Genes de virulência e resistência antimicrobiana detectados em Staphylococcus spp. isolados de mastite clínica e não clínica usando sequenciamento do genoma completo

Autores

  • Nathália Cristina Cirone Silva Universidade Estadual de Campinas https://orcid.org/0000-0002-2839-1416
  • Marjory Xavier Rodrigues Cornell University
  • Ana Carolina de Campos Henrique Tomazi Cornell University
  • Tiago Tomazi Cornell University https://orcid.org/0000-0001-8978-6254
  • Bruna Lourenço Crippa Universidade Estadual de Campinas https://orcid.org/0000-0003-2235-6879
  • Liliana de Oliveira Rocha Universidade Estadual de Campinas
  • Rodrigo Carvalho Bicalho Cornell University

DOI:

https://doi.org/10.5433/1679-0359.2024v44n2p393

Palavras-chave:

Análise genética, Estafilococos, Gado leiteiro, Segurança de alimentos.

Resumo

Staphylococcus spp. estão entre as bactérias mais isoladas em casos de mastite clínica e subclínica em bovinos leiteiros. O gênero compreende bactérias formadoras de biofilme capazes de produzir toxinas e adquirir resistência a múltiplos medicamentos. Este trabalho teve como objetivo avaliar o perfil genético relacionado às características de virulência e resistência antimicrobiana de Staphylococcus spp., isolados de mastites clínicas e vacas recém paridas não clínicas, utilizando sequenciamento do genoma completo (WGS). A coleta bacteriana foi composta por 29 Staphylococcus isolados de casos clínicos de mastite (n = 7), além de amostras de leite coletadas de vacas recém paridas (n = 22). Os isolados foram identificadas como Staphylococcus aureus (n = 2), Staphylococcus chromogenes (n = 19) e Staphylococcus haemolyticus (n = 8). Foram observados um total de 94 genes de virulência, incluindo genes pvl, icaA, icaD e componentes de superfície microbiana que reconhecem moléculas de matriz adesiva (MSCRAMMs). Também foram detectados importantes genes de resistência como blaZ, ant(4), erm(B), fexA, lnu(D), tet(L) e tet(M). A árvore filogenética listou as espécies conforme o esperado e apresentou quatro clados. Uma variedade de genes de virulência e resistência foram detectados. Além disso, a expressão de genes importantes como os responsáveis pela formação de biofilmes e enterotoxinas pode representar um risco à saúde dos consumidores. sendo uma preocupação para a saúde pública.

Métricas

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Biografia do Autor

Nathália Cristina Cirone Silva , Universidade Estadual de Campinas

Prof.. Dra., Departamento de Ciência de Alimentos e Nutrição, Faculdade de Engenharia de Alimentos, FEA, Universidade Estadual de Campinas UNICAMP, Campinas, SP, Brasil.

Marjory Xavier Rodrigues , Cornell University

Researcher at the Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.

Ana Carolina de Campos Henrique Tomazi , Cornell University

Researcher at the Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.

Tiago Tomazi, Cornell University

Researcher at the Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.

Bruna Lourenço Crippa, Universidade Estadual de Campinas

Doutoranda do Programa de Pós-Graduação em Ciência dos Alimentos (PPGCA), Faculdade de Engenharia de Alimentos (FEA), UNICAMP, Campinas, SP, Brasil.

Liliana de Oliveira Rocha, Universidade Estadual de Campinas

Profa. Dra., Departamento de Ciência de Alimentos e Nutrição, Faculdade de Engenharia de Alimentos, FEA, Universidade Estadual de Campinas UNICAMP, Campinas, SP, Brasil.

Rodrigo Carvalho Bicalho, Cornell University

Researcher at the Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.

Referências

Aarestrup, F. M., Wegener, H. C., Rosdahl, V. T., & Jensen, N. E., (1995). Staphylococcal and other bacterial species associated with intramammary infections in Danish dairy herds. Acta Veterinaria Scandinavica, 36(4), 475-487. doi: 10.1186/bf03547662 DOI: https://doi.org/10.1186/BF03547662

Almeida, R. A., Matthews, K. R., Cifrian, E., Guidry, A. J., & Oliver, S. P. (1996). Staphylococcus aureus invasion of bovine mammary epithelial cells. Journal of Dairy Science, 79(6), 1021-1026. doi: 10.3168/jds.S0022-0302(96)76454-8 DOI: https://doi.org/10.3168/jds.S0022-0302(96)76454-8

Aslantaş, Ö., & Demir, C. (2016). Investigation of the antibiotic resistance and biofilm-forming ability of Staphylococcus aureus from subclinical bovine mastitis cases. Journal of Dairy Science, 99(11), 8607-8613. doi: 10.3168/jds.2016-11310 DOI: https://doi.org/10.3168/jds.2016-11310

Babić, M.S., & Bonomo, R.A. (2009). Mutations as a basis of antimicrobial resistance. In D. L. Mayers (Ed.), Antimicrobial drug resistance (vol. 1, pp. 65-74). Humana Press. https://doi.org/10.1007/978-1-59745-180-2_6 DOI: https://doi.org/10.1007/978-1-59745-180-2_6

Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., Lesin, V. M., Nikolenko, S. I., Pham, S., Prjibelski, A. D., Pyshkin, A. V., Sirotkin, A. V., Vyahhi, N., Tesler, G., Alekseyev, M. A., & Pevzner, P. A. (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology 19(5), 455-477. doi: 10.1089/cmb.2012.0021 DOI: https://doi.org/10.1089/cmb.2012.0021

Brettin, T., Davis, J. J., Disz, T., Edwards, R. A., Gerdes, S., Olsen, G. J., Olson, R., Overbeek, R., Parrello, B., Pusch, G. D., Shukla, M., Thomason, J. A., Stevens, R., Vonstein, V., Wattam, A. R., & Xia, F. (2015). RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Scientific Reports, 5, 8365. doi: 10.1038/srep08365 DOI: https://doi.org/10.1038/srep08365

Capurro, A. C., Aspán, A., Unnerstad, H. E., Waller, K. P., & Artursson, K. (2010). Identification of potential sources of Staphylococcus aureus in herds with mastitis problems. Journal of Dairy Science, 93 1, 180-91. doi: 10.3168/jds.2009-2471 DOI: https://doi.org/10.3168/jds.2009-2471

Cucarella, C., Tormo, M. A., Knecht, E., Amorena, B., Lasa, I., Foster, T. J., & Penadés, J. R. (2002). Expression of the biofilm-associated protein interferes with host protein receptors of Staphylococcus aureus and alters the infective process. Infection and Immunity, 70(6), 3180-3186. doi: 10.1128/IAI.70.6.3180-3186.2002 DOI: https://doi.org/10.1128/IAI.70.6.3180-3186.2002

Fitzpatrick, F., Humphreys, H., & O'Gara, J. P. (2005). The genetics of staphylococcal biofilm formation will a greater understanding of pathogenesis lead to better management of device-related infection? Clinical Microbiology and Infection, 11(12), 967-973. doi: 10.1111/j.1469-0691.2005.01274.x DOI: https://doi.org/10.1111/j.1469-0691.2005.01274.x

Freitas Guimarães, F. de, Nóbrega, D. B., Richini-Pereira, V. B., Marson, P. M., Figueiredo Pantoja, J. C. de, &. Langoni, H. (2013). Enterotoxin genes in coagulase-negative and coagulase-positive staphylococci isolated from bovine milk. Journal of Dairy Science, 96(5), 2866-2872. doi: 10.3168/jds.2012-5864 DOI: https://doi.org/10.3168/jds.2012-5864

Frey, Y., Rodriguez, J. P., Thomann, A., Schwendener, S., & Perreten, V. (2013). Genetic characterization of antimicrobial resistance in coagulase-negative staphylococci from bovine mastitis milk. Journal of Dairy Science, 96(4), 2247-2257. doi: 10.3168/jds.2012-6091 DOI: https://doi.org/10.3168/jds.2012-6091

Fuda, C. C., Fisher, J. F., & Mobashery, S. (2005). Beta-lactam resistance in Staphylococcus aureus: the adaptive resistance of a plastic genome. Cellular and Molecular Life Sciences, 62(22), 2617-2633. doi: 10.1007/s00018-005-5148-6 DOI: https://doi.org/10.1007/s00018-005-5148-6

Garzoni, C., & Kelley, W. L. (2009). Staphylococcus aureus: new evidence for intracellular persistence. Trends in Microbiology, 17(2), 59-65. doi: 10.1016/j.tim.2008.11.005 DOI: https://doi.org/10.1016/j.tim.2008.11.005

Ghebremedhin, B., Layer, F., König, W., & König, B. (2008). Genetic classification and distinguishing of Staphylococcus species based on different partial gap, 16S rRNA, hsp60, rpoB, sodA, and tuf gene sequences. Journal of Clinical Microbiology, 46(3), 1019-1025. doi: 10.1128/JCM.02058-07 DOI: https://doi.org/10.1128/JCM.02058-07

