Microbial Succession in the Cheese Ripening Process-Competition of the Starter Cultures and the Microbiota of the Cheese Plant Environment
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
QK1910121
Ministry of Agriculture
RVO0523
Instituonal support
PubMed
37512907
PubMed Central
PMC10385115
DOI
10.3390/microorganisms11071735
PII: microorganisms11071735
Knihovny.cz E-zdroje
- Klíčová slova
- 16S rRNA gene sequencing, cheese microbiota, smear-ripened cheese, starter cultures,
- Publikační typ
- časopisecké články MeSH
A large variety of cheeses can be produced using different manufacturing processes and various starter or adjunct cultures. In this study, we have described the succession of the microbial population during the commercial production and subsequent ripening of smear-ripened cheese using 16S rRNA gene sequencing. The composition of the microbiota during the first 6 days of production was constant and consisted mainly of LAB (lactic acid bacteria) originating from the starter culture. From day 7, the proportion of LAB decreased as other bacteria from the production environment appeared. From the 14th day of production, the relative proportion of LAB decreased further, and at the end of ripening, bacteria from the environment wholly dominated. These adventitious microbiota included Psychrobacter, Pseudoalteromonas haloplanktis/hodoensis, Vibrio toranzoniae, and Vibrio litoralis (Proteobacteria phylum), as well as Vagococcus and Marinilactibacillus (Firmicutes phylum), Psychrilyobacter (Fusobacteria phylum), and Malaciobacter marinus (Campylobacterota phylum), all of which appeared to be characteristic taxa associated with the cheese rind. Subsequent analysis showed that the production and ripening of smear-ripened cheese could be divided into three stages, and that the microbiota compositions of samples from the first week of production, the second week of production, and supermarket shelf life all differed.
Zobrazit více v PubMed
Choi J., In Lee S., Rackerby B., Frojen R., Goddik L., Ha S.D., Park S.H. Assessment of Overall Microbial Community Shift during Cheddar Cheese Production from Raw Milk to Aging. Appl. Microbiol. Biotechnol. 2020;104:6249–6260. doi: 10.1007/s00253-020-10651-7. PubMed DOI
Juricova H., Matiasovicova J., Faldynova M., Sebkova A., Kubasova T., Prikrylova H., Karasova D., Crhanova M., Havlickova H., Rychlik I. Probiotic Lactobacilli Do Not Protect Chickens against Salmonella Enteritidis Infection by Competitive Exclusion in the Intestinal Tract but in Feed, Outside the Chicken Host. Microorganisms. 2022;10:219. doi: 10.3390/microorganisms10020219. PubMed DOI PMC
Monnet C., Dugat-Bony E., Swennen D., Beckerich J.M., Irlinger F., Fraud S., Bonnarme P. Investigation of the Activity of the Microorganisms in a Reblochon-Style Cheese by Metatranscriptomic Analysis. Front. Microbiol. 2016;7:536. doi: 10.3389/fmicb.2016.00536. PubMed DOI PMC
Ritschard J.S., Amato L., Kumar Y., Müller B., Meile L., Schuppler M. The Role of the Surface Smear Microbiome in the Development of Defective Smear on Surface-Ripened Red-Smear Cheese. AIMS Microbiol. 2018;4:622–641. doi: 10.3934/microbiol.2018.4.622. PubMed DOI PMC
Dugat-Bony E., Straub C., Teissandier A., Onésime D., Loux V., Monnet C., Irlinger F., Landaud S., Leclercq-Perlat M.N., Bento P., et al. Overview of a Surface-Ripened Cheese Community Functioning by Meta-Omics Analyses. PLoS ONE. 2015;10:e0124360. doi: 10.1371/journal.pone.0124360. PubMed DOI PMC
Irlinger F., Layec S., Hélinck S., Dugat-Bony E. Cheese Rind Microbial Communities: Diversity, Composition and Origin. FEMS Microbiol. Lett. 2015;362:1–11. doi: 10.1093/femsle/fnu015. PubMed DOI
Marino M., Innocente N., Maifreni M., Mounier J., Cobo-Díaz J.F., Coton E., Carraro L., Cardazzo B. Diversity within Italian Cheesemaking Brine-Associated Bacterial Communities Evidenced by Massive Parallel 16S rRNA Gene Tag Sequencing. Front. Microbiol. 2017;8:2119. doi: 10.3389/fmicb.2017.02119. PubMed DOI PMC
