Microbiome Associated with Slovak Traditional Ewe’s Milk Lump Cheese
Abstract
:1. Introduction
2. Materials and Methods
3. Results and Discussion
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Uhrín, V.; Lauková, A.; Jančová, A.; Plintovič, V. Mlieko a Mliečna Žľaza. Milk and Mammary Gland; Publ. No. 92; Faculty of Natural Sciences of the University Constantinus Philosophus: Nitra, Slovakia, 2002; pp. 5–167. ISBN 80-8050-511-X. (in Slovak) [Google Scholar]
- Lauková, A.; Focková, V.; Simonová, M.P. Enterococcus mundtii Isolated from Slovak Raw Goat Milk and Its Bacteriocinogenic Potential. Int. J. Environ. Res. Public Health 2020, 17, 9504. [Google Scholar] [CrossRef]
- Herian. Benefit of sheep milk products to human health. Milk Lett. Mlékařské Listy 2014, 143, 1–6. (In Slovak) [Google Scholar]
- Lauková, A.; Simonová, M.P.; Focková, V.; Kološta, M.; Tomáška, M.; Dvorožňáková, E. Susceptibility to Bacteriocins in Biofilm-Forming, Variable Staphylococci Isolated from Local Ewe`s Milk Lump Cheeses. Foods 2020, 9, 1335. [Google Scholar] [CrossRef] [PubMed]
- Vatačšinová, T.; Pipová, M.; Fraqueza, M.J.R.; Maľa, P.; Dudríková, E.; Drážovská, M.; Lauková, A. Short communication: Antimicrobial Potential of Lactobacillus plantarum Strains Isolated from Slovak Raw Sheep Milk Cheeses. J. Dairy Sci. 2020, 103, 6900–6903. [Google Scholar] [CrossRef] [PubMed]
- Supeková, S.; Honza, M.; Kačenová, D. Perception of Slovak Foodstuffs Designated by Protected Geographical Indication by Slovak Consumers. J. Food Nutr. Res. 2008, 47, 205–208. [Google Scholar]
- The Slovak Spectator. 2011. Available online: https://spectator.sme.sk (accessed on 6 August 2021).
- Fox, P.F.; McSweeney, P.L.H.; Cogan, T.M.; Guinee, T.P. Fundamentals of Cheese Science, 4th ed.; Springer: Boston, MA, USA, 2017; pp. 185–229. ISBN 978-0-8342-1260-2. [Google Scholar]
- Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A Flexible Trimmer for Illumina Sequence Data. Bioinformatics 2014, 30, 2114–2120. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aronesty, E. Ea-utils. “Command-Line Tools for Processing Biological Sequencing Data”. Available online: https://github.com/ExpressionAnalysis/ea-utils (accessed on 20 June 2020).
- Edgar, R.C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26, 2460–2461. [Google Scholar] [CrossRef] [Green Version]
- Caporaso, J.G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F.D.; Costello, E.K.; Fierer, N.; Peña, A.G.; Goodrich, J.K.; Gordon, J.I.; et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Meth. 2010, 7, 335–336. [Google Scholar] [CrossRef] [Green Version]
- Quast, C.; Pruesse, E.; Yilmaz, P.; Gerken, J.; Schweer, T.; Yarza, P.; Peplies, J.; Glockner, F.O. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucl. Acids Res. 2013, 41, D590–D596. [Google Scholar] [CrossRef]
- Endo, A.; Dicks, L.M.T. Lactic Acid Bacteria: Biodiversity and Taxonom; Holzapfel, W.H., Wood, B.J.B., Eds.; Wiley-Blackwell: Hoboken, NJ, USA, 2014; p. 632. ISBN 9781444333831. [Google Scholar]
- Bouton, Y.; Buchin, S.; Duboz, G.; Pochet, S.; Beuvier, E. Effect of mesophilic lactobacilli and enterococci adjunct cultures on the final characteristics of a microfiltered milk Swiss-type cheese. Food Microbiol. 2009, 26, 183–191. [Google Scholar] [CrossRef]
- Tofalo, R.; Schirone, M.; Fasoli, G.; Perpetuini, G.; Patrignani, F.; Manetta, A.C.; Lanciotti, R.; Corsetti, A.; Martino, G.; Suzzi, G. Influence of pig rennet on proteolysis, organic acids content and microbiota of Pecorino di Farindola, a traditional Italian ewe’s raw milk cheese. Food Chem. 2015, 175, 121–127. [Google Scholar] [CrossRef] [PubMed]
- Tofalo, R.; Perpetuini, G.; Battistelli, N.; Pepe, A.; Ianni, A.; Martino, G.; Suzzi, G. Accumulation ᵧ-Aminobutyric Acid and Biogenic Amines in a Traditional Raw Milk Ewe’s Cheese. Foods 2019, 8, 401. [Google Scholar] [CrossRef] [Green Version]
