Independent domestication events in the blue-cheese fungus<i>Penicillium roqueforti</i>

Dumas, Émilie; Feurtey, Alice; Vega, Ricardo C. Rodrí­guez de la; Prieur, Stéphanie Le; Snirc, Alodie; Coton, Monika; Thierry, Anne; Coton, Emmanuel; Piver, Mélanie Le; Roueyre, Daniel; Ropars, Jeanne; Branca, Antoine; Giraud, Tatiana

doi:10.1101/451773

Cited by 15 publications

(110 citation statements)

References 91 publications

(119 reference statements)

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“…Both cheese populations have lower levels of genetic diversity than the two non-cheese populations, indicating an occurrence of bottlenecks (Dumas et al, 2020), which typically occur during domestication. The two cheese populations are genetically and phenotypically differentiated from each other, suggesting that they result from independent domestication events (Dumas et al, 2020). One of the cheese populations, the non-Roquefort population, is a clonal lineage with a very low level of genetic diversity, used to produce most types of blue…”

Section: /38mentioning

confidence: 98%

“…Penicillium roqueforti is also found in non-cheese environments (Pitt et al, 2009;Ropars et al, 2012), 4/38 and four genetically differentiated clusters of individuals (i.e., populations) have been identified in P. roqueforti. Two populations are used for cheesemaking, whereas the other two populations thrive in silage, lumber or spoiled food (Ropars et al, 2014;Gillot et al, 2015;Dumas et al, 2020). Genomic and experimental approaches have provided compelling…”

Section: /38mentioning

confidence: 99%

“…evidence for the domestication of cheese P. roqueforti populations (Cheeseman et al, 2014;Ropars et al, 2015Ropars et al, a & b, 2017Gillot et al, 2015Gillot et al, , 2017Dumas et al, 2020). Indeed, the populations of P. roqueforti used to make blue cheeses display the characteristic features of domesticated organisms: genetic and phenotypic differences relative to non-cheese populations, with, in particular, traits beneficial for cheese production, such as faster growth on cheese medium (Ropars et al, 2014Gillot et al, 2015;Dumas et al, 2020), but also lower fertility and lower fitness in nutrient-poor conditions (Ropars et al, 2015.…”

Section: /38mentioning

confidence: 99%

“…cheeses worldwide. The second cheese population, the Roquefort population, is genetically more diverse and contains all the strains used to produce blue cheeses from the emblematic Roquefort protected designation of origin (PDO) (Dumas et al, 2020). In vitro tests showed that the non-Roquefort population displayed faster tributyrin degradation (i.e.…”

Section: /38mentioning

confidence: 99%

“…In vitro tests showed that the non-Roquefort population displayed faster tributyrin degradation (i.e. a certain type of lipolysis) and a higher salt tolerance, faster in vitro growth on cheese medium and better exclusion of competitors than the Roquefort population (Ropars et al, 2014(Ropars et al, , 2015Dumas et al, 2020). The specific features of the Roquefort population may result from the constraints of the PDO, requiring the use of local strains and at least 90 days of maturation, and…”

Section: /38mentioning

confidence: 99%

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Strong effect ofPenicillium roquefortipopulations on volatile and metabolic compounds responsible for aromas, flavor and texture in blue cheeses

Caron¹,

Piver²,

Péron³

et al. 2020

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The study of food microorganism domestication can bring important insights on adaptation mechanisms and have industrial applications. The Penicillium roqueforti mold is divided into four main populations, with two populations domesticated for blue-cheese making and two populations thriving in other environments. While most blue cheeses worldwide are made with the same P. roqueforti clonal lineage, the emblematic Roquefort cheeses are inoculated with a specific population. To study the differences among P.roqueforti populations in the context of domestication for cheesemaking, we compared blue cheeses made with the four fungal populations following Roquefort-type production specifications. We found that the P. roqueforti populations had a minor impact on the cheese bacterial diversity and none on the main microorganism abundance. The cheese P. roqueforti populations produced cheeses with higher percentages of blue area and with different sets and higher quantities of desired volatile compounds. The Roquefort P. roqueforti population in particular produced higher quantities of positive aromatic compounds in cheeses, which was related due to its most efficient proteolysis and lipolysis, and also produced cheeses with lower water activity, thus restricting spoiler microorganisms. Our results show the strong influence of P. roqueforti populations on several important aspects of cheese safety, appearance and flavour. The typical appearance and flavours of blue cheeses are therefore the result of human selection on P. roqueforti, thus constituting domestication, and the two cheese populations have acquired specificities. This has important implications for our understanding of adaptation and domestication processes as well as for improving cheese production.Importance: Several fungi have been domesticated for food fermentation, with selection for traits beneficial for food production. The mold used for making blue cheeses, Penicillium roqueforti, is subdivided into four genetically different populations, two being found in cheese, one being specific of the Roquefort protected designation of origin, and two in other environments. The cheese P. roqueforti populations produced bluer cheeses with higher quantities of desired volatile compounds. The Roquefort P. roqueforti population in particular produced higher quantities of positive aromatic compounds in cheeses, in relation to its most efficient proteolysis and lipolysis, and also produced cheeses with lower water activity, thus restricting spoiler microorganisms. Our results support that the blue cheese typical aspect and flavors are the result of a selection by humans and show the strong influence of P. roqueforti populations for several important aspects of cheese safety, aspect and flavor, paving the way for improving cheese production.

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Section: /38mentioning

confidence: 98%

Section: /38mentioning

confidence: 99%

Section: /38mentioning

confidence: 99%

Section: /38mentioning

confidence: 99%

Section: /38mentioning

confidence: 99%

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Strong effect ofPenicillium roquefortipopulations on volatile and metabolic compounds responsible for aromas, flavor and texture in blue cheeses

Caron¹,

Piver²,

Péron³

et al. 2020

Preprint

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Domestication of Industrial Microbes

et al. 2019

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Domestication refers to artificial selection and breeding of wild species to obtain cultivated variants that thrive in man-made niches and meet human or industrial requirements. Several genotypic and phenotypic signatures of domestication have been described in crops, livestock and pets. However, domestication is not unique to plants and animals. Microbial diversity has also been shaped by the emergence of novel and highly specific man-made environments, like food and beverage fermentations. This allowed rapid adaptation and diversification of various microbes, such as certain Lactococcus, Lactobacillus, Oenococcus, Saccharomyces and Aspergillus species. During the domestication process, microbes gained the capacity to efficiently consume particular nutrients, cope with a multitude of industry-specific stress factors and produce desirable compounds, often at the cost of a reduction in fitness in their original, natural environments. Moreover, different lineages of the same species adapted to highly diverse niches, resulting in genetically and phenotypically distinct strains. In this Review, we discuss the basic principles of microbial domestication and describe how recent research is uncovering its genetic underpinnings.

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Hallstatt miners consumed blue cheese and beer during the Iron Age and retained a non-Westernized gut microbiome until the Baroque period

et al. 2021

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Independent domestication events in the blue-cheese fungusPenicillium roqueforti

Cited by 15 publications

References 91 publications

Strong effect ofPenicillium roquefortipopulations on volatile and metabolic compounds responsible for aromas, flavor and texture in blue cheeses

Strong effect ofPenicillium roquefortipopulations on volatile and metabolic compounds responsible for aromas, flavor and texture in blue cheeses

Domestication of Industrial Microbes

Hallstatt miners consumed blue cheese and beer during the Iron Age and retained a non-Westernized gut microbiome until the Baroque period

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