{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,2]],"date-time":"2026-06-02T10:23:12Z","timestamp":1780395792091,"version":"3.54.1"},"reference-count":38,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2022,2,25]],"date-time":"2022-02-25T00:00:00Z","timestamp":1645747200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004281","name":"National Science Center","doi-asserted-by":"publisher","award":["2015\/19\/B\/NZ7\/00447"],"award-info":[{"award-number":["2015\/19\/B\/NZ7\/00447"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>In the current study, we screened a collection of coagulase-negative staphylococci (CoNS) isolates for orthologues of staphylococcal enterotoxins (SEs) involved in S. aureus-related staphylococcal food poisoning (SFP). The amplicons corresponding to SEs were detected in S. chromogenes, S. epidermidis, S. haemolyticus, S. borealis, S. pasteuri, S. saprophyticus, S. vitulinus, S. warneri, and S. xylosus. All amplicons were sequenced and identified as parts of known S. aureus or S. epidermidis SE genes. Quantitative real-time PCR allowed determining the relative copy number of each SE amplicon. A significant portion of the amplicons of the sea, seb, sec, and seh genes occurred at low copy numbers. Only the amplicons of the sec gene identified in three isolates of S. epidermidis displayed relative copy numbers comparable to sec in the reference enterotoxigenic S. aureus and S. epidermidis strains. Consecutive passages in microbiological media of selected CoNS isolates carrying low copy numbers of sea, seb, sec, and seh genes resulted in a decrease of gene copy number. S. epidermidis isolates harbored a high copy number of sec, which remained stable over the passages. We demonstrated that enterotoxin genes may occur at highly variable copy numbers in CoNS. However, we could identify enterotoxin genes only in whole-genome sequences of CoNS carrying them in a stable form at high copy numbers. Only those enterotoxins were expressed at the protein level. Our results indicate that PCR-based detection of enterotoxin genes in CoNS should always require an additional control, like analysis of their presence in the bacterial genome. We also demonstrate S. epidermidis as a CoNS species harboring SE genes in a stable form at a specific chromosome site and expressing them as a protein.<\/jats:p>","DOI":"10.3390\/ijms23052560","type":"journal-article","created":{"date-parts":[[2022,2,25]],"date-time":"2022-02-25T10:00:40Z","timestamp":1645783240000},"page":"2560","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["Staphylococcal Enterotoxin Genes in Coagulase-Negative Staphylococci\u2014Stability, Expression, and Genomic Context"],"prefix":"10.3390","volume":"23","author":[{"given":"Sylwia","family":"Banaszkiewicz","sequence":"first","affiliation":[{"name":"Department of Food Hygiene and Consumer Health Protection, Wroclaw University of Environmental and Life Sciences, 50-375 Wroclaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1840-9731","authenticated-orcid":false,"given":"Ewa","family":"Wa\u0142ecka-Zacharska","sequence":"additional","affiliation":[{"name":"Department of Food Hygiene and Consumer Health Protection, Wroclaw University of Environmental and Life Sciences, 50-375 Wroclaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Justyna","family":"Schubert","sequence":"additional","affiliation":[{"name":"Department of Food Hygiene and Consumer Health Protection, Wroclaw University of Environmental and Life Sciences, 50-375 Wroclaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0100-0657","authenticated-orcid":false,"given":"Aleksandra","family":"Tabi\u015b","sequence":"additional","affiliation":[{"name":"Department of Food Hygiene and Consumer Health Protection, Wroclaw University of Environmental and Life Sciences, 50-375 Wroclaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0012-4022","authenticated-orcid":false,"given":"Jaros\u0142aw","family":"Kr\u00f3l","sequence":"additional","affiliation":[{"name":"Department of Pathology, Division of Microbiology, Wroclaw University of Environmental and Life Sciences, 50-375 Wroclaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8982-211X","authenticated-orcid":false,"given":"Tadeusz","family":"Stefaniak","sequence":"additional","affiliation":[{"name":"Department of Immunology, Pathophysiology and Veterinary Preventive Medicine, Wroclaw University of Environmental and Life Sciences, 50-375 Wroclaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4940-3615","authenticated-orcid":false,"given":"Ewelina","family":"W\u0119sierska","sequence":"additional","affiliation":[{"name":"Department of Animal Product Technology, University of Agriculture in Krakow, 30-239 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacek","family":"Bania","sequence":"additional","affiliation":[{"name":"Department of Food Hygiene and Consumer Health Protection, Wroclaw University of Environmental and Life Sciences, 50-375 Wroclaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,2,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1751","DOI":"10.3390\/toxins2071751","article-title":"Food Poisoning and Staphylococcus aureus Enterotoxins","volume":"2","author":"Mendoza","year":"2010","journal-title":"Toxins"},{"key":"ref_2","first-page":"92","article-title":"A Staphylococcal Food-Poisoning Caused by a Coagulase-Negative Strain","volume":"2","author":"Omori","year":"1959","journal-title":"Biken\u2019s J."