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Evolution of a major bovine mastitic genotype (rpoB sequence type 10-2) of Staphylococcus aureus in cows

  • Dae-Sung Ko
  • Danil Kim
  • Eun-Kyung Kim
  • Jae-Hong Kim
  • Hyuk-Joon KwonEmail author
Article

Abstract

Staphylococcus aureus is the major pathogen leading to bovine mastitis globally while livestock-associated methicillin resistant S. aureus (LA-MRSA) has become a potential threat to public health. MRSA from bovine mastitis is not common but a methicillin susceptible S. aureus (MSSA) genotype, rpoB sequence type (RST)10-2 (RST10-2), is prevalent in Korea. To date, many genomic sequences from S. aureus have been elucidated, but the complete genome sequences of RST10-2 MSSA from bovine mastitis has never been reported. In this study, we determined the complete genome sequence of two RST10-2 MSSA that differ from each other in staphylococcal protein A and molecular prophage types [PMB64-1 (t2489/ mPPT0) and PMB81-4 (t127/mPPT1-2-3)] and conducted a comparative genomics study. The genomic sequences of PMB64-1 and PMB81-4 were more homologous to the representative human RST10-2 strains (MSSA476, MW2 etc.) compared to other RSTs. Most of them shared five common pseudogenes, along with high amino acid identity of four variable virulence genes that were identified in this study. However, PMB64-1 and PMB81-4 acquired different strainspecific pseudogenes and mobile genetic elements than the human strains. The unique pseudogene profile and high identity of the virulence genes were verified in RST10-2 field strains from bovine mastitis. Thus, bovine mastitic RST10-2 MSSA may have an evolutionary relationship with the human RST10-2 community-associated (CA) MSSA and CA-MRSA strains but may have adapted to cows.

Keywords

Staphylococcus aureus bovine mastitis comparative genomics pseudogenes virulence genes 

