Penicillium roqueforti

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Penicillium roqueforti
Blue Stilton Penicillium.jpg
Blue Stilton cheese, showing the blue-green mold veins produced by Penicillium roqueforti
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Eurotiomycetes
Order: Eurotiales
Family: Aspergillaceae
Genus: Penicillium
Species:
P. roqueforti
Binomial name
Penicillium roqueforti
Thom (1906)
Synonyms [1]
  • Penicillium roqueforti var. weidemannii Westling (1911) [2]
  • Penicillium weidemannii(Westling) Biourge (1923) [3]
  • Penicillium gorgonzolaeWeid. (1923)
  • Penicillium roqueforti var. virideDatt.-Rubbo (1938) [4]
  • Penicillium roqueforti var. punctatumS.Abe (1956)
  • Penicillium conservandiNovobr. (1974)

Penicillium roqueforti is a common saprotrophic fungus in the genus Penicillium . Widespread in nature, it can be isolated from soil, decaying organic matter, and plants.

Contents

The major industrial use of this fungus is the production of blue cheeses, flavouring agents, antifungals, polysaccharides, proteases, and other enzymes. The fungus has been a constituent of Roquefort, Stilton, Danish blue, Cabrales, and other blue cheeses. Other blue cheeses, such as Gorgonzola, are made with Penicillium glaucum .

Classification

First described by American mycologist Charles Thom in 1906, [5] P. roqueforti was initially a heterogeneous species of blue-green, sporulating fungi. They were grouped into different species based on phenotypic differences, but later combined into one species by Kenneth B. Raper and Thom (1949). The P. roqueforti group got a reclassification in 1996 due to molecular analysis of ribosomal DNA sequences. Formerly divided into two varieties―cheese-making (P. roqueforti var. roqueforti) and patulin-making (P. roqueforti var. carneum)―P. roqueforti was reclassified into three species: P. roqueforti, P. carneum , and P. paneum . [6] The complete genome sequence of P. roqueforti was published in 2014. [7]

Description

As this fungus does not form visible fruiting bodies, descriptions are based on macromorphological characteristics of fungal colonies growing on various standard agar media, and on microscopic characteristics. When grown on Czapek yeast autolysate agar or yeast-extract sucrose (YES) agar, P. roqueforti colonies are typically 40 mm in diameter, olive brown to dull green (dark green to black on the reverse side of the agar plate), with a velutinous texture. Grown on malt extract agar, colonies are 50 mm in diameter, dull green in color (beige to greyish green on the reverse side), with arachnoid (with many spider-web-like fibers) colony margins. [8] Another characteristic morphological feature of this species is its production of asexual spores in phialides with a distinctive brush-shaped configuration. [9] [10] [11]

Evidence for a sexual stage in P. roqueforti has been found, based in part on the presence of functional mating-type genes and most of the important genes known to be involved in meiosis. [12] In 2014, researchers reported inducing the growth of sexual structures in P. roqueforti, including ascogonia, cleistothecia, and ascospores. Genetic analysis and comparison of many different strains isolated from various environments around the world indicate that it is a genetically diverse species. [13]

P. roqueforti can tolerate cold temperatures, low oxygen levels, and both alkali and weaker acid preservatives which allows the fungi to thrive and be found in dairy environments, such as cheese. On the other hand, it also spoils refrigerated foods and meats, breads, and silage.

Uses

The chief industrial use of this species is the production of blue cheeses, such as its namesake Roquefort, [14] Bleu de Bresse, Bleu du Vercors-Sassenage, Brebiblu, Cabrales, Cambozola (Blue Brie), Cashel Blue, Danish blue, Swedish Ädelost, Polish Rokpol made from cow's milk, Fourme d'Ambert, Fourme de Montbrison, Lanark Blue, Shropshire Blue, and Stilton, and some varieties of Bleu d'Auvergne and Gorgonzola. (Other blue cheeses, including Bleu de Gex and Rochebaron, use Penicillium glaucum .)