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1056\/NEJM197103112841010","article-title":"Outbreak of Food-Borne Gastroenteritis Due to a Coagulase-Negative Enterotoxin-Producing Staphylococcus","volume":"284","author":"Breckinridge","year":"1971","journal-title":"N. Engl. J. Med."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1128\/jcm.23.1.43-45.1986","article-title":"Involvement of coagulase-negative staphylococci in toxic shock syndrome","volume":"23","author":"Crass","year":"1986","journal-title":"J. Clin. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"566","DOI":"10.1128\/aem.54.2.566-569.1988","article-title":"A quantitative study of enterotoxin production by sheep milk staphylococci","volume":"54","author":"Bautista","year":"1988","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1111\/j.1574-6968.1991.tb04163.x","article-title":"Detection of antibodies to staphylococcal enterotoxins in the serum and milk of healthy goats","volume":"76","author":"Valle","year":"1991","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"899","DOI":"10.1292\/jvms.65.899","article-title":"Concentrations and Specific Antibodies to Staphylococcal Enterotoxin-C and Toxic Shock Syndrome Toxin-1 in Bovine Mammary Gland Secretions, and Inflammatory Response to the Intramammary Inoculation of These Toxins","volume":"65","author":"Kuroishi","year":"2003","journal-title":"J. Vet. Med. Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1111\/j.1348-0421.2007.tb03925.x","article-title":"Detection of Enterotoxin and Toxic Shock Syndrome Toxin 1 Genes in Staphylococcus, with Emphasis on Coagulase-Negative Staphylococci","volume":"51","author":"Calsolari","year":"2007","journal-title":"Microbiol. Immunol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/j.vetmic.2010.06.021","article-title":"Detection of classical and newly described staphylococcal superantigen genes in coagulase-negative staphylococci isolated from bovine intramammary infections","volume":"147","author":"Park","year":"2011","journal-title":"Vet. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2866","DOI":"10.3168\/jds.2012-5864","article-title":"Enterotoxin genes in coagulase-negative and coagulase-positive staphylococci isolated from bovine milk","volume":"96","author":"Marson","year":"2013","journal-title":"J. Dairy Sci."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Mello, P.L., Riboli, D.F.M., Pinheiro, L., de Almeida Martins, L., Brito, M.A.V.P., and da Cunha, M.D.L.R.D.S. (2016). Detection of Enterotoxigenic Potential and Determination of Clonal Profile in Staphylococcus aureus and Coagulase-Negative Staphylococci Isolated from Bovine Subclinical Mastitis in Different Brazilian States. Toxins, 8.","DOI":"10.3390\/toxins8040104"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1089\/mdr.2019.0114","article-title":"Enterotoxigenicity and Antibiotic Resistance of Coagulase-Negative Staphylococci Isolated from Raw Buffalo and Cow Milk","volume":"26","author":"Osman","year":"2020","journal-title":"Microb. Drug Resist."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.ijfoodmicro.2016.04.013","article-title":"Genotype and enterotoxigenicity of Staphylococcus epidermidis isolate from ready to eat meat products","volume":"229","author":"Podkowik","year":"2016","journal-title":"Int. J. Food Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/S0147-619X(02)00157-9","article-title":"Mobile genetic elements and bacterial toxinoses: The superantigen-encoding pathogenicity islands of Staphylococcus aureus","volume":"49","author":"Novick","year":"2003","journal-title":"Plasmid"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"7520","DOI":"10.1128\/JB.00738-07","article-title":"Transducing Particles of Staphylococcus aureus Pathogenicity Island SaPI1 Are Comprised of Helper Phage-Encoded Proteins","volume":"189","author":"Tallent","year":"2007","journal-title":"J. Bacteriol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1111\/j.1365-2958.2007.06027.x","article-title":"SaPI mutations affecting replication and transfer and enabling autonomous replication in the absence of helper phage","volume":"67","author":"Maiques","year":"2008","journal-title":"Mol. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1126\/science.1164783","article-title":"Phage-Mediated Intergeneric Transfer of Toxin Genes","volume":"323","author":"Chen","year":"2009","journal-title":"Science"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1854","DOI":"10.1128\/JB.00162-10","article-title":"An Enterotoxin-Bearing Pathogenicity Island in Staphylococcus epidermidis","volume":"193","author":"Madhusoodanan","year":"2011","journal-title":"J. Bacteriol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"e00098-18","DOI":"10.1128\/mSystems.00098-18","article-title":"Comprehensive Virulence Gene Profiling of Bovine Non-aureus Staphylococci Based on Whole-Genome Sequencing Data","volume":"4","author":"Naushad","year":"2019","journal-title":"mSystems"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"108371","DOI":"10.1016\/j.lwt.2019.108371","article-title":"Technological and safety characterization of coagulase-negative staphylococci with high protease activity isolated from Traditional Chinese fermented