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References

  1. Alba, P., Feltrin, F., Cordaro, G., Porrero, M.C., Kraushaar, B., Argudin, M.A., Nykasenoja, S., Monaco, M., Stegger, M., Aarestrup, F.M., et al. 2015. Livestock-associated methicillin resistant and methicillin susceptible Staphylococcus aureus sequence type (CC)1 in European farmed animals: High genetic relatedness of isolates from Italian cattle herds and humans. PLoS One 10, e0137143.Google Scholar
  2. Arndt, D., Grant, J.R., Marcu, A., Sajed, T., Pon, A., Liang, Y., and Wishart, D.S. 2016. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res. 44, W16–21.CrossRefGoogle Scholar
  3. Baba, T., Bae, T., Schneewind, O., Takeuchi, F., and Hiramatsu, K. 2008. Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes: polymorphism and evolution of two major pathogenicity islands. J. Bacteriol. 190, 300–310.CrossRefGoogle Scholar
  4. Baba, T., Takeuchi, F., Kuroda, M., Yuzawa, H., Aoki, K., Oguchi, A., Nagai, Y., Iwama, N., Asano, K., Naimi, T., et al. 2002. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359, 1819–1827.CrossRefGoogle Scholar
  5. Battisti, A., Franco, A., Merialdi, G., Hasman, H., Iurescia, M., Lorenzetti, R., Feltrin, F., Zini, M., and Aarestrup, F.M. 2010. Heterogeneity among methicillin-resistant Staphylococcus aureus from Italian pig finishing holdings. Vet. Microbiol. 142, 361–366.CrossRefGoogle Scholar
  6. Fitzgerald, J.R., Sturdevant, D.E., Mackie, S.M., Gill, S.R., and Musser, J.M. 2001. Evolutionary genomics of Staphylococcus aureus: insights into the origin of methicillin-resistant strains and the toxic shock syndrome epidemic. Proc. Natl. Acad. Sci. USA 98, 8821–8826.CrossRefGoogle Scholar
  7. Garcia, P., Martinez, B., Obeso, J.M., Lavigne, R., Lurz, R., and Rodriguez, A. 2009. Functional genomic analysis of two Staphylococcus aureus phages isolated from the dairy environment. Appl. Environ. Microbiol. 75, 7663–7673.CrossRefGoogle Scholar
  8. Gill, S.R., Fouts, D.E., Archer, G.L., Mongodin, E.F., Deboy, R.T., Ravel, J., Paulsen, I.T., Kolonay, J.F., Brinkac, L., Beanan, M., et al. 2005. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillinresistant Staphylococcus epidermidis strain. J. Bacteriol. 187, 2426–2438.CrossRefGoogle Scholar
  9. Guinane, C.M., Ben Zakour, N.L., Tormo-Mas, M.A., Weinert, L.A., Lowder, B.V., Cartwright, R.A., Smyth, D.S., Smyth, C.J., Lindsay, J.A., Gould, K.A., et al. 2010. Evolutionary genomics of Staphylococcus aureus reveals insights into the origin and molecular basis of ruminant host adaptation. Genome Biol. Evol. 2, 454–466.CrossRefGoogle Scholar
  10. Herron-Olson, L., Fitzgerald, J.R., Musser, J.M., and Kapur, V. 2007. Molecular correlates of host specialization in Staphylococcus aureus. PLoS One 2, e1120.CrossRefGoogle Scholar
  11. Hiramatsu, K., Ito, T., Tsubakishita, S., Sasaki, T., Takeuchi, F., Morimoto, Y., Katayama, Y., Matsuo, M., Kuwahara-Arai, K., Hishinuma, T., et al. 2013. Genomic basis for methicillin resistance in Staphylococcus aureus. Infect. Chemother. 45, 117–136.CrossRefGoogle Scholar
  12. Holden, M.T., Feil, E.J., Lindsay, J.A., Peacock, S.J., Day, N.P., Enright, M.C., Foster, T.J., Moore, C.E., Hurst, L., Atkin, R., et al. 2004. Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc. Natl. Acad. Sci. USA 101, 9786–9791.CrossRefGoogle Scholar
  13. IWG-SCC, E. 2009. Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob. Agents Chemother. 53, 4961–4967.CrossRefGoogle Scholar
  14. Jeon, J., D’Souza, R., Hong, S.K., Lee, Y., Yong, D., Choi, J., Lee, K., and Chong, Y. 2014. complete genome sequence of the bacteriophage YMC/09/04/R1988 MRSA BP: A lytic phage from a methicillin-resistant Staphylococcus aureus isolate. FEMS Microbiol. Lett. 359, 144–146.CrossRefGoogle Scholar
  15. Jevons, M.P. 1961. Celebin-resistant staphylococci. Br. Med. J. 1, 124–125.CrossRefGoogle Scholar
  16. Jia, H., Bai, Q., Yang, Y., and Yao, H. 2013. Complete genome sequence of Staphylococcus aureus siphovirus phage JS01. Genome Announc. 1, e00797-13.CrossRefGoogle Scholar
  17. Kaya, H., Hasman, H., Larsen, J., Stegger, M., Johannesen, T.B., Allesoe, R.L., Lemvigh, C.K., Aarestrup, F.M., Lund, O., and Larsen, A.R. 2018. SCCmecFinder, a web-based tool for typing of staphylococcal cassette chromosome mec in Staphylococcus aureus using whole-genome sequence data. mSphere 3, e00612-17.Google Scholar
  18. Kim, D., Kim, E.K., Seong, W.J., Ro, Y.H., Ko, D.S., Kim, N.H., Kim, J.H., and Kwon, H.J. 2017. Identification of microbiome with 16S rRNA gene pyrosequencing and antimicrobial effect of egg white in bovine mastitis. Korean J. Vet. Res. 57, 117–126.Google Scholar
  19. Ko, D.S., Seong, W.J., Kim, D., Kim, E.K., Kim, N.H., Lee, C.Y., Kim, J.H., and Kwon, H.J. 2018. Molecular prophage typing of Staphylococcus aureus isolates from bovine mastitis. J. Vet. Sci. 19, 771–781.CrossRefGoogle Scholar
