Genomic Characteristics of Cfr and FexA Carrying Staphylococcus Aureus Isolated from Pig Carcasses in Korea

Overview

Journal Vet Res

Publisher Biomed Central

Specialty Veterinary Medicine

Date 2024 Feb 16

PMID 38365748

Authors

Eiseul Kim

Seung-Min Yang

Hyo-Sun Kwak

Bo-Youn Moon

Suk-Kyung Lim

Hae-Yeong Kim

Affiliations

Soon will be listed here.

Abstract

The emergence of transferable linezolid resistance genes poses significant challenges to public health, as it does not only confer linezolid resistance but also reduces susceptibility to florfenicol, which is widely used in the veterinary field. This study evaluated the genetic characteristics of linezolid-resistant Staphylococcus aureus strains isolated from pig carcasses and further clarified potential resistance and virulence mechanisms in a newly identified sequence type. Of more than 2500 strains isolated in a prior study, 15 isolated from pig carcasses exhibited linezolid resistance (minimum inhibitory concentration ≥ 8 mg/L). The strains were characterized in detail by genomic analysis. Linezolid-resistant S. aureus strains exhibited a high degree of genetic lineage diversity, with one strain (LNZ_R_SAU_64) belonging to ST8004, which has not been reported previously. The 15 strains carried a total of 21 antibiotic resistance genes, and five carried mecA associated with methicillin resistance. All strains harbored cfr and fexA, which mediate resistance to linezolid, phenicol, and other antibiotics. Moreover, the strains carried enterotoxin gene clusters, including the hemolysin, leukotoxin, and protease genes, which are associated with humans or livestock. Some genes were predicted to be carried in plasmids or flanked by ISSau9 and the transposon Tn554, thus being transmittable between staphylococci. Strains carrying the plasmid replicon repUS5 displayed high sequence similarity (99%) to the previously reported strain pSA737 in human clinical samples in the United States. The results illustrate the need for continuous monitoring of the prevalence and transmission of linezolid-resistant S. aureus isolated from animals and their products.

Citing Articles

Genetic Complexity of CC5 Isolates Associated with Sternal Bursitis in Chickens: Antimicrobial Resistance, Virulence, Plasmids, and Biofilm Formation.

Silva V, Ribeiro J, Teixeira P, Pinto P, Vieira-Pinto M, Poeta P Pathogens. 2024; 13(6).

PMID: 38921816 PMC: 11206601. DOI: 10.3390/pathogens13060519.

References

Liang Y, Tu C, Tan C, Ahmed M, Dai M, Xia Y . Antimicrobial resistance, virulence genes profiling and molecular relatedness of methicillin-resistant strains isolated from hospitalized patients in Guangdong Province, China. Infect Drug Resist. 2019; 12:447-459. PMC: 6394240. DOI: 10.2147/IDR.S192611. View

Rao S, Linke L, Magnuson R, Jauch L, Hyatt D . Antimicrobial resistance and genetic diversity of collected from livestock, poultry and humans. One Health. 2022; 15:100407. PMC: 9582408. DOI: 10.1016/j.onehlt.2022.100407. View

Chuang Y, Huang Y . Livestock-associated meticillin-resistant Staphylococcus aureus in Asia: an emerging issue?. Int J Antimicrob Agents. 2015; 45(4):334-40. DOI: 10.1016/j.ijantimicag.2014.12.007. View

Bender J, Fleige C, Klare I, Fiedler S, Mischnik A, Mutters N . Detection of a cfr(B) Variant in German Enterococcus faecium Clinical Isolates and the Impact on Linezolid Resistance in Enterococcus spp. PLoS One. 2016; 11(11):e0167042. PMC: 5125667. DOI: 10.1371/journal.pone.0167042. View

Feltrin F, Alba P, Kraushaar B, Ianzano A, Argudin M, Di Matteo P . A Livestock-Associated, Multidrug-Resistant, Methicillin-Resistant Staphylococcus aureus Clonal Complex 97 Lineage Spreading in Dairy Cattle and Pigs in Italy. Appl Environ Microbiol. 2015; 82(3):816-21. PMC: 4725266. DOI: 10.1128/AEM.02854-15. View

MASON W, Blevins J, Beenken K, Wibowo N, Ojha N, Smeltzer M . Multiplex PCR protocol for the diagnosis of staphylococcal infection. J Clin Microbiol. 2001; 39(9):3332-8. PMC: 88340. DOI: 10.1128/JCM.39.9.3332-3338.2001. View