Haastrup M.K., Johansen P., Malskær A.H., Castro-Mejía J.L., Kot W., Krych L., Arneborg N., Jespersen L. Cheese Brines from Danish Dairies Reveal a Complex Microbiota Comprising Several Halotolerant Bacteria and Yeasts. Int. J. Food Microbiol. 2018;285:173–187. doi: 10.1016/j.ijfoodmicro.2018.08.015. PubMed DOI
Vermote L., Verce M., De Vuyst L., Weckx S. Amplicon and Shotgun Metagenomic Sequencing Indicates That Microbial Ecosystems Present in Cheese Brines Reflect Environmental Inoculation during the Cheese Production Process. Int. Dairy J. 2018;87:44–53. doi: 10.1016/j.idairyj.2018.07.010. DOI
Unno R., Suzuki T., Matsutani M., Ishikawa M. Evaluation of the Relationships Between Microbiota and Metabolites in Soft-Type Ripened Cheese Using an Integrated Omics Approach. Front. Microbiol. 2021;12:681185. doi: 10.3389/fmicb.2021.681185. PubMed DOI PMC
Bertuzzi A.S., Walsh A.M., Sheehan J.J., Cotter P.D., Crispie F., Mcsweeney P.L.H., Kilcawley K.N., Rea M.C. Omics-Based Insights into Flavor Development and Microbial Succession within Surface-Ripened Cheese. mSystems. 2018;3:e00211-17. doi: 10.1128/mSystems.00211-17. PubMed DOI PMC
Jin H., Mo L., Pan L., Hou Q., Li C., Darima I., Yu J. Using PacBio sequencing to investigate the bacterial microbiota of traditional Buryatian cottage cheese and comparison with Italian and Kazakhstan artisanal cheeses. J. Dairy Sci. 2018;101:6885–6896. doi: 10.3168/jds.2018-14403. PubMed DOI
Méndez-Romero J.I., Reyes-Díaz R., Santiago-López L., Hernández-Mendoza A., Vallejo-Cordoba B., Sayago-Ayerdi S.G., Gómez-Gil B., González-Córdova A.F. Artisanal Fresco cheese from Sonora: Physicochemical composition, microbial quality, and bacterial characterization by high-throughput sequencing. Int. J. Dairy Technol. 2021;74:359–370. doi: 10.1111/1471-0307.12751. DOI
Mureşan C.C., Marc R.A., Anamaria Semeniuc C., Ancuţa Socaci S., Fărcaş A., Fracisc D., Rodica Pop C., Rotar A., Dodan A., Mureşan V., et al. Changes in Physicochemical and Microbiological Properties, Fatty Acid and Volatile Compound Profiles of Apuseni Cheese during Ripening. Foods. 2021;10:258. doi: 10.3390/foods10020258. PubMed DOI PMC
Karasova D., Crhanova M., Babak V., Jerabek M., Brzobohaty L., Matesova Z., Rychlik I. Development of Piglet Gut Microbiota at the Time of Weaning Influences Development of Postweaning Diarrhea—A Field Study. Res. Vet. Sci. 2021;135:59–65. doi: 10.1016/j.rvsc.2020.12.022. PubMed DOI
Segata N., Izard J., Waldron L., Gevers D., Miropolsky L., Garrett W.S., Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60. doi: 10.1186/gb-2011-12-6-r60. PubMed DOI PMC
Salazar J.K., Carstens C.K., Ramachandran 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. doi: 10.1186/s12866-018-1323-4. PubMed DOI PMC
Van Hoorde K., Heyndrickx M., Vandamme P., Huys G. Influence of Pasteurization, Brining Conditions and Production Environment on the Microbiota of Artisan Gouda-Type Cheeses. Food Microbiol. 2010;27:425–433. doi: 10.1016/j.fm.2009.12.001. PubMed DOI
Ogier J.C., Lafarge V., Girard V., Rault A., Maladen V., Gruss A., Leveau J.Y., Delacroix-Buchet A. Molecular Fingerprinting of Dairy Microbial Ecosystems by Use of Temporal Temperature and Denaturing Gradient Gel Electrophoresis. Appl. Environ. Microbiol. 2004;70:5628–5643. doi: 10.1128/AEM.70.9.5628-5643.2004. PubMed DOI PMC
Settanni L., Moschetti G. Non-Starter Lactic Acid Bacteria Used to Improve Cheese Quality and Provide Health Benefits. Food Microbiol. 2010;27:691–697. doi: 10.1016/j.fm.2010.05.023. PubMed DOI
