The Good, the Bad, and the Ugly: Tales of Mold-Ripened Cheese
- Authors: Sister Noëlla Marcellino O.S.B.1, David R. Benson2
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VIEW AFFILIATIONS HIDE AFFILIATIONSAffiliations: 1: Abbey of Regina Laudis, Bethlehem, CT 06751; 2: Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269-3125; 3: University of Vermont, Burlington, VT
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Received 13 April 2011 Accepted 02 September 2011 Published 31 October 2013
- Correspondence: Sister Noëlla Marcellino, O.S.B., [email protected]

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Abstract:
The history of cheese manufacture is a “natural history” in which animals, microorganisms, and the environment interact to yield human food. Part of the fascination with cheese, both scientifically and culturally, stems from its ability to assume amazingly diverse flavors as a result of seemingly small details in preparation. In this review, we trace the roots of cheesemaking and its development by a variety of human cultures over centuries. Traditional cheesemakers observed empirically that certain environments and processes produced the best cheeses, unwittingly selecting for microorganisms with the best biochemical properties for developing desirable aromas and textures. The focus of this review is on the role of fungi in cheese ripening, with a particular emphasis on the yeast-like fungus Geotrichum candidum. Conditions that encourage the growth of problematic fungi such as Mucor and Scopulariopsis as well as Arachnida (cheese mites), and how such contaminants might be avoided, are discussed. Bethlehem cheese, a pressed, uncooked, semihard, Saint-Nectaire-type cheese manufactured in the United Sates without commercial strains of bacteria or fungi, was used as a model for the study of stable microbial succession during ripening in a natural environment. The appearance of fungi during a 60-day ripening period was documented using light and scanning electron microscopy, and it was shown to be remarkably reproducible and parallel to the course of ripening of authentic Saint-Nectaire cheese in the Auvergne region of France. Geotrichum candidum, Mucor, and Trichothecium roseum predominate the microbiotas of both cheese types. Geotrichum in particular was shown to have high diversity in different traditional cheese ripening environments, suggesting that traditional manufacturing techniques selected for particular fungi. This and other studies suggest that strain diversity arises in relation to the lore and history of the regions from which these types of cheeses arose.
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Citation: Marcellino O.S.B. S, Benson D. 2013. The Good, the Bad, and the Ugly: Tales of Mold-Ripened Cheese. Microbiol Spectrum 1(1):CM-0005-12. doi:10.1128/microbiolspec.CM-0005-12.




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Abstract:
The history of cheese manufacture is a “natural history” in which animals, microorganisms, and the environment interact to yield human food. Part of the fascination with cheese, both scientifically and culturally, stems from its ability to assume amazingly diverse flavors as a result of seemingly small details in preparation. In this review, we trace the roots of cheesemaking and its development by a variety of human cultures over centuries. Traditional cheesemakers observed empirically that certain environments and processes produced the best cheeses, unwittingly selecting for microorganisms with the best biochemical properties for developing desirable aromas and textures. The focus of this review is on the role of fungi in cheese ripening, with a particular emphasis on the yeast-like fungus Geotrichum candidum. Conditions that encourage the growth of problematic fungi such as Mucor and Scopulariopsis as well as Arachnida (cheese mites), and how such contaminants might be avoided, are discussed. Bethlehem cheese, a pressed, uncooked, semihard, Saint-Nectaire-type cheese manufactured in the United Sates without commercial strains of bacteria or fungi, was used as a model for the study of stable microbial succession during ripening in a natural environment. The appearance of fungi during a 60-day ripening period was documented using light and scanning electron microscopy, and it was shown to be remarkably reproducible and parallel to the course of ripening of authentic Saint-Nectaire cheese in the Auvergne region of France. Geotrichum candidum, Mucor, and Trichothecium roseum predominate the microbiotas of both cheese types. Geotrichum in particular was shown to have high diversity in different traditional cheese ripening environments, suggesting that traditional manufacturing techniques selected for particular fungi. This and other studies suggest that strain diversity arises in relation to the lore and history of the regions from which these types of cheeses arose.

