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Biodiversity of the Surface Microbial Consortia from Limburger, Reblochon, Livarot, Tilsit, and Gubbeen Cheeses

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  • Authors: Timothy M. Cogan1, Stefanie Goerges2, Roberto Gelsomino3, Sandra Larpin4, Markus Hohenegger5, Nagamani Bora6, Emmanuel Jamet7, Mary C. Rea8, Jérôme Mounier9, Marc Vancanneyt10, Micheline Guéguen11, Nathalie Desmasures12, Jean Swings13, Mike Goodfellow14, Alan C. Ward15, Hans Sebastiani16, Françoise Irlinger17, Jean-Francois Chamba18, Ruediger Beduhn19, Siegfried Scherer20
  • Editor: Catherine W. Donnelly21
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Moorepark Food Research Center, Teagasc, Fermoy, Ireland; 2: Naturkost Ernst Weber GmbH, 81371 Munich, Germany; 3: SA Coca Cola Services N.V., 1070 Brussels, Belgium; 4: Bioprocess Division, Millipore Corporation, 67120 Molsheim, France; 5: Bundesanstalt für Alpenländische Milchwirtschaft, 6200 Rotholz, Austria; 6: School of Life and Health Sciences, Aston University, Birmingham B4 7ET, United Kingdom; 7: Actilait, 75314 Paris Cedex 09, France; 8: Moorepark Food Research Center, Teagasc, Fermoy, Ireland; 9: Laboratoire Universitaire de Biodiversité et Ecologie Microbienne (EA3882), IFR148 ScInBioS, Université Européenne de Bretagne, Université de Brest, ESMISAB, Technopôle de Brest Iroise, 29280 Plouzané, France; 10: BCCM/LMG Bacteria Collection, Laboratorium voor Microbiologie, Universiteit Gent, 9000 Gent, Belgium; 11: Unité des Micro-organismes d'Intérêt Laitier et Alimentaire, IFR146 ICORE, Université de Caen Basse-Normandie, 14032 Caen, France; 12: Unité des Micro-organismes d'Intérêt Laitier et Alimentaire, IFR146 ICORE, Université de Caen Basse-Normandie, 14032 Caen, France; 13: BCCM/LMG Bacteria Collection, Laboratorium voor Microbiologie, Universiteit Gent, 9000 Gent, Belgium; 14: Microbial Resources Centre, University of Newcastle, Newcastle upon Tyne NE1 7RU, United Kingdom; 15: Microbial Resources Centre, University of Newcastle, Newcastle upon Tyne NE1 7RU, United Kingdom; 16: Bundesanstalt für Alpenländische Milchwirtschaft, 6200 Rotholz, Austria; 17: Laboratoire de Génie et de Microbiologie des Procédés Alimentaires, INRA, AgroParis-Tech, 78850 Thiverval Grignon, France; 18: Deceased, Institut Technique Français des Fromages, 74801 La Roche sur Foron Cedex, France; 19: J. Bauer KG, 83512 Wasserburg/Inn, Germany; 20: Lehrstuhl für Mikrobielle Ökologie, Abteilung für Mikrobiologie, Zentralinstitut für Ernährungs-und Lebensmittelforschung, Technische Universität München, 85354 Freising, Germany; 21: University of Vermont, Burlington, VT
  • Source: microbiolspec January 2014 vol. 2 no. 1 doi:10.1128/microbiolspec.CM-0010-2012
  • Received 17 January 2011 Accepted 04 April 2012 Published 31 January 2014
  • Tim Cogan, tmcogan@gmail.com
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  • Abstract:

