disinfectant and Heavy Metal Ions in Listeria monocytogenes and Listeria innocua Swine Isolates from China. AU - Xu,Dongyang, AU - Deng,Yan, AU - Fan,Rongdong, AU - Shi,Lei, AU - Bai,Jianshan, AU - Yan,He, Y1 - 2019/05/22/ PY - 2019/5/24/entrez KW - KW - arsenic KW - benzalkonium chloride KW - cadmium JF - Foodborne pathogens and disease JO - Foodborne Pathog. Dis. N2 - The development of coresistance to disinfectants and heavy metals contributes to the fitness of Listeria spp. in foods or food processing environments, where life-threatening Listeria monocytogenes coexist and coevolve with other Listeria spp. Despite extensive research on L. monocytogenes, coresistance to disinfectants and heavy metals is less documented for other Listeria spp. In this study, we screened 30 L. monocytogenes and 27 Listeria innocua isolates recovered from 273 swine samples for resistance to quaternary ammonium compound benzalkonium chloride (BC) and to heavy metals cadmium (Cd) and arsenic (As). Moreover, we evaluated the potential mechanisms of resistance by detecting the efflux pump activity in BC resistance and the presence of resistance determinants. The average minimum inhibitory concentrations of BC in L. innocua (10.7 ± 2.0) were significantly higher than that in L. monocytogenes (6.9 ± 3.7) (p < 0.05). Resistance to BC and heavy metals was correlated, where all BC-resistant L. innocua and As-resistant L. monocytogenes isolates were coresistant to BC and Cd. Twenty percent and 66.7% of BC resistance in L. monocytogenes and L. innocua were related to reserpine-associated efflux pumps, whereas all cases of BC resistance were related to carbonyl cyanide 3-chlorophenylhydrazone-associated efflux pumps. The cadA1 and cadA2 genes were present in Cd-resistant isolates but not in Cd-sensitive isolates, and cadA3 was undetectable in all isolates examined. cadA4 conferring lower level of Cd resistance was copresent with arsA1 and arsA2 in the Cd-resistant and As-susceptible L. monocytogenes isolate LM3. Our findings suggest that swine serves as a reservoir for developing resistance to disinfectant and heavy metals in L. monocytogenes and L. innocua, which share common resistance mechanisms such as efflux pumps and resistance genes. This work provides new insight into the coresistance events of other Listeria as a potential contributor of the resistance in L. monocytogenes. SN - 1556-7125 UR - https://www.unboundmedicine.com/medline/citation/31120347/Coresistance_to_Benzalkonium_Chloride_Disinfectant_and_Heavy_Metal_Ions_in_Listeria_monocytogenes_and_Listeria_innocua_Swine_Isolates_from_China L2 - https://www.liebertpub.com/doi/full/10.1089/fpd.2018.2608?url_ver=Z39.88-2003&amp;rfr_id=ori:rid:crossref.org&amp;rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -