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Genomic characterization of Staphylococcus aureus from Canastra Minas Artisanal Cheeses

  • Food Microbiology - Research Paper
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Abstract

Canastra Minas Artisanal Cheese is produced in the Brazilian State of Minas Gerais using raw milk, rennet, and pingo, a natural endogenous starter culture (fermented whey) collected from the previous day’s production. Due to the use of raw milk, the product can carry microorganisms that may cause foodborne diseases (FBD), including Staphylococcus aureus. Genomic characterization of S. aureus is an important tool to assess diversity, virulence, antimicrobial resistance, and the potential for causing food poisoning due to enterotoxin production. This study is aimed at exploring the genomic features of S. aureus strains isolated from Canastra Minas Artisanal Cheeses. Multilocus sequence typing (MLST) classified these strains as ST1, ST5, and a new profile ST7849 (assigned to the clonal complex CC97). These strains belonged to four spa types: t008, t127, t359, and t992. We identified antimicrobial resistance genes with phenotypic correlation against methicillin (MRSA) and tetracycline. Virulome analysis revealed genes associated with iron uptake, immune evasion, and potential capacity for adherence and biofilm formation. The toxigenic potential included cyto- and exotoxins genes, and all strains presented the genes that encode for Panton-Valentine toxin and hemolysin, and two strains encoded 4 and 8 Staphylococcal enterotoxin (SE) genes. The results revealed the pathogenic potential of the evaluated S. aureus strains circulating in the Canastra region, representing a potential risk to public health. This study also provides useful information to monitor and guide the application of control measures to the artisanal dairy food production chain.

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Data availability

The assembled genome sequences were deposited in GenBank under BioProject number PRJNA803870 and accession numbers JAKNRH000000000, JAKNRI000000000, JAKNRJ000000000, JAKNRK000000000, and JAKNRL000000000.

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Acknowledgements

The authors thank the Sao Paulo Research Foundation (FAPESP, Brazil) for the financial support (grant #2013/07914-8) to the Food Research Center. We thank Fabiana da Silva Lima, Loredana d’Ovidio, and Luciano Queiroz for technical assistance during library preparation for WGS. We also thank Christian Hoffmann for the helpful discussions and critical review of the manuscript. We extend our special gratitude to each cheese producer who actively participated in this study, demonstrating eagerness to contribute not only to this research but also to the various other studies we undertake.

Funding

This work was supported by “Fundação de Amparo a Pesquisa de Sao Paulo (FAPESP-Brazil-grant #2013/07914–8).

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Author notes

  1. Ana P. Arellano Pineda, Carmen L. Rodríguez Cueva, and Ruy D. Chacón contributed equally to this work.

Authors and Affiliations

  1. Food Research Center, Department of Food and Experimental Nutrition, Faculty of Pharmaceutical Sciences, University of São Paulo, Av. Prof. Lineu Prestes, 580, São Paulo, SP, 05508-000, Brazil

    Ana P. Arellano Pineda, Débora P. de Oliveira, Bernadette D. G. M. Franco, Mariza Landgraf & Uelinton Manoel Pinto

  2. Laboratory of Biology and Molecular Genetics, Faculty of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, 15021, Peru

    Carmen L. Rodríguez Cueva

  3. Department of Pathology, School of Veterinary Medicine, University of São Paulo, Av. Prof. Orlando M. Paiva, 87, São Paulo, SP, 05508-270, Brazil

    Ruy D. Chacón

  4. Faculty of Science and Health, Peruvian University of Applied Sciences-UPC, Prolongación Primavera 2390, Santiago de Surco, Lima, 15023, Peru

    Manuel Ramírez

  5. Department of Clinical Analysis, Toxicology and Food Science, Faculty of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Avenida Do Café, S/N, Ribeirão Preto, SP, 14040-903, Brazil

    Otávio G. G. de Almeida

  6. Federal Institute of Minas Gerais - Campus Bambuí, Bambuí, MG, 30575-180, Brazil

    Gustavo Lacorte

  7. Department of Food Sciences and Nutrition, Faculty of Food Engineering, State University of Campinas (UNICAMP), Campinas, São Paulo, Brazil

    Nathalia Cristina Cirone Silva

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  1. Ana P. Arellano Pineda
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Contributions

Conceptualization: Gustavo Lacorte and Uelinton M. Pinto; methodology: Ana P.A. Pineda, Carmen L.R. Cueva, Ruy D. Chacón, Manuel Ramírez, Débora P. Oliveira, and Gustavo Lacorte; formal analysis and investigation: Ana P.A. Pineda, Carmen L.R. Cueva, Ruy D. Chácon, Manuel Ramírez, Otávio G.G. Almeida, Débora P. Oliveira, Gustavo Lacorte, and Nathalia C.S. Silva; writing—original draft preparation: Ana P.A. Pineda, Carmen L.R. Cueva, and Ruy D. Chácon; writing—review and editing: Manuel Ramírez, Otávio G.G. Almeida, Bernadette D.G.M. Franco, Nathalia C.S. Silva, and Uelinton M. Pinto; funding acquisition: Bernadette D.G.M. Franco, Mariza Landgraf, and Uelinton M. Pinto; resources: Bernadette D.G.M. Franco, Mariza Landgraf, and Uelinton M. Pinto; supervision: Bernadette D.G.M. Franco, Gustavo Lacorte, Mariza Landgraf, Nathalia C.S. Silva, and Uelinton M. Pinto.

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Correspondence to Uelinton Manoel Pinto.

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Pineda, A.P.A., Cueva, C.L.R., Chacón, R.D. et al. Genomic characterization of Staphylococcus aureus from Canastra Minas Artisanal Cheeses. Braz J Microbiol 54, 2103–2116 (2023). https://doi.org/10.1007/s42770-023-01099-8

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