Diversity and Safety Aspects of Coagulase-Negative Staphylococci in Ventricina del Vastese Italian Dry Fermented Sausage
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bacterial Strains and Culture Conditions
2.2. DNA Isolation
2.3. PCR Assays
2.4. Sequencing
2.5. Data Analyses
3. Results and Discussion
3.1. CNS Microbiota Composition
3.2. Safety Assessment of Ventricina Del Vastese CNS
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Palavecino Prpich, N.Z.; Camprubí, G.E.; Cayré, M.E.; Castro, M.P. Indigenous Microbiota to Leverage Traditional Dry Sausage Production. Int. J. Food Sci. 2021, 2021, 6696856. [Google Scholar] [CrossRef] [PubMed]
- Italian Ministry of Agriculture. Ventiduesima Revisione Dell’elenco Dei Prodotti Agroalimentari Tradizionali. Available online: https://www.politicheagricole.it/flex/cm/pages/ServeBLOB.php/L/IT/IDPagina/17979 (accessed on 22 October 2022).
- Fondazione Slow Food per la Biodiversità Onlus. Ventricina del Vastese Presidio Slow Food. Available online: https://www.fondazioneslowfood.com/it/presidi-slow-food/ventricina-del-vastese/ (accessed on 22 October 2022).
- Amadoro, C.; Rossi, F.; Piccirilli, M.; Berardino, L.; Colavita, G. Studio della flora microbica pro-tecnologica nella ventricina. Ing. Aliment. 2013, 50, 51–54. [Google Scholar]
- Nováková, D.; Sedláček, I.; Pantůček, R.; Štětina, V.; Švec, P.; Petráš, P. Staphylococcus equorum and Staphylococcus succinus isolated from human clinical specimens. J. Med. Microbiol. 2006, 55, 523–528. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van Ba, H.; Seo, H.W.; Kim, J.H.; Cho, S.H.; Kim, Y.S.; Ham, J.S.; Park, B.Y.; Kim, H.W.; Kim, T.B.; Seong, P.N. The effects of starter culture types on the technological quality, lipid oxidation and biogenic amines in fermented sausages. LWT 2016, 74, 191–198. [Google Scholar] [CrossRef]
- Marty, E.; Bodenmann, C.; Buchs, J.; Hadorn, R.; Eugster-Meier, E.; Lacroix, C.; Meile, L. Prevalence of antibiotic resistance in coagulase-negative staphylococci from spontaneously fermented meat products and safety assessment for new starters. Int. J. Food Microbiol. 2012, 159, 74–83. [Google Scholar] [CrossRef] [PubMed]
- Rebecchi, A.; Miragoli, F.; Lopez, C.; Bassi, D.; Fontana, C. Exploring Coagulase-Negative Staphylococci Diversity from Artisanal Llama Sausages: Assessment of Technological and Safety Traits. Microorganisms 2020, 8, 629. [Google Scholar] [CrossRef] [PubMed]
- EFSA BIOHAZ Panel. Updated List of QPS-Recommended Biological Agents for Safety Risk Assessments Carried Out by EFSA. Available online: https://zenodo.org/record/6902983#.Y3i0VX3MLIV (accessed on 22 October 2022).