When placed into cream and aerated, P. roqueforti produces concentrated blue cheese flavoring, a type of enzyme-modified cheese. [15] A similar flavoring can be produced using other sources of fatty acids such as coconut oil. [16]

Strains of the microorganism are also used to produce compounds that can be employed as antibiotics, flavours, and fragrances, [17] uses not regulated under the U.S. Toxic Substances Control Act. Its texture is chitinous.

Secondary metabolites

Considerable evidence indicates that most strains are capable of producing harmful secondary metabolites (alkaloids and other mycotoxins) under certain growth conditions. [18] [19] [20] [21] Aristolochene is a sesquiterpenoid compound produced by P. roqueforti, and is likely a precursor to the toxin known as PR toxin, made in large amounts by the fungus. [22] PR-toxin has been implicated in incidents of mycotoxicoses resulting from eating contaminated grains. [20] [23] However, PR toxin is not stable in cheese and breaks down to the less toxic PR imine. [24]

Secondary metabolites of P. roqueforti, named andrastins A–D, are found in blue cheese. The andrastins inhibit proteins involved in the efflux of anticancer drugs from multidrug-resistant cancer cells. [25]

P. roqueforti also produces the neurotoxin roquefortine C. [26] [27] However, the levels of roquefortine C in cheese made from it is usually too low to produce toxic effects. The organism can also be used for the production of proteases and specialty chemicals, such as methyl ketones, including 2-heptanone. [28]

See also

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<i>Penicillium</i> Genus of fungi

Penicillium is a genus of ascomycetous fungi that is part of the mycobiome of many species and is of major importance in the natural environment, in food spoilage, and in food and drug production.

<span class="mw-page-title-main">Blue cheese</span> Cheese with blue veins of mold

Blue cheese is any of a wide range of cheeses made with the addition of cultures of edible molds, which create blue-green spots or veins through the cheese. Blue cheeses vary in taste from very mild to strong, and from slightly sweet to salty or sharp; in colour from pale to dark; and in consistency from liquid or very soft to firm or hard. They may have a distinctive smell, either from the mold or from various specially cultivated bacteria such as Brevibacterium linens.

<i>Penicillium camemberti</i> Species of fungus

Penicillium camemberti is a species of fungus in the genus Penicillium. It is used in the production of Camembert, Brie, Langres, Coulommiers, and Cambozola cheeses, on which colonies of P. camemberti form a hard, white crust. It is responsible for giving these cheeses their distinctive flavors. An allergy to the antibiotic penicillin does not necessarily imply an allergy to cheeses made using P. camemberti.

Penicillium crustosum is a blue-green or blue-grey mold that can cause food spoilage, particularly of protein-rich foods such as meats and cheeses. It is identified by its complex biseriate conidiophores on which phialides produce asexual spores. It can grow at fairly low temperatures, and in low water activity environments.

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<i>Penicillium expansum</i> Species of fungus

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<span class="mw-page-title-main">Aristolochene</span> Chemical compound

Aristolochene is a bicyclic sesquiterpene produced by certain fungi including the cheese mold Penicillium roqueforti. It is biosynthesized from farnesyl pyrophosphate by aristolochene synthase and is the parent hydrocarbon of a large variety of fungal toxins.

<span class="mw-page-title-main">Roquefortine C</span> Chemical compound

Roquefortine C is a mycotoxin that belongs to a class of naturally occurring 2,5-diketopiperazines produced by various fungi, particularly species from the genus Penicillium. It was first isolated from a strain of Penicillium roqueforti, a species commercially used as a source of proteolytic and lipolytic enzymes during maturation of the blue-veined cheeses, Roquefort, Danish Blue, Stilton and Gorgonzola.

