[en] A previous study identified differences in rind aspects between Cantal-type cheeses manufactured from the same skimmed milk, supplemented with cream derived either from pasture-raised cows (P) or from cows fed with maize silage (M). Using an integrated analysis of multiomic data, the present study aimed at investigating potential correlations between cream origin and metagenomic, lipidomic and volatolomic profiles of these Cantal cheeses. Fungal and bacterial communities of cheese cores and rinds were characterized using DNA metabarcoding at different ripening times. Lipidome and volatolome were obtained from the previous study at the end of ripening. Rind microbial communities, especially fungal communities, were influenced by cream origin. Among bacteria, Brachybacterium were more abundant in P-derived cheeses than in M-derived cheeses after 90 and 150 days of ripening. Sporendonema casei, a yeast added as a ripening starter during Cantal manufacture, which contributes to rind typical aspect, had a lower relative abundance in P-derived cheeses after 150 days of ripening. Relative abundance of this fungus was highly negatively correlated with concentrations of C18 polyunsaturated fatty acids and to concentrations of particular volatile organic compounds, including 1-pentanol and 3-methyl-2-pentanol. Overall, these results evidenced original interactions between milk fat composition and the development of fungal communities in cheeses.
Disciplines :
Food science
Author, co-author :
Frétin, Marie; UMR 0545 Fromage, Université Clermont Auvergne, INRAE, VetAgro Sup, 20 Côte de Reyne, F-15000 Aurillac, France
Gérard, Amaury ; Université de Liège - ULiège ; UMR 0545 Fromage, Université Clermont Auvergne, INRAE, VetAgro Sup, 20 Côte de Reyne, F-15000 Aurillac, France
Ferlay, Anne; UMR 1213 Herbivores, Université Clermont Auvergne, INRAE, VetAgro Sup, 63122 Saint-Genès-Champanelle, France
Martin, Bruno; UMR 1213 Herbivores, Université Clermont Auvergne, INRAE, VetAgro Sup, 63122 Saint-Genès-Champanelle, France
Buchin, Solange; URTAL, INRAE, F-39800 Poligny, France
Theil, Sébastien ; UMR 0545 Fromage, Université Clermont Auvergne, INRAE, VetAgro Sup, 20 Côte de Reyne, F-15000 Aurillac, France
Rifa, Etienne; Toulouse Biotechnology Institute (TBI), Université de Toulouse, CNRS, INRAE, INSA, F-31077 Toulouse, France ; Plateforme Genome et Transcriptome (GeT), Genopole Toulouse, F-31077 Toulouse, France
Loux, Valentin; MIGALE Bioinformatics Facility, Université Paris-Saclay, INRAE, BioinfOmics, F-78350 Jouy-en-Josas, France ; MaIAGE, Université Paris-Saclay, INRAE, F-78350 Jouy-en-Josas, France
Acknowledgments: Amaury Gérard is the recipient of a fellowship from the Fonds pour la Formation à la Recherche dans l’Industrie et l’Agriculture (FRIA), Brussel, Belgium [grant number 21563]. The authors thank Carole Cirié and the staff of the INRA Herbipôle farm (Université Cler-mont Auvergne, INRAE, UE 1414 Herbipôle, F-63122 Saint-Genès-Champanelle, France) for animal care, and René Lavigne (UMR 0545 Fromage, Aurillac, France) for his valuable help in the cheesemaking experiments.Funding: Financial support for this study was provided by the Auvergne region and FEDER funds in the framework of a CPER T2ANSH 2013 project no. 2101 088 272 SyEL-inAuv (Systemes d’Elevage laitier innovants en Auvergne; France).
Gérard, A.; El-Hajjaji, S.; Burteau, S.; Fall, P.A.; Pirard, B.; Taminiau, B.; Daube, G.; Sindic, M. Study of the microbial diversity of a panel of Belgian artisanal cheeses associated with challenge studies for Listeria monocytogenes. Food Microbiol. 2021, 100, 103861.
Frétin, M.; Martin, B.; Rifa, E.; Verdier-Metz, I.; Pomiès, D.; Ferlay, A.; Montel, M.C.; Delbès, C. Bacterial community assembly form cow teat skin to ripened cheeses is influenced by grazing systems. Sci. Rep. 2018, 8, 200.
Irlinger, F.; Layec, S.; Hélinck, S.; Dugat-Bony, E. Cheese rind microbial communities: Diversity, composition and origin. FEMS Microbiol. Lett. 2015, 362, 1–11.
Frétin, M.; Martin, B.; Buchin, S.; Desserre, B.; Lavigne, R.; Tixier, E.; Cirié, C.; Bord, C.; Montel, M.-C.; Delbès, C.; et al. Milk fat composition modifies the texture and appearance of Cantal-type cheeses but not their flavor. J. Dairy Sci. 2019, 102, 1131–1143.
Callon, C.; Berdagué, J.L.; Dufour, E.; Montel, M.C. The effect of raw milk microbial flora on the sensory characteristics of Salerstype cheeses. J. Dairy Sci. 2015, 88, 3840–3850.
Ferlay, A.; Bernard, L.; Meynadier, A.; Malpuech-Brugère, C. Production of trans and conjugated fatty acids in dairy ruminants and their putative effects on human health: A review. Biochimie 2017, 141, 107–120.
Buchin, S.; Delague, V.; Duboz, G.; Berdague, J.; Beuvier, E.; Pochet, S.; Grappin, R. Influence of Pasteurization and Fat Composition of Milk on the Volatile Compounds and Flavor Characteristics of a Semi-hard Cheese. J. Dairy Sci. 1998, 81, 3097–3108.