- Zell, C.; Resch, M.; Rosenstein, R.; Albrecht, T.; Hertel, C.; Götz, F. Characterization of toxin production of coagulase-negative staphylococci isolated from food and starter cultures. Int. J. Food Microbiol. 2008, 127, 246–251. [Google Scholar] [CrossRef]
- Versalovic, J.; Schneider, M.; De Bruijn, F.J.; Lupski, J.R. Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol. Cell. Biol. 1994, 5, 25–40. [Google Scholar]
- Fredriksson, N.J.; Hermansson, M.; Wilén, B.M. The choice of PCR primers has great impact on assessments of bacterial community diversity and dynamics in a wastewater treatment plant. PLoS ONE 2013, 8, e76431. [Google Scholar] [CrossRef]
- La Gioia, F.; Rizzotti, L.; Rossi, F.; Gardini, F.; Tabanelli, G.; Torriani, S. Identification of a tyrosine decarboxylase gene (tdcA) in Streptococcus thermophilus 1TT45 and analysis of its expression and tyramine production in milk. Appl. Environ. Microbiol. 2011, 77, 1140–1144. [Google Scholar] [CrossRef] [Green Version]
- Rossi, F.; Gardini, F.; Rizzotti, L.; La Gioia, F.; Tabanelli, G.; Torriani, S. Quantitative analysis of histidine decarboxylase gene (hdcA) transcription and histamine production by Streptococcus thermophilus PRI60 under conditions relevant to cheese making. Appl. Environ. Microbiol. 2011, 77, 2817–2822. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yu, Z.; Michel, F.C., Jr.; Hansen, G.; Wittum, T.; Morrison, M. Development and application of real-time PCR assays for quantification of genes encoding tetracycline resistance. Appl. Environ. Microbiol. 2005, 71, 6926–6933. [Google Scholar] [CrossRef] [PubMed]
- Omoe, K.; Hu, D.L.; Takahashi-Omoe, H.; Nakane, A.; Shinagawa, K. Comprehensive analysis of classical and newly described staphylococcal superantigenic toxin genes in Staphylococcus aureus isolates. FEMS Microbiol. Lett. 2005, 246, 191–198. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rossi, F.; Tofalo, R.; Torriani, S.; Suzzi, G. Identification by 16S-23S rDNA intergenic region amplification, genotypic and phenotypic clustering of Staphylococcus xylosus strains from dry sausages. J. Appl. Microbiol. 2001, 90, 365–371. [Google Scholar] [CrossRef] [PubMed]
- Mauriello, G.; Casaburi, A.; Blaiotta, G.; Villani, F. Isolation and technological properties of coagulase negative staphylococci from fermented sausages of Southern Italy. Meat Sci. 2004, 67, 149–158. [Google Scholar] [CrossRef]
- Ravyts, F.; Steen, L.; Goemaere, O.; Paelinck, H.; De Vuyst, L.; Leroy, F. The application of staphylococci with flavour-generating potential is affected by acidification in fermented dry sausages. Food Microbiol. 2010, 27, 945–954. [Google Scholar] [CrossRef]
- Heilmann, C.; Ziebuhr, W.; Becker, K. Are coagulase-negative staphylococci virulent? Clin. Microbiol. Infect. 2019, 25, 1071–1080. [Google Scholar] [CrossRef]
- Hur, J.; Lee, A.; Hong, J.; Jo, W.Y.; Cho, O.H.; Kim, S.; Bae, I.G. Staphylococcus saprophyticus Bacteremia originating from Urinary Tract Infections: A Case Report and Literature Review. Infect. Chemother. 2016, 48, 136–139. [Google Scholar] [CrossRef]
- Hong-Eun, N.; Sojeong, H.; Yoon-Su, K.; Tao, K.; Gawon, L.; Jong-Hoon, L.; Do-Won, J. The safety and technological properties of Bacillus velezensis DMB06 used as a starter candidate were evaluated by genome analysis. LWT 2022, 161, 113398. [Google Scholar]
- Milicevic, B.; Danilovic, B.; ZDolec, N.; Kozachinski, L.; Dobranic, V.; Savic, D. Microbiota of the fermented sausages: Influence to product quality and safety. Bulg. J. Agric. Sci. 2014, 20, 1061–1078. [Google Scholar]
- Van Reckem, E.; Charmpi, C.; Van der Veken, D.; Borremans, W.; De Vuyst, L.; Weckx, S.; Leroy, F. Application of a High-Throughput Amplicon Sequencing Method using a partial region of the tuf gene to Chart the Bacterial Communities that Are Associated with European Fermented Meats from Different Origins. Foods 2020, 9, 1247. [Google Scholar] [CrossRef] [PubMed]
- Jeong, D.W.; Lee, B.; Her, J.Y.; Lee, K.G.; Lee, J.H. Safety and technological characterization of coagulase-negative staphylococci isolates from traditional Korean fermented soybean foods for starter development. Int. J. Food Microbiol. 2016, 236, 9–16. [Google Scholar] [CrossRef] [PubMed]