Goerke, C., Köller, J., & Wolz, C. (2006). Ciprofloxacin and trimethoprim cause phage induction and virulence modulation in Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 50(1), 171-177. doi: 10.1128/AAC.50.1.171-177.2006 DOI: https://doi.org/10.1128/AAC.50.1.171-177.2006

Haran, K. P., Godden, S. M., Boxrud, D., Jawahir, S., Bender, J. B., & Sreevatsan, S. (2012). Prevalence and characterization of Staphylococcus aureus, including methicillin-resistant Staphylococcus aureus, isolated from bulk tank milk from Minnesota dairy farms. Journal of Clinical Microbiology, 50(3), 688-695. doi: 10.1128/JCM.05214-11 DOI: https://doi.org/10.1128/JCM.05214-11

Harkins, C. P., Pichon, B., Doumith, M., Parkhill, J., Westh, H., Tomasz, A., Lencastre, S. D. de, Bentley, H., Kearns, A. M., & Holden, M. T. G. (2017). Methicillin-resistant Staphylococcus aureus emerged long before the introduction of methicillin into clinical practice. Genome Biology, 18(1), 130. doi: 10.1186/s13059-017-1252-9 DOI: https://doi.org/10.1186/s13059-017-1252-9

Joensen, K. G., Scheutz, F., Lund, O., Hasman, H., Kaas, R. S., Nielsen, E. M., & Aarestrup, F. M. (2014). Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. Journal of Clinical Microbiology, 52(5), 1501-1510. doi: 10.1128/JCM.03617-13 DOI: https://doi.org/10.1128/JCM.03617-13

Kerro Dego, O., van Dijk, J. E., & Nederbragt, H. (2002). Factors involved in the early pathogenesis of bovine Staphylococcus aureus mastitis with emphasis on bacterial adhesion and invasion. A review. Veterinary Quarterly, 24(4), 181-198. doi: 10.1080/01652176.2002.9695135 DOI: https://doi.org/10.1080/01652176.2002.9695135

Lamers, R. P., Muthukrishnan, G., Castoe, T. A., Tafur, S., Cole, A. M., & Parkinson, C. L. (2012). Phylogenetic relationships among Staphylococcus species and refinement of cluster groups based on multilocus data. BMC Evolutionary Biology, 12, 171. doi: 10.1186/1471-2148-12-171 DOI: https://doi.org/10.1186/1471-2148-12-171

Leclercq, R. (2002). Mechanisms of resistance to macrolides and lincosamides: nature of the resistance elements and their clinical implications. Clinical Infectious Diseases, 34(4), 482-492. doi: 10.1086/324626 DOI: https://doi.org/10.1086/324626

Levison, L. J., Miller-Cushon, E. K., Tucker, A. L., Bergeron, R., Leslie, K. E., Barkema, H. W., & DeVries, T. J. (2016). Incidence rate of pathogen-specific clinical mastitis on conventional and organic Canadian dairy farms. Journal of Dairy Science, 99(2), 1341-1350. doi: 10.3168/jds.2015-9809 DOI: https://doi.org/10.3168/jds.2015-9809

Li, L., Wang, G., Cheung, A., Abdelhady, W., Seidl, K., &. Xiong, Y. Q. (2019). MgrA governs adherence, host cell interaction, and virulence in a murine model of bacteremia due to Staphylococcus aureus. Journal of Infectious Diseases, 220(6), 1019-1028. doi: 10.1093/infdis/jiz219 DOI: https://doi.org/10.1093/infdis/jiz219

Lozano, C., Aspíroz, C., Sáenz, Y., Ruiz-García, M., Royo-García, G., Gómez-Sanz, E., Ruiz‐Larrea, F., Zarazaga, M., & Torres, C. (2012). Genetic environment and location of the lnu(A) and lnu(B) genes in methicillin-resistant Staphylococcus aureus and other staphylococci of animal and human origin. The Journal of Antimicrobial Chemotherapy, 67(12), 2804-8. doi: 10.1093/jac/dks320 DOI: https://doi.org/10.1093/jac/dks320

Mahmmod, Y. S., Nonnemann, B., Svennesen, L., Pedersen, K., & Klaas, I. C. (2018). Typeability of MALDI-TOF assay for identification of non-aureus staphylococci associated with bovine intramammary infections and teat apex colonization. Journal of Dairy Science, 101(10), 9430-9438. doi: 10.3168/jds.2018-14579 DOI: https://doi.org/10.3168/jds.2018-14579