sausages","volume":"114","author":"Sun","year":"2019","journal-title":"LWT"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3498","DOI":"10.1093\/gbe\/evz259","article-title":"Genetic Diversity of Composite Enterotoxigenic Staphylococcus epidermidis Pathogenicity Islands","volume":"11","author":"Banaszkiewicz","year":"2019","journal-title":"Genome Biol. Evol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Argemi, X., Nanoukon, C., Affolabi, D., Keller, D., Hansmann, Y., Riegel, P., Baba-Moussa, L., and Pr\u00e9vost, G. (2018). Comparative Genomics and Identification of an Enterotoxin-Bearing Pathogenicity Island, SEPI-1\/SECI-1, in Staphylococcus epidermidis Pathogenic Strains. Toxins, 10.","DOI":"10.3390\/toxins10030093"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Jolley, K.A., and Maiden, M.C. (2010). BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinform., 11.","DOI":"10.1186\/1471-2105-11-595"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1323","DOI":"10.1128\/aem.56.5.1323-1326.1990","article-title":"Enterotoxin production by staphylococci isolated from healthy goats","volume":"56","author":"Valle","year":"1990","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1016\/j.ijfoodmicro.2008.07.016","article-title":"Characterization of toxin production of coagulase-negative staphylococci isolated from food and starter cultures","volume":"127","author":"Zell","year":"2008","journal-title":"Int. J. Food Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1590\/S0074-02762006000600014","article-title":"Study of virulence factors in coagulase-negative staphylococci isolated from newborns","volume":"101","year":"2006","journal-title":"Mem\u00f3rias Inst. Oswaldo Cruz"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1121","DOI":"10.1089\/fpd.2009.0478","article-title":"Polymerase Chain Reaction Detection of Enterotoxins Genes in Coagulase-Negative Staphylococci Isolated from Brazilian Minas Cheese","volume":"7","author":"Rall","year":"2010","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_28","first-page":"13","article-title":"Staphylococcal Superantigens: Do They Play a Role in Sepsis?","volume":"53","author":"Holtfreter","year":"2005","journal-title":"Arch. Immunol. Ther. Exp."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1186\/s44149-021-00007-7","article-title":"Update on molecular diversity and multipathogenicity of staphylococcal superantigen toxins","volume":"1","author":"Hu","year":"2021","journal-title":"Anim. Dis."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Argemi, X., Hansmann, Y., Prola, K., and Pr\u00e9vost, G. (2019). Coagulase-Negative Staphylococci Pathogenomics. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20051215"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"126979","DOI":"10.1016\/j.micres.2022.126979","article-title":"Analysis of enterotoxigenic effect of Staphylococcus aureus and Staphylococcus epidermidis enterotoxins C and L on mice","volume":"258","author":"Gonet","year":"2022","journal-title":"Microbiol. Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"e45","DOI":"10.1093\/nar\/29.9.e45","article-title":"A new mathematical model for relative quantification in real-time RT-PCR","volume":"29","author":"Pfaffl","year":"2001","journal-title":"Nucleic Acids Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2697","DOI":"10.1093\/gbe\/evu214","article-title":"Extensive Horizontal Gene Transfer during Staphylococcus aureus Co-colonization In Vivo","volume":"6","author":"McCarthy","year":"2014","journal-title":"Genome Biol. Evol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.ijfoodmicro.2016.06.043","article-title":"Production of staphylococcal enterotoxins in microbial broth and milk by Staphylococcus aureus strains harboring seh gene","volume":"235","author":"Schubert","year":"2016","journal-title":"Int. J. Food Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"238","DOI":"10.4315\/0362-028X.JFP-11-336","article-title":"Temporal Expression of Staphylococcal Enterotoxin H in Comparison with Accessory Gene Regulator\u2013Dependent and \u2013Independent Enterotoxins","volume":"75","author":"Lis","year":"2012","journal-title":"J. Food Prot."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3627","DOI":"10.1128\/IAI.00550-13","article-title":"Emetic Potentials of Newly Identified Staphylococcal Enterotoxin-Like Toxins","volume":"81","author":"Omoe","year":"2013","journal-title":"Infect. Immun."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"10","DOI":"10.14806\/ej.17.1.200","article-title":"Cutadapt removes adapter sequences from high-throughput sequencing reads","volume":"17","author":"Martin","year":"2011","journal-title":"EMBnet. J."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1089\/cmb.2012.0021","article-title":"SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing","volume":"19","author":"Bankevich","year":"2012","journal-title":"J. Comput. Biol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/5\/2560\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:27:40Z","timestamp":1760135260000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/5\/2560"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,2,25]]},"references-count":38,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2022,3]]}},"alternative-id":["ijms23052560"],"URL":"https:\/\/doi.org\/10.3390\/ijms23052560","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,2,25]]}}}