High sorbic acid resistance of Penicillium roqueforti is mediated by the SORBUS gene cluster

Punt, Maarten; Seekles, Sjoerd J; Dam, Jisca van; Toorop, Connor de Adelhart; Martina, Raithel R; Houbraken, Jos; Wösten, Han A. B.; Ohm, Robin A.

doi:10.1371/journal.pgen.1010086

Cited by 10 publications

(14 citation statements)

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“…Fungi can be exposed to various chemical biocides, in particular in crops and in food with preservatives. in some strains isolated from spoiled food, which has been attributed to the presence of a horizontally transferred region named SORBUS (Punt et al 2022). Here, we studied the impact, on the growth of the different P. roqueforti populations, of chemical preservatives used in the food industry (natamycin and sorbate), a fungicide used for crop treatment (tebuconazole) and of a weak organic acid present in cheese (lactic acid resulting from lactose degradation by lactic acid bacteria).…”

Section: Specific Traits In Penicillium Roqueforti Populations Benefi...mentioning

confidence: 99%

“…potassium sorbate and natamycin). In P. roqueforti , sorbate resistance has been reported in some strains isolated from spoiled food, which has been attributed to the presence of a horizontally transferred region named SORBUS (Punt et al 2022). In addition, the P. roqueforti population associated with silage may be exposed to triazoles, commonly used as fungicides on crops.…”

Section: Introductionmentioning

confidence: 99%

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A new cheese population inPenicillium roquefortiand adaptation of the five populations to their ecological niche

Crequer

Ropars

Jany

et al. 2023

Preprint

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Domestication is an excellent case study for understanding adaptation and multiple fungal lineages have been domesticated for fermenting food products. Studying domestication in fungi has thus both fundamental and applied interest. Genomic studies have revealed the existence of four populations within the blue-cheese-making fungus Penicillium roqueforti. The two cheese populations show footprints of domestication, but the adaptation of the two non-cheese populations to their ecological niches (i.e. silage/spoiled food and lumber/spoiled food) has not been investigated yet. Here, we reveal the existence of a new P. roqueforti population, specific to French Termignon cheeses, produced using small-scale traditional practices, with spontaneous blue mould colonisation. This Termignon population is genetically differentiated from the four previously identified populations, providing a novel source of genetic diversity for cheese making. Phenotypically, the non-Roquefort cheese population was the most differentiated, with specific traits beneficial for cheese making, in particular higher tolerance to salt, to acidic pH and to lactic acid. Our results support the view that this clonal population, used for many cheese types in multiple countries, is a domesticated lineage on which humans exerted strong selection. The Termignon population displayed substantial genetic diversity, both mating types, horizontally transferred regions previously detected in the non-Roquefort population, and intermediate phenotypes between cheese and non-cheese populations. The lumber/spoiled food and silage/spoiled food populations were not more tolerant to crop fungicides but showed faster growth in various carbon sources (e.g. dextrose, pectin, sucrose, xylose and/or lactose), which can be beneficial in their ecological niches. Such contrasted phenotypes between P. roqueforti populations, with beneficial traits for cheese-making in the cheese populations and enhanced ability to metabolise sugars in the lumber/spoiled food population, support the inference of domestication in cheese fungi and more generally of adaptation to anthropized environments.

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Section: Specific Traits In Penicillium Roqueforti Populations Benefi...mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A new cheese population inPenicillium roquefortiand adaptation of the five populations to their ecological niche

Crequer

Ropars

Jany

et al. 2023

Preprint

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“…The comparative genomics and transcriptomics in this study focussed on conidial heat resistance, and thus the presence of homologous weak acid resistance genes was not studied. Recently, the same GWAS methods were used to identify weak acid resistance gene cluster SORBUS in P. roqueforti (Punt et al, 2022b). For every P. variotii strain used in this study, a higher MIC for sorbic acid was found than previously reported for a P. variotii strain isolated from a South American soft drink production facility (Stratford et al, 2009).…”

