Fungal diversity of “Tomme d'Orchies” cheese during the ripening process as revealed by a metagenomic study

Artisanal cheese; Fungal microbiota; Illumina; Cladosporium cladosporioides; Clavispora lusitaniae; Debaryomyces; Geotrichum candidum; Kazachstania unispora; Kluyveromyces; Yarrowia lipolytica; DNA sequence; France; Cheese; DNA, Ribosomal; Fungi; Genome, Fungal; High-Throughput Nucleotide Sequencing; Metagenomics; Sequence Analysis, DNA

Abstract :

[en] Tomme d'Orchies is an artisanal pressed and uncooked cheese produced and marketed in the north of France. This study aimed at showing the fungal microbiota evolution of this cheese using a metagenetic based Illumina technology targeting the ITS2 domain of 5.8S fungal rDNAs. To this end, samples were taken from the rind and the core of different cheeses, after 0, 1, 3, 7, 14 and 21 days of ripening. The data underpinned the prevalence of Yarrowia lipolytica and Galactomyces geotrichum for both microbiotas. Unusual species including Clavispora lusitaniae, Kazachstania unispora and Cladosporium cladosporioides were also detected, but their origins remain to be ascertained. The metagenomic revealed also the presence of Kluyveromyces and Debaryomyces species. © 2017 Elsevier B.V.

Disciplines :

Microbiology

Author, co-author :

Ceugniez, A.; Univ. Lille, INRA, Univ. Artois, Univ. Littoral Côte d'Opale, EA 7394 – ICV - Institut Charles Viollette, Lille, France

Taminiau, Bernard ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires

Coucheney, F.; Univ. Lille, INRA, Univ. Artois, Univ. Littoral Côte d'Opale, EA 7394 – ICV - Institut Charles Viollette, Lille, France

Jacques, Philippe ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Microbial, food and biobased technologies

Delcenserie, Véronique ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Gestion de la qualité dans la chaîne alimentaire

Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires

Drider, D.; Univ. Lille, INRA, Univ. Artois, Univ. Littoral Côte d'Opale, EA 7394 – ICV - Institut Charles Viollette, Lille, France

Title :

Fungal diversity of “Tomme d'Orchies” cheese during the ripening process as revealed by a metagenomic study

Publication date :

2017

Journal title :

International Journal of Food Microbiology

ISSN :

0168-1605

eISSN :

1879-3460

Publisher :

Elsevier B.V.

Volume :

258

Pages :

89-93

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 13 August 2019

Statistics

Number of views

119 (2 by ULiège)

