Antimicrobial susceptibility, multilocus sequence typing, and virulence of listeria isolated from a slaughterhouse in Jiangsu, China

Abstract Background Listeria monocytogenes is one of the deadliest foodborne pathogens. The bacterium can tolerate severe environments through biofilm formation and antimicrobial resistance. This study aimed to investigate the antimicrobial susceptibility, resistance genes, virulence, and molecular...

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Main Authors: Liting Wu, Hongduo Bao, Zhengquan Yang, Tao He, Yuan Tian, Yan Zhou, Maoda Pang, Ran Wang, Hui Zhang
Format: Article
Language:English
Published: BMC 2021-11-01
Series:BMC Microbiology
Subjects:
Online Access:https://doi.org/10.1186/s12866-021-02335-7
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author Liting Wu
Hongduo Bao
Zhengquan Yang
Tao He
Yuan Tian
Yan Zhou
Maoda Pang
Ran Wang
Hui Zhang
author_facet Liting Wu
Hongduo Bao
Zhengquan Yang
Tao He
Yuan Tian
Yan Zhou
Maoda Pang
Ran Wang
Hui Zhang
author_sort Liting Wu
collection DOAJ
description Abstract Background Listeria monocytogenes is one of the deadliest foodborne pathogens. The bacterium can tolerate severe environments through biofilm formation and antimicrobial resistance. This study aimed to investigate the antimicrobial susceptibility, resistance genes, virulence, and molecular epidemiology about Listeria from meat processing environments. Methods This study evaluated the antibiotic resistance and virulence of Listeria isolates from slaughtering and processing plants. All isolates were subjected to antimicrobial susceptibility testing using a standard microbroth dilution method. The harboring of resistant genes was identified by polymerase chain reaction. The multilocus sequence typing was used to determine the subtyping of the isolates and characterize possible routes of contamination from meat processing environments. The virulence of different STs of L. monocytogenes isolates was evaluated using a Caco-2 cell invasion assay. Results A total of 59 Listeria isolates were identified from 320 samples, including 37 L. monocytogenes isolates (62.71%). This study evaluated the virulence of L. monocytogenes and the antibiotic resistance of Listeria isolates from slaughtering and processing plants. The susceptibility of these 59 isolates against 8 antibiotics was analyzed, and the resistance levels to ceftazidime, ciprofloxacin, and lincomycin were as high as 98.31% (L. m 37; L. innocua 7; L. welshimeri 14), 96.61% (L. m 36; L. innocua 7; L. welshimeri 14), and 93.22% (L. m 35; L. innocua 7; L. welshimeri 13), respectively. More than 90% of the isolates were resistant to three to six antibiotics, indicating that Listeria isolated from meat processing environments had high antimicrobial resistance. Up to 60% of the isolates harbored the tetracycline-resistance genes tetA and tetM. The frequency of ermA, ermB, ermC, and aac(6′)-Ib was 16.95, 13.56, 15.25, and 6.78%, respectively. Notably, the resistant phenotype and genotype did not match exactly, suggesting that the mechanisms of antibiotic resistance of these isolates were likely related to the processing environment. Multilocus sequence typing (MLST) revealed that 59 Listeria isolates were grouped into 10 sequence types (STs). The dominant L. monocytogenes STs were ST5, ST9, and ST121 in the slaughtering and processing plant of Jiangsu province. Moreover, ST5 subtypes exhibited high invasion in Caco-2 cells compared with ST9 and ST121 cells. Conclusion The dominant L. monocytogenes ST5 persisted in the slaughtering and processing plant and had high antimicrobial resistance and invasion characteristics, illustrating a potential risk in food safety and human health.