Dugat-Bony, E.; Garnier, L.; Denonfoux, J.; Ferreira, S.; Sarthou, A.-S.; Bonnarme, P.; Irlinger, F. Highlighting the microbial diversity of 12 French cheese varieties. Int. J. Food Microbiol. 2016, 238, 265–273.
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.
Ceugniez, A.; Taminiau, B.; Coucheney, F.; Jacques, P.; Delcenserie, V.; Daube, G.; Drider, D. Fungal diversity of “Tomme d’Orchies” cheese during the ripening process as revealed by a metagenomic study. Int. J. Food Microbiol. 2017, 258, 89–93.
Schornsteiner, E.; Mann, E.; Bereuter, O.; Wagner, M.; Schmitz-Esser, S. Cultivation-independent analysis of microbial communities on Austrian raw milk hard cheese rinds. Int. J. Food Microbiol. 2014, 180, 88–97.
Frétin, M.; Ferlay, A.; Verdier-Metz, I.; Fournier, F.; Montel, M.-C.; Farruggia, A.; Delbès, C.; Martin, B. The effects of low-input grazing systems and milk pasteurisation on the chemical composition, microbial communities, and sensory properties of uncooked pressed cheeses. Int. Dairy J. 2017, 64, 56–67.
Meola, M.; Rifa, E.; Shani, N.; Delbès, C.; Berthoud, H.; Chassard, C. DAIRYdb: A manually curated reference database for improved taxonomy annotation of 16S rRNA gene sequences from dairy products. BMC Genom. 2019, 20, 560.
Nilsson, R.H.; Larsson, K.-H.; Taylor, A.F.S.; Bengtsson-Palme, J.; Jeppesen, T.S.; Schigel, D.; Kennedy, P.; Picard, K.; Glöckner, F.O.; Tedersoo, L.; et al. The UNITE database for molecular identification of fungi: Handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res. 2019, 47, D259–D264.
Lerch, S.; Ferlay, A.; Graulet, B.; Cirié, C.; Verdiez-Metz, I.; Montel, M.C.; Chilliard, Y.; Martin, B. Extruded linseeds, vitamin E and plant extracts in corn silage-based diest of dairy cows: Effects on sensory properties of raw milk and uncooked pressed cheese. Int. Dairy J. 2015, 51, 65–74.
Di Cagno, R.; De Pasquale, I.; De Angelis, M.; Buchin, S.; Rizzello, C.G.; Gobbetti, M. Use of microparticulated whey protein concentrate, exopolysaccharide-producing Streptococcus thermophilus, and adjunct cultures for making low-fat Italian Caciottatype cheese. J. Dairy Sci. 2014, 97, 7284.
Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 550.
Paulson, J.N.; Stine, O.C.; Bravo, H.C.; Pop, M. Differential abundance analysis for microbial marker-gene surveys. Nat. Methods 2013, 10, 1200–1202.
Foster, Z.S.L.; Sharpton, T.J.; Grünwald, N.J. Metacoder: An R package for visualization and manipulation of community taxonomic diversity data. PLoS Comput. Biol. 2017, 13, e1005404.
Galili, T.; O’Callaghan, A.; Sidi, J.; Sievert, C. heatmaply: An R package for creating interactive cluster heatmaps for online publishing. Bioinformatics 2018, 34, 1600–1602.
Chilliard, Y.; Flasser, F.; Ferlay, A.; Bernard, L.; Rouel, J.; Doreau, M. Diet, rumen biohydrogenation and nutritional quality of cow and goat milk fat: A review. Eur. J. Lipid. Sci. Technol. 2007, 109, 828–855.
Jonnala, B.R.Y.; McSweeney, P.L.; Cotter, P.D.; Zhong, S.; Sheehan, J.J.; Kopec, R.E. Comparison of the carotenoid profiles of commonly consumed smear-ripened cheeses. LWT 2020, 135, 110241.
Gori, K.; Ryssel, M.; Arneborg, N.; Jespersen, L. Isolation and indentification of the microbiota of Danish farmhouse and industrially produced surface-ripened cheeses. Microb. Ecol. 2013, 65, 602–615.
Johnson, M.; Zaretskaya, I.; Raytselis, Y.; Merezhuk, Y.; McGinnis, S.; Madden, T.L. NCBI BLAST: A better web interface. Nucleic Acids Res. 2008, 36, W5–W9.
Morin-Sardin, S.; Jany, J.L.; Artigaud, S.; Pichereau, V.; Bernay, B.; Coton, E.; Madec, S. Proeomic analysis of the adaptative response of Mucor spp. to cheese environment. J. Proteom. 2017, 154, 30–39.
Turri, F.; Cremonesi, P.; Battelli, G.; Severgnini, M.; Brasca, M.; Gandini, G.; Pizzi, F. High biodiversity in a limited mountain area revealed in the traditional production of Historic Rebel cheese by an integrated microbiota–lipidomic approach. Sci. Rep. 2021, 11, 1374.
Penland, M.; Falentin, H.; Parayre, S.; Pawtowski, A.; Maillard, M.-B.; Thierry, A.; Mounier, J.; Coton, M.; Deutsch, S.-M. Linking Pélardon artisanal goat cheese microbial communities to aroma compounds during cheese-making and ripening. Int. J. Food Microbiol. 2021, 345, 109130.