Matthews, K. R., Harmon, R. J., & Smith, B. A. (1990). Protective effect of Staphylococcus chromogenes infection against Staphylococcus aureus infection in the lactating bovine mammary gland. Journal of Dairy Science, 73(12), 3457-3462. doi: 10.3168/jds.S0022-0302(90)79044-3 DOI: https://doi.org/10.3168/jds.S0022-0302(90)79044-3

McDougall, S., Parker, K. I., Heuer, C., & Compton, C. W. (2009). A review of prevention and control of heifer mastitis via non-antibiotic strategies. Veterinary Microbiology, 134(1-2), 177-185. doi: 10.1016/j vetmic.2008.09.026 DOI: https://doi.org/10.1016/j.vetmic.2008.09.026

Mei, J. M., Nourbakhsh, F., Ford, C. W., & Holden, D. W. (1997). Identification of Staphylococcus aureus virulence genes in a murine model of bacteraemia using signature-tagged mutagenesis. Molecular Microbiology, 26(2), 399-407. doi: 10.1046/j.1365-2958.1997.5911966.x DOI: https://doi.org/10.1046/j.1365-2958.1997.5911966.x

Morar, M., Bhullar, K., Hughes, D. W., Junop, M., & Wright, G. D. (2009). Structure and mechanism of the lincosamide antibiotic adenylyltransferase LinB. Structure (London, England, 1993), 17(12), 1649-1659. doi: 10.1016/j.str.2009.10.013 DOI: https://doi.org/10.1016/j.str.2009.10.013

Naushad, S., Barkema, H. W., Luby, C., Condas, L. A., Nobrega, D. B., Carson, D. A., & De Buck, J. (2016). Comprehensive phylogenetic analysis of bovine non-aureus Staphylococci species based on whole-genome sequencing. Frontiers in Microbiology, 7, 1990. doi: 10.3389/fmicb.2016.01990 DOI: https://doi.org/10.3389/fmicb.2016.01990

Naushad, S., Naqvi, S. A., Nobrega, D., Luby, C., Kastelic, J. P., Barkema, H. W., & De Buck, J. (2019). Comprehensive virulence gene profiling of bovine non- aureus Staphylococci based on whole-genome sequencing data. Msystems, 4(2), e00098-00018. doi: 10.1128/mSystems.00098-18 DOI: https://doi.org/10.1128/mSystems.00098-18

Nawrotek, P., Karakulska, J., & Fijałkowski, K. (2018). The Staphylococcal Panton-Valentine Leukocidin (PVL). Pet-to-Man Travelling Staphylococci, 9, 117-125. doi: 10.1016/B978-0-12-813547-1.00009-1 DOI: https://doi.org/10.1016/B978-0-12-813547-1.00009-1

Olsen, J. E., Christensen, H., & Aarestrup, F. M. (2006). Diversity and evolution of blaZ from Staphylococcus aureus and coagulase-negative staphylococci. Journal of Antimicrobial Chemotherapy, 57(3), 450-460. doi: 10.1093/jac/dki492 DOI: https://doi.org/10.1093/jac/dki492

Osman, K. M., Abd El-Razik, K. A., Marie, H. S., & Arafa, A. (2015). Relevance of biofilm formation and virulence of different species of coagulase-negative staphylococci to public health. European Journal of Clinical Microbiology & Infectious Diseases, 34(10), 2009-2016. doi: 10.1007/s10096-015-2445-3 DOI: https://doi.org/10.1007/s10096-015-2445-3

Pyörälä, S. (2009). Treatment of mastitis during lactation. Irish Veterinary Journal, 62(Suppl. 4), 40-44. doi: 10.1186/2046-0481-62-S4-S40 DOI: https://doi.org/10.1186/2046-0481-62-S4-S40

Roberts, M. C., & Schwarz, S. (2017). Tetracycline and chloramphenicol resistance mechanisms. In D. Mayers, J. Sobel, M. Ouellette, K. Kaye, & D. Marchaim (Eds.), Antimicrobial drug resistance (pp. 183-193). Cham: Springer. doi: 10.1007/978-3-319-46718-4_15 DOI: https://doi.org/10.1007/978-3-319-46718-4_15