<i>Penicillium chrysogenum</i> Species of fungus

Penicillium chrysogenum is a species of fungus in the genus Penicillium. It is common in temperate and subtropical regions and can be found on salted food products, but it is mostly found in indoor environments, especially in damp or water-damaged buildings. It has been recognised as a species complex that includes P. notatum, P. meleagrinum, and P. cyaneofulvum. Molecular phylogeny has established that Alexander Fleming's first discovered penicillin producing strain is of a distinct species, P. rubens, and not of P. notatum. It has rarely been reported as a cause of human disease. It is the source of several β-lactam antibiotics, most significantly penicillin. Other secondary metabolites of P. chrysogenum include roquefortine C, meleagrin, chrysogine, 6-MSA YWA1/melanin, andrastatin A, fungisporin, secalonic acids, sorbicillin, and PR-toxin.

Penicillium carneum is a fungus species of the genus of Penicillium.Penicillium roqueforti var. carneum was reclassified to Penicillium carneum.P. carneum was isolated from spoiled meat products, silage, rye bread, water, beer, cheese, mouldy barkers yeast and cork. P. carneum produces patulin, penicillic acid, penitrem A, mycophenolic acid roquefortines.

Penicillium psychrosexualis is a filamentous fungus in the genus Penicillium. Described as new to science in 2010, the species was found growing on refrigerated moldy apples in the Netherlands. It is closely related to the blue cheese fungus P. roqueforti.

Penicillium paneum is a species of fungus in the genus Penicillium which can spoil cereal grains. Penicillium paneum produces 1-Octen-3-ol and penipanoid A, penipanoid B, penipanoid C, patulin and roquefortine C

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<i>Penicillium solitum</i> Species of fungus

Penicillium solitum is an anamorphic, mesophilic, salinity-tolerant, and psychrotolerant species of fungus in the genus Penicillium. It is known to produce various compounds including polygalacturonase, compactin, cyclopenin, cyclopenol, cyclopeptin, dehydrocompactin, dihydrocyclopeptin, palitantin, solistatin, solistatinol, viridicatin, viridicatol.

Penicillium tulipae is a species of fungus in the genus Penicillium which produces penicillic acid, roquefortine C, roquefortine D, terrestric acid, glandicoline A, glandicoline B, meleagrin, oxaline, penitrem A and epineoxaline.

Penicillium verrucosum is a psychrophilic fungus which was discovered in Belgium and introduced by Dierckx in 1901. Six varieties of this species have been recognized based primarily on differences in colony colour: P. verrucosum var. album, P. verrucosum var. corymbiferum, P. verrucosum var. cyclopium, P. verrucosum var. ochraceum, P. verrucosum var. melanochlorum and P. verrucosum var. verrucosum. This fungus has important implications in food, specifically for grains and other cereal crops on which it grows. Its growth is carefully regulated in order to reduce food spoilage by this fungi and its toxic products. The genome of P. verrucosum has been sequenced and the gene clusters for the biosyntheses of its mycotoxins have been identified.

Aspergillus brevipes is an anamorph species of fungus in the genus Aspergillus. It is from the Fumigati section. It was first described in 1952. It has been isolated from soil in Australia. Aspergillus brevipes produces roquefortine C, meleagrin and viriditoxin.

Penicillium commune is an indoor fungus belonging to the genus Penicillium. It is known as one of the most common fungi spoilage moulds on cheese. It also grows on and spoils other foods such as meat products and fat-containing products like nuts and margarine. Cyclopiazonic acid and regulovasine A and B are the most important mycotoxins produced by P. commune. The fungus is the only known species to be able to produce both penitrem A and roquefortine. Although this species does not produce penicillin, it has shown to have anti-pathogenic activity. There are no known plant, animal or human diseases caused by P. commune.

<span class="mw-page-title-main">PR toxin</span> Chemical compound

Penicillin Roquefort toxin is a mycotoxin produced by the fungi Penicillium roqueforti. In 1973, PR toxin was first partially characterized by isolating moldy corn on which the fungi had grown. Although its lethal dose was determined shortly after the isolation of the chemical, details of its toxic effects were not fully clarified until 1982 in a study with mice, rats, anesthetized cats and preparations of isolated rat auricles.