Irlinger F., In Yung S.A.Y., Sarthou A.S., Delbès-Paus C., Montel M.C., Coton E., Coton M., Helinck S. Ecological and Aromatic Impact of Two Gram-Negative Bacteria (Psychrobacter Celer and Hafnia Alvei) Inoculated as Part of the Whole Microbial Community of an Experimental Smear Soft Cheese. Int. J. Food Microbiol. 2012;153:332–338. doi: 10.1016/j.ijfoodmicro.2011.11.022. PubMed DOI
Fontana C., Cappa F., Rebecchi A., Cocconcelli P.S. Surface Microbiota Analysis of Taleggio, Gorgonzola, Casera, Scimudin and Formaggio Di Fossa Italian Cheeses. Int. J. Food Microbiol. 2010;138:205–211. doi: 10.1016/j.ijfoodmicro.2010.01.017. PubMed DOI
Chaves-López C., De Angelis M., Martuscelli M., Serio A., Paparella A., Suzzi G. Characterization of the Enterobacteriaceae Isolated from an Artisanal Italian Ewe’s Cheese (Pecorino Abruzzese) J. Appl. Microbiol. 2006;101:353–360. doi: 10.1111/j.1365-2672.2006.02941.x. PubMed DOI
Morales P., Fernández-García E., Nuñez M. Caseinolysis in Cheese by Enterobacteriaceae Strains of Dairy Origin. Lett. Appl. Microbiol. 2003;37:410–414. doi: 10.1046/j.1472-765X.2003.01422.x. PubMed DOI
Wolfe B.E., Button J.E., Santarelli M., Dutton R.J. Cheese rind communities provide tractable systems for in situ and in vitro studies of microbial diversity. Cell. 2014;158:422–433. doi: 10.1016/j.cell.2014.05.041. PubMed DOI PMC
Yesilmen S., Vural A., Erkan M.E., Yildirim I.H. Prevalence and antimicrobial susceptibility of Arcobacter species in cow milk, water buffalo milk and fresh village cheese. Int. J. Food Microbiol. 2014;188:11–14. doi: 10.1016/j.ijfoodmicro.2014.07.006. PubMed DOI
Scarano C., Giacometti F., Manfreda G., Lucchi A., Pes E., Spanu C., De Santis E.P., Serraino A. Arcobacter butzleri in sheep ricotta cheese at retail and related sources of contamination in an industrial dairy plant. Appl. Environ. Microbiol. 2014;80:7036–7041. doi: 10.1128/AEM.02491-14. PubMed DOI PMC
Serraino A., Giacometti F. Short communication: Occurrence of Arcobacter species in industrial dairy plants. J. Dairy Sci. 2014;97:2061–2065. doi: 10.3168/jds.2013-7682. PubMed DOI
Kothe C.I., Bolotin A., Kraïem B.F., Dridi B., Renault P. Unraveling the World of Halophilic and Halotolerant Bacteria in Cheese by Combining Cultural, Genomic and Metagenomic Approaches. Int. J. Food Microbiol. 2021:358. doi: 10.1016/j.ijfoodmicro.2021.109312. PubMed DOI
Giacometti F., Losio M.N., Daminelli P., Cosciani-Cunico E., Dalzini E., Serraino A. Short Communication: Arcobacter Butzleri and Arcobacter Cryaerophilus Survival and Growth in Artisanal and Industrial Ricotta Cheese. J. Dairy Sci. 2015;98:6776–6781. doi: 10.3168/jds.2015-9560. PubMed DOI
Cruzado-Bravo M.L.M., Barancelli G.V., Dini Andreote A.P., Saldaña E., Vidal-Veuthey B., Collado L., Contreras-Castillo C.J. Occurrence of Arcobacter Spp. in Brazilian Minas Frescal Cheese and Raw Cow Milk and Its Association with Microbiological and Physicochemical Parameters. Food Control. 2020;109:106904. doi: 10.1016/j.foodcont.2019.106904. DOI
Liu M., Wei G., Lai Q., Huang Z., Li M. The First Host-Associated Anaerobic Isolate of Psychrilyobacter Provides Insights into Its Potential Roles in the Abalone Gut. bioRxiv. 2022 doi: 10.1101/2022.11.24.517839. DOI
Yang Z., Liu S., Lv J., Sun Z., Xu W., Ji C., Liang H., Li S., Yu C., Lin X. Microbial Succession and the Changes of Flavor and Aroma in Chouguiyu, a Traditional Chinese Fermented Fish. Food Biosci. 2020;37:100725. doi: 10.1016/j.fbio.2020.100725. DOI
Schön K., Schornsteiner E., Dzieciol M., Wagner M., Müller M., Schmitz-Esser S. Microbial Communities in Dairy Processing Environment Floor-Drains Are Dominated by Product-Associated Bacteria and Yeasts. Food Control. 2016;70:210–215. doi: 10.1016/j.foodcont.2016.05.057. DOI
Montel M.C., Buchin S., Mallet A., Delbes-Paus C., Vuitton D.A., Desmasures N., Berthier F. Traditional Cheeses: Rich and Diverse Microbiota with Associated Benefits. Int. J. Food Microbiol. 2014;177:136–154. doi: 10.1016/j.ijfoodmicro.2014.02.019. PubMed DOI