Section: Discussionmentioning

confidence: 47%

“…Besides the eight P. variotii strains containing the 60 kbp cluster, the cluster was identified in nine of the 21 P. chrysogenum assemblies currently available on NCBI (https://www. ncbi.nlm.nih.gov/assembly/?term=penicillium+chrysogenum, June 21, 2021) and in one out of 34 newly sequenced P. roqueforti genomes (Punt et al, 2022b). In addition, various Aspergillus species contain fragments of the 60 kbp cluster.…”

Section: Discussionmentioning

confidence: 99%

“…Genome Wide Association Studies (GWAS) can also be used to identify genes involved in heat and weak acid resistance. The gene cluster SORBUS in P. roqueforti involved in sorbate resistance was identified using GWAS, which is homologous to the A. niger cluster that mediates weak acid resistance (Punt et al, 2022b). Hence, this example indicates that many more mechanisms of stress resistance could be studied by using the datasets presented in this research project.…”

Section: Implications and Future Researchmentioning

confidence: 99%

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Heterogeneity in stress resistance of Paecilomyces variotii and related food spoilage fungi

Brule¹

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Eurotiales reproduce sexually in different ways. In general, a compatible mating type is needed for sexual reproduction. Homothallic species are self-fertile and both mating types are present within their genome. Therefore, each individual colony can produce sexual spores, while it can also recombine with another strain. Heterothallic species, on the other hand, only contain one mating type in their genomes, meaning that they need to encounter another colony with the compatible mating type locus in order to reproduce sexually. During sexual reproduction, fruiting bodies like cleistothecia are formed, in which asci are produced that contain the sexually formed spores called ascospores.Many heterothallic Eurotiales were assumed to be asexual because their sexual form of reproduction was never observed. For this reason, they were called anamorphic fungi, Aspergillus niger and Penicillium roquefortiThe fungus A. niger is well known for its biotechnological applications and used for citric acid and enzyme production. Because of its industrial role, it has been widely used as a model organism to study fungal genetics (Pel et al., 2007). In addition, it is a food spoilage fungus causing black rot in grapes, onions and other fruits and vegetables. The fungus grows well under acidic conditions and therefore, it is a common spoiler of yoghurt products (Gougouli and Koutsoumanis, 2017).The fungus P. roqueforti, is known as the fermentation organism of blue vain cheeses (Coton et al., 2020;Ropars et al., 2012). It is well adapted to grow at low temperatures (Nguyen Van Long et al., 2021) and is able to grow at high concentrations of weak acids (Samson et al., 2019). Therefore, it is also an efficient spoiler of dairy products with a chilled chain storage. In addition, it is a common spoiler of bakery products and silage (Samson et al., 2019).Like P. variotii, both species are heterothallic and require mating with another strain with compatible mating type for sexual reproduction. Strains of P. roqueforti can recombine under specific conditions (Ropars et al., 2014), while sexual reproduction of A. niger has not yet been observed. Nevertheless, there are conditions in which sexual structures called sclerotia are formed (Ellena et al., 2021) and some strains can be recombined under lab conditions using the parasexual cycle (Arentshorst and Ram, 2018). STRESS RESISTANCE IN EUROTIALESThe ability of a fungus to spoil food is largely determined by its stress resistance and, as a consequence, its ability to grow through hurdles applied within the food environments. Stress resistance of fungal spores, which are regarded dormant with minimal metabolic activity (Novodvorska et al., 2016;Teertstra et al., 2017) and growing vegetative mycelium is different. In general, spores are considered more stress resistant than vegetative cells (Wyatt et al., 2013), but the resistance of mycelium to food preservative factors is equally important as it has to deal with low water activity and the presence of preservatives in order to grow.Spores mus...

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Starship Discovery: A Collaborative Approach to Uncover Massive Transposable Elements

Ament-Velásquez,

Gluck-Thaler,

Urquhart

et al. 2024

The Mycota

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High sorbic acid resistance of Penicillium roqueforti is mediated by the SORBUS gene cluster

Cited by 10 publications

References 60 publications

A new cheese population inPenicillium roquefortiand adaptation of the five populations to their ecological niche

A new cheese population inPenicillium roquefortiand adaptation of the five populations to their ecological niche

Heterogeneity in stress resistance of Paecilomyces variotii and related food spoilage fungi

Starship Discovery: A Collaborative Approach to Uncover Massive Transposable Elements

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