- Corbière Morot-Bizot, S.; Leroy, S.; Talon, R. Staphylococcal community of a small unit manufacturing traditional dry fermented sausages. Int. J. Food Microbiol. 2006, 108, 210–217. [Google Scholar] [CrossRef] [PubMed]
- Jeong, D.W.; Lee, J.H. Complete Genome Sequence of Staphylococcus succinus 14BME20 Isolated from a Traditional Korean Fermented Soybean Food. Genome Announc. 2017, 5, e01731-16. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.; Rosazza, J.P.N. Purification and characterization of nitric oxide synthase (NOSnoc) from a Nocardia species. J. Bacteriol. 1995, 177, 5122–5128. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Place, R.B.; Hiestand, D.; Burri, S.; Teuber, M. Staphylococcus succinus subsp. casei subsp. nov., a dominant isolate from a surface ripened cheese. Syst. Appl. Microbiol. 2002, 25, 353–359. [Google Scholar]
- Jeong, D.W.; Lee, H.; Jeong, K.; Kim, C.T.; Shim, S.T.; Lee, J.H. Effects of starter candidates and NaCl on the production of volatile compounds during soybean fermentation. J. Microbiol. Biotechnol. 2019, 29, 191–199. [Google Scholar] [CrossRef]
- Guay, G.G.; Khan, S.A.; Rothstein, D.M. The tet(K) gene of plasmid pt181 of Staphylococcus aureus encodes an efflux protein that contains 14 transmembrane helices. Plasmid 1993, 30, 163–166. [Google Scholar] [CrossRef]
- Soares Casaes Nunes, R.; Mere Del Aguila, E.; Paschoalin, V.M. Safety Evaluation of the Coagulase-Negative Staphylococci Microbiota of Salami: Superantigenic Toxin Production and Antimicrobial Resistance. Biomed. Res. Int. 2015, 2015, 483548. [Google Scholar] [CrossRef] [Green Version]
- Fontana, C.; Patrone, V.; Lopez, C.M.; Morelli, L.; Rebecchi, A. Incidence of Tetracycline and Erythromycin Resistance in Meat-Associated Bacteria: Impact of Different Livestock Management Strategies. Microorganisms 2021, 9, 2111. [Google Scholar] [CrossRef]
- Dias, I.; Laranjo, M.; Potes, M.E.; Agulheiro-Santos, A.C.; Ricardo-Rodrigues, S.; Fialho, A.R.; Véstia, J.; Fraqueza, M.J.; Oliveira, M.; Elias, M. Co-Inoculation with Staphylococcus equorum and Lactobacillus sakei Reduces Vasoactive Biogenic Amines in Traditional Dry-Cured Sausages. Int. J. Environ. Res. Public Health 2021, 18, 7100. [Google Scholar] [CrossRef] [PubMed]
Manufacturer | A | B | C | D |
---|---|---|---|---|
Day 0 | A1, A3, A4, A5, A6, A7, A8 | B1, B2 | C1, C2, C3, C4, C5, C6, C7, C8 | D1, D2, D3, D4, D5, D6, D7 |
Day 20 | A9, A10, A11, A12, A14, A16, A17 | B4, B6, B8 | C9, C10, C11, C12, C13, C14, C15, C16, C17 | D8, D9, D10, D11, D12, D13, D14, D15, D16 |
Day 50 | A22, A23, A24, A26, A27, A28 | B10, B11 | C18, C19, C20, C21, C22, C23, C24 | D17, D18, D19, D20, D21, D22, D23 |
Day 150 | A29, A31, A32, A33, A34 | B12, B15 | C25, C26, C27, C28, C29, C30 | D24, D25, D26, D27, D28, D29, D30 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Amadoro, C.; Rossi, F.; Poltronieri, P.; Marino, L.; Colavita, G. Diversity and Safety Aspects of Coagulase-Negative Staphylococci in Ventricina del Vastese Italian Dry Fermented Sausage. Appl. Sci. 2022, 12, 13042. https://doi.org/10.3390/app122413042
Amadoro C, Rossi F, Poltronieri P, Marino L, Colavita G. Diversity and Safety Aspects of Coagulase-Negative Staphylococci in Ventricina del Vastese Italian Dry Fermented Sausage. Applied Sciences. 2022; 12(24):13042. https://doi.org/10.3390/app122413042
Chicago/Turabian StyleAmadoro, Carmela, Franca Rossi, Palmiro Poltronieri, Lucio Marino, and Giampaolo Colavita. 2022. "Diversity and Safety Aspects of Coagulase-Negative Staphylococci in Ventricina del Vastese Italian Dry Fermented Sausage" Applied Sciences 12, no. 24: 13042. https://doi.org/10.3390/app122413042
APA StyleAmadoro, C., Rossi, F., Poltronieri, P., Marino, L., & Colavita, G. (2022). Diversity and Safety Aspects of Coagulase-Negative Staphylococci in Ventricina del Vastese Italian Dry Fermented Sausage. Applied Sciences, 12(24), 13042. https://doi.org/10.3390/app122413042