References

  1. ↑ "GSD Species Synonymy: Penicillium roqueforti Thom". Species Fungorum. CAB International. Archived from the original on 10 March 2021. Retrieved 27 May 2015.
  2. ↑ Westling R. (1911). "Über die grünen Spezies der Gattung Penicillium". Arkiv før Botanik (in German) (1): 71.
  3. ↑ Biourge P. (1923). "Les moissisures du groupe Penicillium Link". La Cellule (in French). 33: 7–331 (see pp. 203–4).
  4. ↑ Dattilo-Rubbo S. (1938). "The taxonomy of fungi of blue-veined cheese". Transactions of the British Mycological Society. 22 (1–2): 174–81. doi:10.1016/s0007-1536(38)80015-2.
  5. ↑ Thom C. (1909). "Fungi in cheese ripening; Camembert and Roquefort". U.S.D.A. Bureau of Animal Industry Bulletin. 82: 1–39 (see p. 36).
  6. ↑ Boysen M, Skouboe P, Frisvad J, Rossen L (1996). "Reclassification of the Penicillium roqueforti group into three species on the basis of molecular genetic and biochemical profiles". Microbiology. 142 (3): 541–9. doi: 10.1099/13500872-142-3-541 . PMID   8868429.
  7. ↑ Cheeseman K, Ropars J, Renault P, et al. (2014). "Multiple recent horizontal transfers of a large genomic region in cheese making fungi". Nature Communications. 5: 2876. Bibcode:2014NatCo...5.2876C. doi:10.1038/ncomms3876. PMC   3896755 . PMID   24407037.
  8. ↑ O'brien M, Egan D, O'kiely P, Forristal PD, Doohan FM, Fuller HT (August 2008). "Morphological and molecular characterisation of Penicillium roqueforti and P. paneum isolated from baled grass silage". Mycol. Res. 112 (Pt 8): 921–32. doi:10.1016/j.mycres.2008.01.023. PMID   18554890.
  9. ↑ Raper KB, Alexander DF, Coghill RD (December 1944). "Penicillin: II. Natural Variation and Penicillin Production in Penicillium notatum and Allied Species". J. Bacteriol. 48 (6): 639–59. doi:10.1128/JB.48.6.639-659.1944. PMC   374019 . PMID   16560880.
  10. ↑ Raper KB (1957). "Nomenclature in Aspergillus and Penicillium". Mycologia. 49 (5): 644–662. doi:10.2307/3755984. JSTOR   3755984.
  11. ↑ Samson RA, Gams W (1984). "The taxonomic situation in the hyphomycete genera Penicillium, Aspergillus and Fusarium". Antonie van Leeuwenhoek. 50 (5–6): 815–24. doi:10.1007/BF02386244. PMID   6397143. S2CID   7084024.
  12. ↑ Ropars J, Dupont J, Fontanillas E, Rodríguez de la Vega RC, Malagnac F, Coton M, Giraud T, López-Villavicencio M (2012). "Sex in cheese: evidence for sexuality in the fungus Penicillium roqueforti". PLOS ONE. 7 (11): e49665. Bibcode:2012PLoSO...749665R. doi: 10.1371/journal.pone.0049665 . PMC   3504111 . PMID   23185400.
  13. ↑ Ropars J, López-Villavicencio M, Dupont J, Snirc A, Gillot G, Coton M, Jany JL, Coton E, Giraud T (2014). "Induction of sexual reproduction and genetic diversity in the cheese fungus Penicillium roqueforti ". Evolutionary Applications. 7 (4): 433–41. doi:10.1111/eva.12140. PMC   4001442 . PMID   24822078. Open Access logo PLoS transparent.svg
  14. ↑ Kinsella JE, Hwang DH (November 1976). "Enzymes of Penicillium roqueforti involved in the biosynthesis of cheese flavour". Crit Rev Food Sci Nutr. 8 (2): 191–228. doi:10.1080/10408397609527222. PMID   21770.