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spelling doaj.art-ddbe349eb0a04137953267194d7d7bcf2022-12-21T18:03:57ZengBMCBMC Microbiology1471-21802021-11-0121111310.1186/s12866-021-02335-7Antimicrobial susceptibility, multilocus sequence typing, and virulence of listeria isolated from a slaughterhouse in Jiangsu, ChinaLiting Wu0Hongduo Bao1Zhengquan Yang2Tao He3Yuan Tian4Yan Zhou5Maoda Pang6Ran Wang7Hui Zhang8Jiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base of MOST, Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural SciencesJiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base of MOST, Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural SciencesCollege of Food Science and Engineering, Yangzhou UniversityJiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base of MOST, Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural SciencesJiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base of MOST, Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural SciencesJiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base of MOST, Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural SciencesJiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base of MOST, Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural SciencesJiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base of MOST, Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural SciencesJiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base of MOST, Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural SciencesAbstract Background Listeria monocytogenes is one of the deadliest foodborne pathogens. The bacterium can tolerate severe environments through biofilm formation and antimicrobial resistance. This study aimed to investigate the antimicrobial susceptibility, resistance genes, virulence, and molecular epidemiology about Listeria from meat processing environments. Methods This study evaluated the antibiotic resistance and virulence of Listeria isolates from slaughtering and processing plants. All isolates were subjected to antimicrobial susceptibility testing using a standard microbroth dilution method. The harboring of resistant genes was identified by polymerase chain reaction. The multilocus sequence typing was used to determine the subtyping of the isolates and characterize possible routes of contamination from meat processing environments. The virulence of different STs of L. monocytogenes isolates was evaluated using a Caco-2 cell invasion assay. Results A total of 59 Listeria isolates were identified from 320 samples, including 37 L. monocytogenes isolates (62.71%). This study evaluated the virulence of L. monocytogenes and the antibiotic resistance of Listeria isolates from slaughtering and processing plants. The susceptibility of these 59 isolates against 8 antibiotics was analyzed, and the resistance levels to ceftazidime, ciprofloxacin, and lincomycin were as high as 98.31% (L. m 37; L. innocua 7; L. welshimeri 14), 96.61% (L. m 36; L. innocua 7; L. welshimeri 14), and 93.22% (L. m 35; L. innocua 7; L. welshimeri 13), respectively. More than 90% of the isolates were resistant to three to six antibiotics, indicating that Listeria isolated from meat processing environments had high antimicrobial resistance. Up to 60% of the isolates harbored the tetracycline-resistance genes tetA and tetM. The frequency of ermA, ermB, ermC, and aac(6′)-Ib was 16.95, 13.56, 15.25, and 6.78%, respectively. Notably, the resistant phenotype and genotype did not match exactly, suggesting that the mechanisms of antibiotic resistance of these isolates were likely related to the processing environment. Multilocus sequence typing (MLST) revealed that 59 Listeria isolates were grouped into 10 sequence types (STs). The dominant L. monocytogenes STs were ST5, ST9, and ST121 in the slaughtering and processing plant of Jiangsu province. Moreover, ST5 subtypes exhibited high invasion in Caco-2 cells compared with ST9 and ST121 cells. Conclusion The dominant L. monocytogenes ST5 persisted in the slaughtering and processing plant and had high antimicrobial resistance and invasion characteristics, illustrating a potential risk in food safety and human health.https://doi.org/10.1186/s12866-021-02335-7Antimicrobial resistanceAntimicrobial resistance genesListeriaMLSTVirulence
spellingShingle Liting Wu
Hongduo Bao
Zhengquan Yang
Tao He
Yuan Tian
Yan Zhou
Maoda Pang
Ran Wang
Hui Zhang
Antimicrobial susceptibility, multilocus sequence typing, and virulence of listeria isolated from a slaughterhouse in Jiangsu, China
BMC Microbiology
Antimicrobial resistance
Antimicrobial resistance genes
Listeria
MLST
Virulence
title Antimicrobial susceptibility, multilocus sequence typing, and virulence of listeria isolated from a slaughterhouse in Jiangsu, China
title_full Antimicrobial susceptibility, multilocus sequence typing, and virulence of listeria isolated from a slaughterhouse in Jiangsu, China
title_fullStr Antimicrobial susceptibility, multilocus sequence typing, and virulence of listeria isolated from a slaughterhouse in Jiangsu, China
title_full_unstemmed Antimicrobial susceptibility, multilocus sequence typing, and virulence of listeria isolated from a slaughterhouse in Jiangsu, China
title_short Antimicrobial susceptibility, multilocus sequence typing, and virulence of listeria isolated from a slaughterhouse in Jiangsu, China
title_sort antimicrobial susceptibility multilocus sequence typing and virulence of listeria isolated from a slaughterhouse in jiangsu china
topic Antimicrobial resistance
Antimicrobial resistance genes
Listeria
MLST
Virulence
url https://doi.org/10.1186/s12866-021-02335-7
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