    Comprehensive collaborative studies from our laboratories reveal the extensive biodiversity of the microflora of the surfaces of smear-ripened cheeses. Two thousand five hundred ninety-seven strains of bacteria and 2,446 strains of yeasts from the surface of the smear-ripened cheeses Limburger, Reblochon, Livarot, Tilsit, and Gubbeen, isolated at three or four times during ripening, were identified; 55 species of bacteria and 30 species of yeast were found. The microfloras of the five cheeses showed many similarities but also many differences and interbatch variation. Very few of the commercial smear microorganisms, deliberately inoculated onto the cheese surface, were reisolated and then mainly from the initial stages of ripening, implying that smear cheese production units must have an adventitious “house” flora. Limburger cheese had the simplest microflora, containing two yeasts, and , and two bacteria, and . The microflora of Livarot was the most complicated, comprising 10 yeasts and 38 bacteria, including many gram-negative organisms. Reblochon also had a very diverse microflora containing 8 yeasts and 13 bacteria (excluding gram-negative organisms which were not identified), while Gubbeen had 7 yeasts and 18 bacteria and Tilsit had 5 yeasts and 9 bacteria. was by far the dominant yeast, followed in order by , , and . was the dominant bacterium and was found in every batch of the 5 cheeses. The next most common bacteria, in order, were , , , , and . was mainly found in Gubbeen, and was found in all cheeses but not in every batch. was found in most batches of Reblochon, Livarot, Tilsit, and Gubbeen. was found in all batches of Gubbeen and Reblochon but in only one batch of Tilsit and in no batch of Limburger or Livarot. Other bacteria were isolated in low numbers from each of the cheeses, suggesting that each of the 5 cheeses has a unique microflora. In Gubbeen cheese, several different strains of the dominant bacteria were present, as determined by pulsed-field gel electrophoresis, and many of the less common bacteria were present as single clones. The culture-independent method, denaturing gradient gel electrophoresis, resulted in identification of several bacteria which were not found by the culture-dependent (isolation and -PCR identification) method. It was thus a useful complementary technique to identify other bacteria in the cheeses. The gross composition, the rate of increase in pH, and the indices of proteolysis were different in most of the cheeses.

  • Citation: Cogan T, Goerges S, Gelsomino R, Larpin S, Hohenegger M, Bora N, Jamet E, Rea M, Mounier J, Vancanneyt M, Guéguen M, Desmasures N, Swings J, Goodfellow M, Ward A, Sebastiani H, Irlinger F, Chamba J, Beduhn R, Scherer S. 2014. Biodiversity of the Surface Microbial Consortia from Limburger, Reblochon, Livarot, Tilsit, and Gubbeen Cheeses. Microbiol Spectrum 2(1):CM-0010-2012. doi:10.1128/microbiolspec.CM-0010-2012.

Key Concept Ranking

Denaturing Gradient Gel Electrophoresis
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Random Amplified Polymorphic DNA
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References

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Abstract:

Comprehensive collaborative studies from our laboratories reveal the extensive biodiversity of the microflora of the surfaces of smear-ripened cheeses. Two thousand five hundred ninety-seven strains of bacteria and 2,446 strains of yeasts from the surface of the smear-ripened cheeses Limburger, Reblochon, Livarot, Tilsit, and Gubbeen, isolated at three or four times during ripening, were identified; 55 species of bacteria and 30 species of yeast were found. The microfloras of the five cheeses showed many similarities but also many differences and interbatch variation. Very few of the commercial smear microorganisms, deliberately inoculated onto the cheese surface, were reisolated and then mainly from the initial stages of ripening, implying that smear cheese production units must have an adventitious “house” flora. Limburger cheese had the simplest microflora, containing two yeasts, and , and two bacteria, and . The microflora of Livarot was the most complicated, comprising 10 yeasts and 38 bacteria, including many gram-negative organisms. Reblochon also had a very diverse microflora containing 8 yeasts and 13 bacteria (excluding gram-negative organisms which were not identified), while Gubbeen had 7 yeasts and 18 bacteria and Tilsit had 5 yeasts and 9 bacteria. was by far the dominant yeast, followed in order by , , and . was the dominant bacterium and was found in every batch of the 5 cheeses. The next most common bacteria, in order, were , , , , and . was mainly found in Gubbeen, and was found in all cheeses but not in every batch. was found in most batches of Reblochon, Livarot, Tilsit, and Gubbeen. was found in all batches of Gubbeen and Reblochon but in only one batch of Tilsit and in no batch of Limburger or Livarot. Other bacteria were isolated in low numbers from each of the cheeses, suggesting that each of the 5 cheeses has a unique microflora. In Gubbeen cheese, several different strains of the dominant bacteria were present, as determined by pulsed-field gel electrophoresis, and many of the less common bacteria were present as single clones. The culture-independent method, denaturing gradient gel electrophoresis, resulted in identification of several bacteria which were not found by the culture-dependent (isolation and -PCR identification) method. It was thus a useful complementary technique to identify other bacteria in the cheeses. The gross composition, the rate of increase in pH, and the indices of proteolysis were different in most of the cheeses.