Yoon S, Ha S, Lim J, Kwon S, Chun J . A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek. 2017; 110(10):1281-1286. DOI: 10.1007/s10482-017-0844-4. View

Bastos M, Murphy E . Transposon Tn554 encodes three products required for transposition. EMBO J. 1988; 7(9):2935-41. PMC: 457088. DOI: 10.1002/j.1460-2075.1988.tb03152.x. View

Lim S, Nam H, Jang G, Lee H, Jung S, Kwak H . The first detection of methicillin-resistant Staphylococcus aureus ST398 in pigs in Korea. Vet Microbiol. 2011; 155(1):88-92. DOI: 10.1016/j.vetmic.2011.08.011. View

10.

Moawad A, Hotzel H, Awad O, Roesler U, Hafez H, Tomaso H . Evolution of Antibiotic Resistance of Coagulase-Negative Staphylococci Isolated from Healthy Turkeys in Egypt: First Report of Linezolid Resistance. Microorganisms. 2019; 7(10). PMC: 6843140. DOI: 10.3390/microorganisms7100476. View

11.

Ozawa M, Furuya Y, Akama R, Harada S, Matsuda M, Abo H . Molecular epidemiology of methicillin-resistant Staphylococcus aureus isolated from pigs in Japan. Vet Microbiol. 2022; 273:109523. DOI: 10.1016/j.vetmic.2022.109523. View

12.

Adame-Gomez R, Castro-Alarcon N, Vences-Velazquez A, Toribio-Jimenez J, Perez-Valdespino A, Leyva-Vazquez M . Genetic Diversity and Virulence Factors of Isolated from Food, Humans, and Animals. Int J Microbiol. 2020; 2020:1048097. PMC: 7474365. DOI: 10.1155/2020/1048097. View

13.

Mendes R, Deshpande L, Jones R . Linezolid update: stable in vitro activity following more than a decade of clinical use and summary of associated resistance mechanisms. Drug Resist Updat. 2014; 17(1-2):1-12. DOI: 10.1016/j.drup.2014.04.002. View

14.

Egan S, Corcoran S, McDermott H, Fitzpatrick M, Hoyne A, McCormack O . Hospital outbreak of linezolid-resistant and vancomycin-resistant ST80 Enterococcus faecium harbouring an optrA-encoding conjugative plasmid investigated by whole-genome sequencing. J Hosp Infect. 2020; 105(4):726-735. DOI: 10.1016/j.jhin.2020.05.013. View

15.

Zecconi A, Scali F . Staphylococcus aureus virulence factors in evasion from innate immune defenses in human and animal diseases. Immunol Lett. 2013; 150(1-2):12-22. DOI: 10.1016/j.imlet.2013.01.004. View

16.

Kim E, Shin S, Kwak H, Cha M, Yang S, Gwak Y . Prevalence and Characteristics of Phenicol-Oxazolidinone Resistance Genes in and Isolated from Food-Producing Animals and Meat in Korea. Int J Mol Sci. 2021; 22(21). PMC: 8583520. DOI: 10.3390/ijms222111335. View

17.

Koser C, Ellington M, Peacock S . Whole-genome sequencing to control antimicrobial resistance. Trends Genet. 2014; 30(9):401-7. PMC: 4156311. DOI: 10.1016/j.tig.2014.07.003. View

18.

Su M, Satola S, Read T . Genome-Based Prediction of Bacterial Antibiotic Resistance. J Clin Microbiol. 2018; 57(3). PMC: 6425178. DOI: 10.1128/JCM.01405-18. View

19.

Moodley A, Espinosa-Gongora C, Nielsen S, McCarthy A, Lindsay J, Guardabassi L . Comparative host specificity of human- and pig- associated Staphylococcus aureus clonal lineages. PLoS One. 2012; 7(11):e49344. PMC: 3498157. DOI: 10.1371/journal.pone.0049344. View

20.

Kim S, Kim G, Lee G, Yang S . Multilocus sequence type-dependent activity of human and animal cathelicidins against community-, hospital-, and livestock-associated methicillin-resistant isolates. J Anim Sci Technol. 2022; 64(3):515-530. PMC: 9184701. DOI: 10.5187/jast.2022.e32. View