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 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.

Comparative Genomics of Listeria Species Recovered from Meat and Food Processing Facilities

“…The STs identified in L. welshimeri were ST1005, ST1084, and ST168. This MLST results tally with two studies conducted in China ( 28 ) and Ireland ( 6 ) which showed the STs detected in the presumed nonpathogenic Listeria spp. were ST537, ST1005, ST1084, and ST168 belonging to L. innocua and L. welshimeri, respectively.…”

“…Some studies have shown L. monocytogenes can acquire resistance genes from the environment through plasmids and transposons, leading to the gradual increase in L. Monocytogenes resistance ( 6 , 40 ). Wu et al ( 28 ) showed Listeria carry multiple resistance genes tetA , tetM , ermA , ermB , ermC , and aac(6′)-Ib . Generally, resistant genes tetB and tetM are frequently detected in mobile plasmids ( 41 ).…”

Genomic Characterization of Listeria innocua Isolates Recovered from Cattle Farms, Beef Abattoirs, and Retail Outlets in Gauteng Province, South Africa

“…Similarly, Hanes and Huang [ 62 ] reported that in the USA, from 2010 through 2021, data analysis identified fosX , lin , abc-f , and tet ( M ) as the four most common AMR genes found in L. monocytogenes. Compared with published reports on resistance genes in L. innocua , the distribution of the resistance genes varied considerably [ 28 , 29 ].…”

“…Variable frequencies of AMR genes have been reported in strains of L. monocytogenes , L. innocua , and other Listeria spp. [ 28 , 29 ]. Hosain et al [ 30 ] have highlighted the potential negative impact of AMR on therapy in feed animals and humans.…”

Whole-genome sequencing of Listeria monocytogenes isolated from the first listeriosis foodborne outbreak in South Korea

“…Lincomycin and tetracycline are used for clinical practice to inhibit protein synthesis in bacteria. Previous studies showed resistance to lincomycin in L. monocytogenes isolated from foods in Italy (100%) and food processing environments in China (90%) (Mauro et al, 2007;Wu et al, 2021). Lincomycin inhibits protein synthesis by binding to the 50S ribosomal subunit (Papich, 2016).…”