Number of downloads

378 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Atanassova, M.R., Fernández-Otero, C., Rodríguez-Alonso, P., Fernández-No, I.C., Garabal, J.I., Centeno, J.A., Characterization of yeasts isolated from artisanal short-ripened cows' cheeses produced in Galicia (NW Spain). Food Microbiol. 53 (2016), 172–181, 10.1016/j.fm.2015.09.012.
Banjara, N., Suhr, M.J., Hallen-Adams, H.E., Diversity of yeast and mold species from a variety of cheese types. Curr. Microbiol. 70 (2015), 792–800, 10.1007/s00284-015-0790-1.
Beresford, T.P., Fitzsimons, N.A., Brennan, N.L., Cogan, T.M., Recent advances in cheese microbiology. Int. Dairy J. 11 (2001), 259–274, 10.1016/S0958-6946(01)00056-5.
Bokulich, N.A., Mills, D.A., Next-generation approaches to the microbial ecology of food fermentations. BMB Rep. 45 (2012), 377–389, 10.5483/BMBRep.2012.45.7.148.
Boutrou, R., Kerriou, L., Gassi, J.-Y., Contribution of Geotrichum candidum to the proteolysis of soft cheese. Int. Dairy J. 16 (2006), 775–783.
Ceugniez, A., Drider, D., Jacques, P., Coucheney, F., Yeast diversity in a traditional French cheese “Tomme d'Orchies” reveals infrequent and frequent species with associated benefits. Food Microbiol. 52 (2015), 177–184, 10.1016/j.fm.2015.08.001.
Ceugniez, A., Taminiau, B., Coucheney, F., Jacques, P., Delcenserie, V., Daube, G., Drider, D., Use of a metagenetic approach to monitor the bacterial microbiota of “Tomme d'Orchies” cheese during the ripening process. Int. J. Food Microbiol., 2016, 10.1016/j.ijfoodmicro.2016.10.034.
Cocolin, L., Aggio, D., Manzano, M., Cantoni, C., Comi, G., An application of PCR-DGGE analysis to profile the yeast populations in raw milk. Int. Dairy J. 12 (2002), 407–411, 10.1016/S0958-6946(02)00023-7.
Corbo, M.R., Lanciotti, R., Albenzio, M., Sinigaglia, M., Occurrence and characterization of yeasts isolated from milks and dairy products of Apulia region. Int. J. Food Microbiol. 69 (2001), 147–152.
Corsetti, A., Rossi, J., Gobbetti, M., Interactions between yeasts and bacteria in the smear surface-ripened cheeses. Int. J. Food Microbiol. 69 (2001), 1–10, 10.1016/S0168-1605(01)00567-0.
Delavenne, E., Mounier, J., Asmani, K., Jany, J.-L., Barbier, G., Le Blay, G., Fungal diversity in cow, goat and ewe milk. Int. J. Food Microbiol. 151 (2011), 247–251, 10.1016/j.ijfoodmicro.2011.08.029.
Delcenserie, V., Taminiau, B., Delhalle, L., Nezer, C., Doyen, P., Crevecoeur, S., Roussey, D., Korsak, N., Daube, G., Microbiota characterization of a Belgian protected designation of origin cheese, Herve cheese, using metagenomic analysis. J. Dairy Sci. 97 (2014), 6046–6056, 10.3168/jds.2014-8225.
Fadda, M., Mossa, V., Pisano, M., Deplano, M., Cosentino, S., Occurrence and characterization of yeasts isolated from artisanal Fiore Sardo cheese. Int. J. Food Microbiol. 95 (2004), 51–59, 10.1016/j.ijfoodmicro.2004.02.001.
Fleet, G.H., Yeast spoilage of foods and beverages. Kurtzman, C.P., Fell, J.W., Boekhout, T., (eds.) The Yeasts: A Taxonomic Study, 2011, Elsevier, Amsterdam, 53–63.
Fox, P.F., McSweeney, P.L.H., Cogan, T.M., Guinee, T., Cheese: Chemistry, Physics and Microbiology. 2004, Elsevier Academic, Oxford.
Franzosa, E.A., Hsu, T., Sirota-Madi, A., Shafquat, A., Abu-Ali, G., Morgan, X.C., Huttenhower, C., Sequencing and beyond: integrating molecular “omics” for microbial community profiling. Nat. Rev. Microbiol. 13 (2015), 360–372, 10.1038/nrmicro3451.
Guého-Kellermann, E., Batra, R., Boekhout, T., Malassezia Baillon (1889). Kurtzman, C.P., Fell, J.W., Boekhout, T., (eds.) The Yeasts: A Taxonomic Study, 2011, Elsevier, Amsterdam, 1807–1832.
Irlinger, F., Mounier, J., Microbial interactions in cheese: implications for cheese quality and safety. Curr. Opin. Biotechnol. 20 (2009), 142–148, 10.1016/j.copbio.2009.02.016.
Jacques, N., Casaregola, S., Safety assessment of dairy microorganisms: the hemiascomycetous yeasts. Int. J. Food Microbiol. 126 (2008), 321–326, 10.1016/j.ijfoodmicro.2007.08.020.
Jakobsen, M., Narvhus, J., Yeasts and their possible beneficial and negative effects on the quality of dairy products. Int. Dairy J. 6 (1996), 755–768, 10.1016/0958-6946(95)00071-2.