Schwarz, S., & Kehrenberg, C. (2006). Old dogs that learn new tricks: modified antimicrobial agents that escape pre-existing resistance mechanisms. International Journal of Medical Microbiology, 296(Suppl. 41), 45-49. doi: 10.1016/j.ijmm.2006.01.061 DOI: https://doi.org/10.1016/j.ijmm.2006.01.061

Schwarz, S., Shen, J., Kadlec, K., Wang, Y., Brenner Michael, G., Feßler, A. T., & Vester, B. (2016). Lincosamides, streptogramins, phenicols, and pleuromutilins: mode of action and mechanisms of resistance. Cold Spring Harbor Perspectives in Medicine, 6(11), a027037. doi: 10.1101/cshperspect.a027037 DOI: https://doi.org/10.1101/cshperspect.a027037

Silva, N. C. C., Guimarães, F. F., Manzi, M. P., Budri, P. E., Gómez-Sanz, E., Benito, D., Langoni, H., Rall, V. L. M., & Torres, C. (2013). Molecular characterization and clonal diversity of methicillin-susceptible Staphylococcus aureus in milk of cows with mastitis in Brazil. Journal of Dairy Science, 96(11), 6856-6862. doi: 10.3168/jds.2013-6719 DOI: https://doi.org/10.3168/jds.2013-6719

Silva, N. C. C., Guimarães, F. F., Manzi, M. de P., Gómez-Sanz, E., Gómez, P., Araújo, J. P., Jr., Langoni, H., Rall, V. L M., & Torres, C. (2014). Characterization of methicillin-resistant coagulase-negative staphylococci in milk from cows with mastitis in Brazil. Antonie Van Leeuwenhoek, 106(2), 227-233. doi: 10.1007/s10482-014-0185-5 DOI: https://doi.org/10.1007/s10482-014-0185-5

Singh, V. K., Vaish, M., Johansson, T. R., Baum, K. R., Ring, R. P., Singh, S., Shukla, S. K., & Moskovitz, J. (2015). Significance of four methionine sulfoxide reductases in Staphylococcus aureus. PloS one, 10(2), e0117594. doi: 10.1371/journal.pone.0117594 DOI: https://doi.org/10.1371/journal.pone.0117594

Souza, G. Á. A. D., Almeida, A. C. de, Xavier, M. A. S., Silva, L. M. V. da, Sousa, C. N., Sanglard, D. A., & Xavier, A. (2019). Characterization and molecular epidemiology of Staphylococcus aureus strains resistant to beta-lactams isolated from the milk of cows diagnosed with subclinical mastitis. Veterinary World, 12(12), 1931-1939. doi: 10.14202/vetworld.2019.1931-1939 DOI: https://doi.org/10.14202/vetworld.2019.1931-1939

Taponen, S., & Pyörälä, S. (2009). Coagulase-negative staphylococci as cause of bovine mastitis- not so different from Staphylococcus aureus? Veterinary Microbiology, 134(1-2), 29-36. doi: 10.1016/j.vetmic.2008.09.011 DOI: https://doi.org/10.1016/j.vetmic.2008.09.011

Thorberg, B. M., Danielsson-Tham, M. L., Emanuelson, U., & Persson Waller, K. (2009). Bovine subclinical mastitis caused by different types of coagulase-negative staphylococci. Journal of Dairy Science, 92(10), 4962-4970. doi: 10.3168/jds.2009-2184 DOI: https://doi.org/10.3168/jds.2009-2184

Tomazi, T., Goncalves, J. L., Barreiro, J. R., Arcari, M. A., & Santos, M. V. dos. (2015). Bovine subclinical intramammary infection caused by coagulase-negative staphylococci increases somatic cell count but has no effect on milk yield or composition. Journal of Dairy Science, 98(5), 3071-3078. doi: 10.3168/jds.2014-8466 DOI: https://doi.org/10.3168/jds.2014-8466

Tomazi, T., Goncalves, J. L., Barreiro, J. R., Campos Braga, P. A. de, Prada e Silva, L. F., Eberlin, M. N., & Santos, M. V. dos. (2014). Identification of coagulase-negative staphylococci from bovine intramammary infection by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Journal of Clinical Microbiology, 52(5), 1658-1663. doi: 10.1128/JCM.03032-13 DOI: https://doi.org/10.1128/JCM.03032-13

Tomazi, T., Sumnicht, M., Tomazi, A. C. C. H., Silva, J. C. C., Bringhenti, L., Duarte, L. M., Silva, M. M. M., Rodrigues, M. X., & Bicalho, R. C. (2021). Negatively controlled, randomized clinical trial comparing different antimicrobial interventions for treatment of clinical mastitis caused by gram-positivepathogens. Journal of Dairy science, 104(3), 3364–3385. doi: 10.3168/jds.2020-18830 DOI: https://doi.org/10.3168/jds.2020-18830