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Figures
Scanning electron micrographs of Bethlehem cheese during ripening. (A) Micrograph of cheese at day 2 of ripening showing multilateral budding yeasts embedded within the cheese surface. Buds and bud scars are clearly visible. Bar, 1 μm. (B) Micrograph of the cheese surface at day 6 showing sporangia and hyphae of the zygomycete Mucor. Bar, 10 µm. (C) At day 59, the V shapes of coryneform bacteria can be distinguished at a high magnification beneath a mass of fungal debris on the cheese rind. Bar, 1 µm. Panels A and B are reproduced with permission from reference 58. doi:10.1128/microbiolspec.CM-0005-2012.f1.

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FIGURE 1
Scanning electron micrographs of Bethlehem cheese during ripening. (A) Micrograph of cheese at day 2 of ripening showing multilateral budding yeasts embedded within the cheese surface. Buds and bud scars are clearly visible. Bar, 1 μm. (B) Micrograph of the cheese surface at day 6 showing sporangia and hyphae of the zygomycete Mucor. Bar, 10 µm. (C) At day 59, the V shapes of coryneform bacteria can be distinguished at a high magnification beneath a mass of fungal debris on the cheese rind. Bar, 1 µm. Panels A and B are reproduced with permission from reference 58. doi:10.1128/microbiolspec.CM-0005-2012.f1.
The yeast-like fungus Geotrichum candidum. (A) G. candidum on the rind of a 10-day-old Tomme de Savoie. (B) Light micrograph of arthrospores and septate hyphae of a wild-type G. candidum strain isolated from a 4-day-old Bethlehem cheese. Bar, 10 µm. (C) Scanning electron micrograph of the surface of a Reblochon ripening shelf showing cylindrical G. candidum arthrospores and bacteria. Bar, 5 µm. Reproduced with permission from reference 77 (micrograph by Romain Briandet, UMR-UBHM, Institut National de la Recherche Agronomique et Ecole Nationale Supérieure des Industries Agricoles et Alimentaires, Massy, France). doi:10.1128/microbiolspec.CM-0005-2012.f2.

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FIGURE 2
The yeast-like fungus Geotrichum candidum. (A) G. candidum on the rind of a 10-day-old Tomme de Savoie. (B) Light micrograph of arthrospores and septate hyphae of a wild-type G. candidum strain isolated from a 4-day-old Bethlehem cheese. Bar, 10 µm. (C) Scanning electron micrograph of the surface of a Reblochon ripening shelf showing cylindrical G. candidum arthrospores and bacteria. Bar, 5 µm. Reproduced with permission from reference 77 (micrograph by Romain Briandet, UMR-UBHM, Institut National de la Recherche Agronomique et Ecole Nationale Supérieure des Industries Agricoles et Alimentaires, Massy, France). doi:10.1128/microbiolspec.CM-0005-2012.f2.
Schema for proteolysis in Camembert cheese. doi:10.1128/microbiolspec.CM-0005-2012.f3.

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FIGURE 3
Schema for proteolysis in Camembert cheese. doi:10.1128/microbiolspec.CM-0005-2012.f3.
Challenges for the cheesemaker. (A) Scanning electron micrograph of a cheese mite. Left unchecked, cheese mites can lead to a 25% reduction in the weight of a ripened cheese. Photograph by William R. McManus, generously provided and used with permission of William R. McManus and Donald J. McMahon, Utah State University. (B) Spoilage of a cheese by contamination and invasion of the rind by the fungal genus Scopulariopsis. (C) Scanning electron micrograph of the zygomycete Mucor showing sporangia among collapsed hyphae. When the fragile outer membrane, the peridium (arrowhead), of the sporangium breaks open, hundreds to thousands of spores can be released, contaminating a cheese cave overnight. Bar, 10 µm. doi:10.1128/microbiolspec.CM-0005-2012.f4.

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FIGURE 4
Challenges for the cheesemaker. (A) Scanning electron micrograph of a cheese mite. Left unchecked, cheese mites can lead to a 25% reduction in the weight of a ripened cheese. Photograph by William R. McManus, generously provided and used with permission of William R. McManus and Donald J. McMahon, Utah State University. (B) Spoilage of a cheese by contamination and invasion of the rind by the fungal genus Scopulariopsis. (C) Scanning electron micrograph of the zygomycete Mucor showing sporangia among collapsed hyphae. When the fragile outer membrane, the peridium (arrowhead), of the sporangium breaks open, hundreds to thousands of spores can be released, contaminating a cheese cave overnight. Bar, 10 µm. doi:10.1128/microbiolspec.CM-0005-2012.f4.
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