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FIGURE 1

Photographs of the cheeses studied. (A) Gubbeen; (B) Limburger; (C) Livarot; (D) Reblochon; (E) Tilsit. Sources: (C) Chambre Régionale d'Agriculture de Normandie (Tesseraud); (D) Wikimedia Commons (user: Myrabella). doi:10.1128/microbiolspec.CM-0010-2012.f1

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FIGURE 2

Changes in dry matter and salt in Gubbeen (GB), Tilsit (TS), Livarot (LV), Limburger (LM), and Reblochon (RB) cheeses during ripening. doi:10.1128/microbiolspec.CM-0010-2012.f2

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FIGURE 3

Changes in pH, lactate, and salt in Gubbeen (GB), Tilsit (TS), Livarot (LV), Limburger (LM), and Reblochon (RB) cheeses during ripening. DM, dry matter. doi:10.1128/microbiolspec.CM-0010-2012.f3

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FIGURE 4

Relationship between pH and lactate in Gubbeen (GB), Tilsit (TS), Livarot (LV), Limburger (LM), and Reblochon (RB) cheeses during ripening. DM, dry matter. doi:10.1128/microbiolspec.CM-0010-2012.f4

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FIGURE 5

Changes in amino-soluble nitrogen (ASN) and nonprotein nitrogen (NPN) in Gubbeen (GB), Tilsit (TS), Livarot (LV), Limburger (LM), and Reblochon (RB) cheeses during ripening. doi:10.1128/microbiolspec.CM-0010-2012.f5

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FIGURE 6

Growth of bacteria and yeast in Gubbeen (GB), Tilsit (TS), Livarot (LV), Limburger (LM), and Reblochon (RB) cheeses during ripening. doi:10.1128/microbiolspec.CM-0010-2012.f6

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FIGURE 7

DGGE profile of Reblochon cheese. Samples were run in duplicate. RB1, RB2, and RB3 refer to batches 1, 2, and 3, respectively, from the early (1 day), middle (6 days), and late (15 days) stages of ripening. Lanes 1, 14, and 21 correspond to a ϕX174 DGGE marker. Organisms were identified as follows: 1 and 2, sp.; 3, sp.; 4, sp.; 5, uncultured actinobacterium; 6, sp.; 7, sp. doi:10.1128/microbiolspec.CM-0010-2012.f7

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Tables

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TABLE 1

Number of isolates of each species of yeast in all batches of cheese

Source: microbiolspec January 2014 vol. 2 no. 1 doi:10.1128/microbiolspec.CM-0010-2012
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TABLE 2

Number of isolates of each species of bacteria in all batches of cheese

Source: microbiolspec January 2014 vol. 2 no. 1 doi:10.1128/microbiolspec.CM-0010-2012
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TABLE 3

Bacterial taxa identified by DGGE in the different cheeses

Source: microbiolspec January 2014 vol. 2 no. 1 doi:10.1128/microbiolspec.CM-0010-2012

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