Tremblay, Y. D., Caron, V., Blondeau, A., Messier, S., & Jacques, M. (2014). Biofilm formation by coagulase-negative staphylococci: impact on the efficacy of antimicrobials and disinfectants commonly used on dairy farms. Veterinary Microbiology, 172(3-4), 511-518. doi: 10.1016/j.vetmic.2014.06.007 DOI: https://doi.org/10.1016/j.vetmic.2014.06.007

Tremblay, Y. D., Lamarche, D., Chever, P., Haine, D., Messier, S., & Jacques, M. (2013). Characterization of the ability of coagulase-negative staphylococci isolated from the milk of Canadian farms to form biofilms. Journal of Dairy Science, 96(1), 234-246. doi: 10.3168/jds.2012-5795 DOI: https://doi.org/10.3168/jds.2012-5795

Valckenier, D., Piepers, S., De Visscher, A., Bruckmaier, R. M., & De Vliegher, S. (2019). Effect of intramammary infection with non-aureus staphylococci in early lactation in dairy heifers on quarter somatic cell count and quarter milk yield during the first 4 months of lactation. Journal of Dairy Science, 102(7), 6442-6453. doi: 10.3168/jds.2018-15913 DOI: https://doi.org/10.3168/jds.2018-15913

Vanderhaeghen, W., Piepers, S., Leroy, F., Van Coillie, E., Haesebrouck, F., & De Vliegher, S. (2014). Invited review: effect, persistence, and virulence of coagulase-negative Staphylococcus species associated with ruminant udder health. Journal of Dairy Science, 97(9), 5275-5293. doi: 10.3168/jds.2013-7775 DOI: https://doi.org/10.3168/jds.2013-7775

Vélez, J. R., Cameron, M., Rodríguez-Lecompte, J. C., Xia, F., Heider, L. C., Saab, M., McClure, J. T., & Sánchez, J. (2017). Whole-Genome sequence analysis of antimicrobial resistance genes in streptococcus uberis and Streptococcus dysgalactiae isolates from canadian dairy herds. Frontiers in Veterinary Science, 4, 63. doi: 10.3389/fvets.2017.00063 DOI: https://doi.org/10.3389/fvets.2017.00063

Wattam, A. R., Davis, J. J., Assaf, R., Boisvert, S., Brettin, T., Bun, C., Conrad, N., Dietrich, E. M., Disz, T., Gabbard, J. L., Gerdes, S., Henry, C. S., Kenyon, R. W., Machi, D., Mao, C., Nordberg, E. K., Olsen, G. J., Murphy-Olson, D. E., Olson, R., ... Stevens, R. L. (2017). Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Research, 45(D1), D535-D542. doi: 10.1093/nar/gkw1017 DOI: https://doi.org/10.1093/nar/gkw1017

Weese, J. S., & van Duijkeren, E. (2010). Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in veterinary medicine. Veterinary of Microbiology, 140(3-4), 418-429. doi: 10.1016/j.vetmic.2009.01.039 DOI: https://doi.org/10.1016/j.vetmic.2009.01.039

Weisburg, W. G., Barns, S. M., Pelletier, D. A., & Lane, D. J. (1991). 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology, 173(2), 697-703. doi: 10.1128/jb.173.2.697-703.1991 DOI: https://doi.org/10.1128/jb.173.2.697-703.1991

Zankari, E., Hasman, H., Cosentino, S., Vestergaard, M., Rasmussen, S., Lund, O., Aarestrup, F. M., & Larsen, M. V. (2012). Identification of acquired antimicrobial resistance genes. Journal of Antimicrobial Chemotherapy, 67(11), 2640-2644. doi: 10.1093/jac/dks261 DOI: https://doi.org/10.1093/jac/dks261

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2024-03-21

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Silva , N. C. C., Rodrigues , M. X., Tomazi , A. C. de C. H., Tomazi, T., Crippa, B. L., Rocha, L. de O., & Bicalho, R. C. (2024). Genes de virulência e resistência antimicrobiana detectados em Staphylococcus spp. isolados de mastite clínica e não clínica usando sequenciamento do genoma completo. Semina: Ciências Agrárias, 44(2), 393–410. https://doi.org/10.5433/1679-0359.2024v44n2p393

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