Abstract
The interest in livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) strains is increasing due to their wide distribution and transmission even in persons without previous contact with livestock, and these strains pose a public health threat. The aim of the study was the genetic characterization of the whole genome of two epidemiologically unrelated t034 LA-MRSA strains previously isolated from the nasal cavities of a goat and a farmer in Greece. Both strains were assigned to the ST398-Vc-t034 type and they were carrying a single transposon identical to Tn6133. They harbored genes conferring resistance to several antibiotics (aminoglycosides, β-lactams, macrolides, streptogramin B, tetracycline, and trimethoprim), and genes associated with virulence (enterotoxins, γ-hemolysins, and aureolysin). The present study can serve as baseline for further LA-MRSA epidemiological and evolutionary studies in Greece, while awareness and increased surveillance are needed to avoid their spread.
Availability of data and material
The whole genome sequences of G-MRSA and H-MRSA were submitted to European Nucleotide Archive (ENA) under the study PRJEB39748 and received the accession numbers ERS4944046 and ERS4944047, respectively.
References
Mediavilla JR et al (2012) Global epidemiology of community-associated methicillin resistant Staphylococcus aureus (CA-MRSA). Curr Opin Microbiol 15(5):588–595
Voss A et al (2005) Methicillin-resistant Staphylococcus aureus in pig farming. Emerg Infect Dis 11(12):1965–1966
Armand-Lefevre L, Ruimy R, Andremont A (2005) Clonal comparison of Staphylococcus aureus isolates from healthy pig farmers, human controls, and pigs. Emerg Infect Dis 11(5):711–714
Mascaro V et al (2018) Prevalence of livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) among farm and slaughterhouse workers in Italy. J Occup Environ Med 60(8):e416–e425
Bosch T et al (2016) Changing characteristics of livestock-associated meticillin-resistant Staphylococcus aureus isolated from humans - emergence of a subclade transmitted without livestock exposure, the Netherlands, 2003 to 2014. Euro Surveill 21(21)
Bosch T et al (2016) Next-generation sequencing confirms presumed nosocomial transmission of livestock-associated methicillin-resistant Staphylococcus aureus in the Netherlands. Appl Environ Microbiol 82(14):4081–4089
Price LB et al (2012) Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 3(1)
Sarrou S et al (2015) Dissemination of methicillin-susceptible CC398 Staphylococcus aureus strains in a rural Greek area. PLoS One 10(4):e0122761
Kinross P et al (2017) Livestock-associated meticillin-resistant Staphylococcus aureus (MRSA) among human MRSA isolates, European Union/European Economic Area countries, 2013. Euro Surveill 22(44).
Hetem DJ et al (2016) Molecular epidemiology of MRSA in 13 ICUs from eight European countries. J Antimicrob Chemother 71(1):45–52
Drougka E et al (2016) Interspecies spread of Staphylococcus aureus clones among companion animals and human close contacts in a veterinary teaching hospital. A cross-sectional study in Greece. Prev Vet Med 126:190–8
Papadopoulos P et al (2019) Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in bulk tank milk, livestock and dairy-farm personnel in north-central and north-eastern Greece: Prevalence, characterization and genetic relatedness. Food Microbiol 84:103249
Stegger M et al (2013) Rapid differentiation between livestock-associated and livestock-independent Staphylococcus aureus CC398 clades. PLoS One 8(11):e79645
Larsen MV et al (2012) Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 50(4):1355–1361
Camacho C et al (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421
Joensen KG et al (2014) Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol 52(5):1501–1510
Carattoli A et al (2014) In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 58(7):3895–3903
Alcock BP et al (2020) CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 48(D1):D517–D525
Clausen P, Aarestrup FM, Lund O (2018) Rapid and precise alignment of raw reads against redundant databases with KMA. BMC Bioinformatics 19(1):307
Siguier P et al (2006) ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34(Database issue):D32-6
Brettin T et al (2015) RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 5:8365
Wulf M, Voss A (2008) MRSA in livestock animals-an epidemic waiting to happen? Clin Microbiol Infect 14(6):519–521
Cuny C, Kock R, Witte W (2013) Livestock associated MRSA (LA-MRSA) and its relevance for humans in Germany. Int J Med Microbiol 303(6–7):331–337
Sarrou S et al (2016) Characterization of a novel lsa(E)- and lnu(B)-carrying structure located in the chromosome of a Staphylococcus aureus Sequence Type 398 Strain. Antimicrob Agents Chemother 60(2):1164–1166