  20. Koren, S., Walenz, B.P., Berlin, K., Miller, J.R., Bergman, N.H., and Phillippy, A.M. 2017. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 27, 722–736.CrossRefGoogle Scholar
  21. Le Loir, Y., Baron, F., and Gautier, M. 2003. Staphylococcus aureus and food poisoning. Genet. Mol. Res. 2, 63–76.Google Scholar
  22. Lerat, E. and Ochman, H. 2005. Recognizing the pseudogenes in bacterial genomes. Nucleic Acids Res. 33, 3125–3132.CrossRefGoogle Scholar
  23. Lowder, B.V., Guinane, C.M., Ben Zakour, N.L., Weinert, L.A., Conway-Morris, A., Cartwright, R.A., Simpson, A.J., Rambaut, A., Nubel, U., and Fitzgerald, J.R. 2009. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 106, 19545–19550.CrossRefGoogle Scholar
  24. Lowy, F.D. 2000. Is Staphylococcus aureus an intracellular pathogen? Trends Microbiol. 8, 341–343.CrossRefGoogle Scholar
  25. Lyon, B.R., May, J.W., and Skurray, R.A. 1984. Tn4001: a gentamicin and kanamycin resistance transposon in Staphylococcus aureus. Mol. Gen. Genet. 193, 554–556.CrossRefGoogle Scholar
  26. Ma, X.X., Ito, T., Kondo, Y., Cho, M., Yoshizawa, Y., Kaneko, J., Katai, A., Higashiide, M., Li, S., and Hiramatsu, K. 2008. Two different Panton-valentine leukocidin phage lineages predominate in Japan. J. Clin. Microbiol. 46, 3246–3258.CrossRefGoogle Scholar
  27. Mariem, B.J., Ito, T., Zhang, M., Jin, J., Li, S., Ilhem, B.B., Adnan, H., Han, X., and Hiramatsu, K. 2013. Molecular characterization of methicillin-resistant Panton-valentine leukocidin positive Staphylococcus aureus clones disseminating in Tunisian hospitals and in the community. BMC Microbiol. 13, 2.CrossRefGoogle Scholar
  28. McArthur, A.G., Waglechner, N., Nizam, F., Yan, A., Azad, M.A., Baylay, A.J., Bhullar, K., Canova, M.J., De Pascale, G., Ejim, L., et al. 2013. The comprehensive antibiotic resistance database. Antimicrob. Agents Chemother. 57, 3348–3357.CrossRefGoogle Scholar
  29. Monaco, M., Pedroni, P., Sanchini, A., Bonomini, A., Indelicato, A., and Pantosti, A. 2013. Livestock-associated methicillin-resistant Staphylococcus aureus responsible for human colonization and infection in an area of Italy with high density of pig farming. BMC Infect. Dis. 13, 258.CrossRefGoogle Scholar
  30. Moon, B.Y., Park, J.Y., Hwang, S.Y., Robinson, D.A., Thomas, J.C., Fitzgerald, J.R., Park, Y.H., and Seo, K.S. 2015. Phage-mediated horizontal transfer of a Staphylococcus aureus virulence-associated genomic island. Sci. Rep. 5, 9784.CrossRefGoogle Scholar
  31. Moon, B.Y., Park, J.Y., Robinson, D.A., Thomas, J.C., Park, Y.H., Thornton, J.A., and Seo, K.S. 2016. Mobilization of genomic islands of Staphylococcus aureus by temperate bacteriophage. PLoS One 11, e0151409.Google Scholar
  32. Nguyen, M.T., Kraft, B., Yu, W., Demircioglu, D.D., Hertlein, T., Burian, M., Schmaler, M., Boller, K., Bekeredjian-Ding, I., Ohlsen, K., et al. 2015. The νSaα specific lipoprotein like cluster (lpl) of S. aureus USA300 contributes to immune stimulation and invasion in human cells. PLoS Pathog. 11, e1004984.CrossRefGoogle Scholar
  33. Novick, R.P., Christie, G.E., and Penades, J.R. 2010. The phage-related chromosomal islands of Gram-positive bacteria. Nat. Rev. Microbiol. 8, 541–551.CrossRefGoogle Scholar
  34. Sakwinska, O., Giddey, M., Moreillon, M., Morisset, D., Waldvogel, A., and Moreillon, P. 2011. Staphylococcus aureus host range and human-bovine host shift. Appl. Environ. Microbiol. 77, 5908–5915.CrossRefGoogle Scholar
  35. Seong, W.J., Kim, J.H., and Kwon, H.J. 2013. Comparison of complete rpoB gene sequence typing and multi-locus sequence typing for phylogenetic analysis of Staphylococcus aureus. J. Gen. Appl. Microbiol. 59, 335–343.CrossRefGoogle Scholar
  36. Sutra, L. and Poutrel, B. 1994. Virulence factors involved in the pathogenesis of bovine intramammary infections due to Staphylococcus aureus. J. Med. Microbiol. 40, 79–89.CrossRefGoogle Scholar
  37. Viana, D., Comos, M., McAdam, P.R., Ward, M.J., Selva, L., Guinane, C.M., Gonzalez-Munoz, B.M., Tristan, A., Foster, S.J., Fitzgerald, J.R., et al. 2015. A single natural nucleotide mutation alters bacterial pathogen host tropism. Nat. Genet. 47, 361–366.CrossRefGoogle Scholar
  38. Weinert, L.A., Welch, J.J., Suchard, M.A., Lemey, P., Rambaut, A., and Fitzgerald, J.R. 2012. Molecular dating of human-to-bovid host jumps by Staphylococcus aureus reveals an association with the spread of domestication. Biol. Lett. 8, 829–832.CrossRefGoogle Scholar

Copyright information

© The Microbiological Society of Korea 2019

Authors and Affiliations

  • Dae-Sung Ko
    • 1
    • 2
  • Danil Kim
    • 1
  • Eun-Kyung Kim
    • 1
  • Jae-Hong Kim
    • 2
    • 3
  • Hyuk-Joon Kwon
    • 1
    • 3
    Email author
  1. 1.Department of Farm Animal MedicineSeoulRepublic of Korea
  2. 2.Laboratory of Avian DiseasesSeoulRepublic of Korea
  3. 3.The Research Institute for Veterinary Science, College of Veterinary Medicine and BK21 for Veterinary ScienceSeoul National UniversitySeoulRepublic of Korea

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