  15. ↑ Zafer Erbay; Pelin Salum; Kieran N. Kilcawley (2021). "Enzyme Modified Cheese". Agents of Change: Enzymes in Milk and Dairy Products. Food Engineering Series. doi:10.1007/978-3-030-55482-8. ISBN   978-3-030-55481-1. S2CID   231671267.
  16. ↑ Raines, Jason (1 August 2012). Factors Affecting the Production of Concentrated Blue Cheese Flavorings (MSc). Clemson University.
  17. ↑ (Sharpell, 1985)
  18. ↑ Möller, T.; Akerstrand, K.; Massoud, T. (1997). "Toxin-producin species of Penicillium and the development of mycotoxins in must and homemade wine". Nat. Toxins. 5 (2): 86–9. doi:10.1002/(SICI)(1997)5:2<86::AID-NT6>3.0.CO;2-7. PMID   9131595.
  19. ↑ Finoli C, Vecchio A, Galli A, Dragoni I (February 2001). "Roquefortine C occurrence in blue cheese". Journal of Food Protection . 64 (2): 246–51. doi: 10.4315/0362-028x-64.2.246 . PMID   11271775.
  20. 1 2 Erdogan A, Sert S (March 2004). "Mycotoxin-forming ability of two Penicillium roqueforti strains in blue moldy tulum cheese ripened at various temperatures". Journal of Food Protection . 67 (3): 533–5. doi: 10.4315/0362-028X-67.3.533 . PMID   15035369.
  21. ↑ O'Brien M, Nielsen KF, O'Kiely P, Forristal PD, Fuller HT, Frisvad JC (November 2006). "Mycotoxins and other secondary metabolites produced in vitro by Penicillium paneum Frisvad and Penicillium roqueforti Thom isolated from baled grass silage in Ireland" (PDF). Journal of Agricultural and Food Chemistry . 54 (24): 9268–76. doi:10.1021/jf0621018. PMID   17117820. S2CID   8916694.
  22. ↑ Proctor RH, Hohn TM (February 1993). "Aristolochene synthase. Isolation, characterization, and bacterial expression of a sesquiterpenoid biosynthetic gene (Ari1) from Penicillium roqueforti". Journal of Biological Chemistry . 268 (6): 4543–8. doi: 10.1016/S0021-9258(18)53644-9 . PMID   8440737. Archived from the original on 25 September 2019. Retrieved 3 December 2008.
  23. ↑ Chen FC, Chen CF, Wei RD (1982). "Acute toxicity of PR toxin, a mycotoxin from Penicillium roqueforti". Toxicon. 20 (2): 433–41. doi:10.1016/0041-0101(82)90006-X. PMID   7080052.
  24. ↑ Siemens, Zawitowski J (1993). "Occurrence of PR imine, a metabolite of Penicillium roqueforti, in blue cheese". Journal of Food Protection . 56 (4): 317–319. doi: 10.4315/0362-028X-56.4.317 . PMID   31091623.
  25. ↑ Nielsen KF, Dalsgaard PW, Smedsgaard J, Larsen TO (April 2005). "Andrastins A-D, Penicillium roqueforti Metabolites consistently produced in blue-mold-ripened cheese". Journal of Agricultural and Food Chemistry . 53 (8): 2908–13. doi:10.1021/jf047983u. PMID   15826038.
  26. ↑ SCBT. "Roquefortine - A potent neurotoxin produced most notably by Penicillium species". Archived from the original on 16 March 2016. Retrieved 17 May 2013.{{cite journal}}: Cite journal requires |journal= (help)
  27. ↑ "Penicillium roqueforti Final Risk Assessment". United States Environmental Protection Agency. 29 April 2015. Archived from the original on 24 September 2015. Retrieved 17 May 2013.
  28. ↑ Larroche C, Arpah M, Gros JB (1989). "Methyl-ketone production by Ca-alginate/Eudragit RL entrapped spores of Penicillium roqueforti". Enzyme and Microbial Technology . 11 (2): 106–112. doi:10.1016/0141-0229(89)90068-9.
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