Deurenberg RH et al (2007) The molecular evolution of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 13(3):222–235
Schwendener S, Perreten V (2011) New transposon Tn6133 in methicillin-resistant Staphylococcus aureus ST398 contains vga(E), a novel streptogramin A, pleuromutilin, and lincosamide resistance gene. Antimicrob Agents Chemother 55(10):4900–4904
Cavaco LM et al (2010) Cloning and occurrence of czrC, a gene conferring cadmium and zinc resistance in methicillin-resistant Staphylococcus aureus CC398 isolates. Antimicrob Agents Chemother 54(9):3605–3608
Hasman H, Aarestrup FM (2002) tcrB, a gene conferring transferable copper resistance in Enterococcus faecium: occurrence, transferability, and linkage to macrolide and glycopeptide resistance. Antimicrob Agents Chemother 46(5):1410–1416
Schijffelen MJ et al (2010) Whole genome analysis of a livestock-associated methicillin-resistant Staphylococcus aureus ST398 isolate from a case of human endocarditis. BMC Genomics 11:376
Kadlec K et al (2012) Novel and uncommon antimicrobial resistance genes in livestock-associated methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 18(8):745–755
McCarthy AJ, Lindsay JA (2012) The distribution of plasmids that carry virulence and resistance genes in Staphylococcus aureus is lineage associated. BMC Microbiol 12:104
Wettstein Rosenkranz K et al (2014) Nasal carriage of methicillin-resistant Staphylococcus aureus (MRSA) among Swiss veterinary health care providers: detection of livestock- and healthcare-associated clones. Schweiz Arch Tierheilkd 156(7):317–325
Larsen J et al (2016) Copresence of tet(K) and tet(M) in livestock-associated methicillin-resistant Staphylococcus aureus clonal complex 398 is associated with increased fitness during exposure to sublethal concentrations of tetracycline. Antimicrob Agents Chemother 60(7):4401–4403
Cuny C et al (2015) Prevalence of the immune evasion gene cluster in Staphylococcus aureus CC398. Vet Microbiol 177(1–2):219–223
Benito D et al (2013) Detection of methicillin-susceptible Staphylococcus aureus ST398 and ST133 strains in gut microbiota of healthy humans in Spain. Microb Ecol 66(1):105–111
Shukla SK et al (2010) Virulence genes and genotypic associations in nasal carriage, community-associated methicillin-susceptible and methicillin-resistant USA400 Staphylococcus aureus isolates. J Clin Microbiol 48(10):3582–3592
Peacock SJ et al (2002) Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect Immun 70(9):4987–4996
Monecke S et al (2011) A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One 6(4):e17936
Mama OM et al (2020) High prevalence of multidrug resistant S. aureus-CC398 and frequent detection of enterotoxin genes among non-CC398 S. aureus from pig-derived food in Spain. Int J Food Microbiol 320:108510
Wang L et al (2015) Characterization of insertion sequence ISSau2 in the human and livestock-associated Staphylococcus aureus. PLoS One 10(5):e0127183
Fessler AT et al (2017) Complete sequence of a plasmid from a bovine methicillin-resistant Staphylococcus aureus harbouring a novel ica-like gene cluster in addition to antimicrobial and heavy metal resistance genes. Vet Microbiol 200:95–100
Tuchscherr LP et al (2007) Characterization of a new variant of IS257 that has displaced the capsule genes within bovine isolates of Staphylococcus aureus. Infect Immun 75(11):5483–5488
Sarrou S et al (2018) MLSB-resistant Staphylococcus aureus in central Greece: rate of resistance and molecular characterization. Microb Drug Resist
Hauschild T et al (2012) Detection of the novel vga(E) gene in methicillin-resistant Staphylococcus aureus CC398 isolates from cattle and poultry. J Antimicrob Chemother 67(2):503–504
Petinaki E, Spiliopoulou I (2012) Methicillin-resistant Staphylococcus aureus among companion and food-chain animals: impact of human contacts. Clin Microbiol Infect 18(7):626–634
Hansen JE et al (2020) Spread of LA-MRSA CC398 in Danish mink (Neovison vison) and mink farm workers. Vet Microbiol 245:108705
Lakhundi S, Zhang K (2018) Methicillin-resistant Staphylococcus aureus: molecular characterization, evolution, and epidemiology. Clin Microbiol Rev 31(4).
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The current work was supported by the European Union’s Horizon 2020 grant VEO (grant number 874735).
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Responsible Editor: Ilana Camargo
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Karampatakis, T., Papadopoulos, P., Tsergouli, K. et al. Genetic characterization of livestock-associated methicillin-resistant Staphylococcus aureus isolated in Greece. Braz J Microbiol 52, 2091–2096 (2021). https://doi.org/10.1007/s42770-021-00587-z
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DOI: https://doi.org/10.1007/s42770-021-00587-z