- Tsanasidou, C.; Asimakoula, S.; Sameli, N.; Fanitsios, C.; Vandera, E.; Bosnea, L.; Koukkou, A.-I.; Samelis, J. Safety Evaluation, Biogenic Amine Formation, and Enzymatic Activity Profiles of Autochthonous Enterocin-Producing Greek Cheese Isolates of the Enterococcus faecium/durans Group. Microorganisms 2021, 9, 777. [Google Scholar] [CrossRef]
- Franz, C.M.A.P.; Huch, M.; Abriouel, H.; Holzapfel, W.; Gálvez, A. Enterococci as probiotics and their implications in food safety. Int. J. Food Microbiol. 2011, 151, 125–140. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Issa, G.; Aksu, H. Detection of Methicillin-Resistant Staphylococcus aureus in Milk by PCR-Based Phenotyping and Genotyping. Acta Veterinaria Eurasia 2020, 46, 120–124. [Google Scholar] [CrossRef]
- Chase, A.B.; Arevalo, P.; Polz, M.F.; Berlemont, R.; Martiny, J.B.H. Evidence for Ecological Flexibility in the Cosmopolitan Genus Curtobacterium. Front. Microbiol. 2016, 7, 1874. [Google Scholar] [CrossRef]
- Quigley, L.; O’Sullivan, O.; Stanton, C.; Beresford, T.P.; Ross, R.P.; Fitzerald, G.F.; Cotter, P.D. The complex microbiota of raw milk. FEMS Microbiol. 2013, 37, 664–698. [Google Scholar] [CrossRef] [Green Version]
- Kazeminia, M.; Mahmoudi, R.; Ghajarbeygi, P.; Mousavi, S. The effect of seasonal variation on the chemical and microbial quality of raw milk samples used in Qazvin. Iran. J. Chem. Health Risk 2019, 9, 157–165. [Google Scholar]
- Kačániová, M.; Kunová, S.; Štefánikova, J.; Felšociová, S.; Godovčíková, L.; Horská, E.; Nagyová, Ľ.; Haščík, P.; Terentjeva, M. Microbiota of the traditional Slovak sheep cheese “Bryndza”. J. Microbiol. Biotechnol. Food Sci. 2019, 9, 482–486. [Google Scholar] [CrossRef]
- Šaková, N.; Sádecká, J.; Lejková, J.; Puškárová, A.; Koreňová, J.; Kolek, E.; Valík, Ľ.; Kuchta, T.; Pangallo, D. Characterization of May bryndza cheese from various regions in Slovakia based on microbial, molecular and principal volatile odorants examinations. J. Food Nutr. Sci. 2015, 54, 239–251. [Google Scholar]
- Salazar, J.K.; Carstens, C.K.; Ramachadran, P.; Shazer, A.G.; Narula, S.S.; Reed, E.; Ottesen, A.; Schill, K.M. Metagenomics of pasteurized and unpasteurized gouda cheese using targeted 16S rDNA sequencing. BMC Microbiol. 2018, 18, 189. [Google Scholar] [CrossRef] [PubMed]
- Gelsomino, R.; Vancanneyet, M.; Condon, S.; Swings, J.; Cogan, T.M. Enterococcal diversity in the environment of an Irish Cheddar-type cheesemaking factory. Int. J. Food Microbiol. 2001, 71, 177–188. [Google Scholar] [CrossRef]
- Lauková, A.; Kandričáková, A.; Bino, E.; Tomáška, M.; Kološta, M.; Kmeť, V.; Strompfová, V. Some safety aspects of enterococci isolated from Slovak lactic acid dairy product “žinčica”. Folia Microbiol. 2020, 65, 79–85. [Google Scholar] [CrossRef] [PubMed]
- Foulquié-Moreno, M.R.; Sarantinopoulos, P.; Tsakalidou, E.; De Vuyst, L. The role and application of enterococci in food and health. Int. J. Food Microbiol. 2006, 106, 1–24. [Google Scholar] [CrossRef] [PubMed]
- Planý, M.; Kuchta, T.; Šoltýs, K.; Szemes, T.; Pangallo, D.; Siekel, P. Metagenomics analysis of Slovak bryndza cheese using next-generation 16S rDNA amplicon sequencing. Nova Biotechnol. Chim. 2016, 15, 23–34. [Google Scholar] [CrossRef] [Green Version]
EMP16S-1 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGAGCCTTCGTCGCGTGTGYCAGCMGCCGCGGTAA | 16S Metagenomic sequencing Library Preparation protocol; Illumina, San Diego, CA, USA (EMP 515-806) |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGCCTAACGGTCCACCGGACTACNVGGGTWTCTAAT | ||
EMP16S-2 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGTCCATACCGGAAGTGTGYCAGCMGCCGCGGTAA | |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGCGCGCCTTAAACCCGGACTACNVGGGTWTCTAAT | ||