Kõljalg, U., Nilsson, R.H., Abarenkov, K., Tedersoo, L., Taylor, A.F.S., Bahram, M., Bates, S.T., Bruns, T.D., Bengtsson-Palme, J., Callaghan, T.M., Douglas, B., Drenkhan, T., Eberhardt, U., Dueñas, M., Grebenc, T., Griffith, G.W., Hartmann, M., Kirk, P.M., Kohout, P., Larsson, E., Lindahl, B.D., Lücking, R., Martín, M.P., Matheny, P.B., Nguyen, N.H., Niskanen, T., Oja, J., Peay, K.G., Peintner, U., Peterson, M., Põldmaa, K., Saag, L., Saar, I., Schüßler, A., Scott, J.A., Senés, C., Smith, M.E., Suija, A., Taylor, D.L., Telleria, M.T., Weiss, M., Larsson, K.-H., Towards a unified paradigm for sequence-based identification of fungi. Mol. Ecol. 22 (2013), 5271–5277, 10.1111/mec.12481.
Kurtzman, C.P., Yarrowia van der Walt & von Arx (1980). Kurtzman, C.P., Fell, J.W., Boekhout, T., (eds.) The Yeasts: A Taxonomic Study, 2011, Elsevier, Amsterdam, 927–929.
Lachance, M.-A., Boekhout, T., Scorzetti, G., Fell, J.W., Kurtzman, C.P., Candida Berkhout (1923). Kurtzman, C.P., Fell, J.W., Boekhout, T., (eds.) The Yeasts: A Taxonomic Study, 2011, Elsevier, Amsterdam, 987–1278.
Lavoie, K., Touchette, M., St-Gelais, D., Labrie, S., Characterization of the fungal microflora in raw milk and specialty cheeses of the province of Quebec. Dairy Sci. Technol. 92 (2012), 455–468, 10.1007/s13594-011-0051-4.
Lindahl, B.D., Nilsson, R.H., Tedersoo, L., Abarenkov, K., Carlsen, T., Kjøller, R., Kõljalg, U., Pennanen, T., Rosendahl, S., Stenlid, J., Kauserud, H., Fungal community analysis by high-throughput sequencing of amplified markers - a user's guide. New Phytol. 199 (2013), 288–299, 10.1111/nph.12243.
Lopandic, K., Zelger, S., Bánszky, L.K., Eliskases-Lechner, F., Prillinger, H., Identification of yeasts associated with milk products using traditional and molecular techniques. Food Microbiol. 23 (2006), 341–350, 10.1016/j.fm.2005.05.001.
Lozupone, C.A., Knight, R., Global patterns in bacterial diversity. Proc. Natl. Acad. Sci. 104 (2007), 11436–11440, 10.1073/pnas.0611525104.
Minervini, F., Montagna, M.T., Spilotros, G., Monaci, L., Santacroce, M.P., Visconti, A., Survey on mycoflora of cow and buffalo dairy products from Southern Italy. Int. J. Food Microbiol. 69 (2001), 141–146.
Ogier, J.-C., Son, O., Gruss, A., Tailliez, P., Delacroix-Buchet, A., Identification of the bacterial microflora in dairy products by temporal temperature gradient gel electrophoresis. Appl. Environ. Microbiol. 68 (2002), 3691–3701.
Quigley, L., O'Sullivan, O., Stanton, C., Beresford, T.P., Ross, R.P., Fitzgerald, G.F., Cotter, P.D., The complex microbiota of raw milk. FEMS Microbiol. Rev. 37 (2013), 664–698, 10.1111/1574-6976.12030.
Rodriguez, C., Taminiau, B., Brévers, B., Avesani, V., Van Broeck, J., Leroux, A., Gallot, M., Bruwier, A., Amory, H., Delmée, M., Daube, G., Faecal microbiota characterisation of horses using 16 rDNA barcoded pyrosequencing, and carriage rate of Clostridium difficile at hospital admission. BMC Microbiol., 15, 2015, 1, 10.1186/s12866-015-0514-5.
Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., Sahl, J.W., Stres, B., Thallinger, G.G., Van Horn, D.J., Weber, C.F., Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75 (2009), 7537–7541, 10.1128/AEM.01541-09.
Schoch, C.L., Seifert, K.A., Huhndorf, S., Robert, V., Spouge, J.L., Levesque, C.A., Chen, W., Bolchacova, E., Voigt, K., Crous, P.W., Fungal barcoding consortium, Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc. Natl. Acad. Sci. 109 (2012), 6241–6246.
Toju, H., Tanabe, A.S., Yamamoto, S., Sato, H., High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PLoS One, 7, 2012, e40863, 10.1371/journal.pone.0040863.
Vaughan-Martini, A., Lachance, M.-A., Kurtzman, C.P., Kazachstania Zubkova (1971). Kurtzman, C.P., Fell, J.W., Boekhout, T., (eds.) The Yeasts: A Taxonomic Study, 2011, Elsevier, Amsterdam, 439–470.
Wojtatowicz, M., Chrzanowska, J., Juszczyk, P., Skiba, A., Gdula, A., Identification and biochemical characteristics of yeast microflora of Rokpol cheese. Int. J. Food Microbiol. 69 (2001), 135–140, 10.1016/S0168-1605(01)00582-7.
Wolfe, B.E., Dutton, R.J., Fermented foods as experimentally tractable microbial ecosystems. Cell 161 (2015), 49–55, 10.1016/j.cell.2015.02.034.
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 158 (2014), 422–433, 10.1016/j.cell.2014.05.041.