EMP16S-3 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGAGCCCTGCTACAGTGTGYCAGCMGCCGCGGTAA | |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGTATGGTACCCAGCCGGACTACNVGGGTWTCTAAT | ||
EMP16S-4 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGTGAGACCCTACAGTGTGYCAGCMGCCGCGGTAA | |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGGCCTCTACGTCGCCGGACTACNVGGGTWTCTAAT | ||
EMP16S-5 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGACTTGGTGTAAGGTGTGYCAGCMGCCGCGGTAA | |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGACTACTGAGGATCCGGACTACNVGGGTWTCTAAT | ||
EMP16S-6 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGATTACGTATCATGTGTGYCAGCMGCCGCGGTAA | |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGAATTCACCTCCTCCGGACTACNVGGGTWTCTAAT | ||
EMP16S-7 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGCACGCAGTCTACGTGTGYCAGCMGCCGCGGTAA | |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGCGTATAAATGCGCCGGACTACNVGGGTWTCTAAT | ||
EMP16S-8 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGTGTGCACGCCATGTGTGYCAGCMGCCGCGGTAA | |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGATGCTGCAACACCCGGACTACNVGGGTWTCTAAT | ||
EMP16S-9 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGCCGGACAAGAAGGTGTGYCAGCMGCCGCGGTAA | |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGACTCGCTCGCTGCCGGACTACNVGGGTWTCTAAT | ||
EMP16S-10 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGTTGCTGGACGCTGTGTGYCAGCMGCCGCGGTAA | |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGTTCCTTAGTAGTCCGGACTACNVGGGTWTCTAAT | ||
EMP16S-11 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGTACTAACGCGGTGTGTGYCAGCMGCCGCGGTAA | |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGCGTCCGTATGAACCGGACTACNVGGGTWTCTAAT | ||
EMP16S-12 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGGCGATCACACCTGTGTGYCAGCMGCCGCGGTAA | |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGACGTGAGGAACGCCGGACTACNVGGGTWTCTAAT | ||
EMP16S-13 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGCAAACGCACTAAGTGTGYCAGCMGCCGCGGTAA | |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGGGTTGCCCTGTACCGGACTACNVGGGTWTCTAAT | ||
EMP16S-14 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGGAAGAGGGTTGAGTGTGYCAGCMGCCGCGGTAA | |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGCATATAGCCCGACCGGACTACNVGGGTWTCTAAT | ||
EMP16S-15 | F | TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGTGAGTGGTCTGTGTGTGYCAGCMGCCGCGGTAA | |
R | GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGGCCTATGAGATCCCGGACTACNVGGGTWTCTAAT |
Phylum | |||
Firmicutes (60.92) | Proteobacteria (38.23) | Actinobacteria (0.38) | Bacteroidetes (0.35) |
Genera | |||
Streptococcus (41.13) | Pseudomonas (20.70) | Curtobacterium (0.7%) | Chryseobacterium (0.03) |
Lactococcus (8.54) | Acinetobacter (6.79) | Shingobacterium (0.03) | |
Fructobacillus (3.91) | Enterobacter (5.14) | Bacteroides (0.001) | |
Enterococcus (3.18) | Ewingella (1.3) | ||
Staphylococcus (1.80) | Escherichia-Shigella (0.55) | ||
Brochotrix (0.08) | Pantoea (0.46) | ||
Moraxella (0.31) |
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Lauková, A.; Micenková, L.; Pogány Simonová, M.; Focková, V.; Ščerbová, J.; Tomáška, M.; Dvorožňáková, E.; Kološta, M. Microbiome Associated with Slovak Traditional Ewe’s Milk Lump Cheese. Processes 2021, 9, 1603. https://doi.org/10.3390/pr9091603
Lauková A, Micenková L, Pogány Simonová M, Focková V, Ščerbová J, Tomáška M, Dvorožňáková E, Kološta M. Microbiome Associated with Slovak Traditional Ewe’s Milk Lump Cheese. Processes. 2021; 9(9):1603. https://doi.org/10.3390/pr9091603
Chicago/Turabian StyleLauková, Andrea, Lenka Micenková, Monika Pogány Simonová, Valentína Focková, Jana Ščerbová, Martin Tomáška, Emília Dvorožňáková, and Miroslav Kološta. 2021. "Microbiome Associated with Slovak Traditional Ewe’s Milk Lump Cheese" Processes 9, no. 9: 1603. https://doi.org/10.3390/pr9091603