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Secondary Metabolites from Penicillium Roqueforti, a Starter for the Production of Gorgonzola Cheese

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Secondary Metabolites from Penicillium Roqueforti, a Starter for the Production of Gorgonzola Cheese Italian Journal of Food Safety 2014; volume 3:2118 Secondary metabolites from agents in the food industry. Penicillium roqueforti , a species especially Correspondence: Lisa Vallone, Dipartimento di Penicillium roqueforti , a starter known for its involvement in silage contamina - Scienze Veterinarie per la Salute, la Produzione for the production of tions, is also commonly involved in the spoila - Animale e la Sicurezza Alimentare, Università di ge of hard, semi-hard and soft-cheeses Milano, via Grasselli 7, 20137 Milan, Italy. Gorgonzola cheese Tel. +39.02.50318511 - Fax: +39.02.50318501. (Filtenborg et al ., 1996; Kure and Skaar, 2000; E-mail: [email protected] Lisa Vallone, 1 Alberto Giardini, 2 Kure et al ., 2004). However, selected strains of Gabriella Soncini 1 P. roqueforti are used in food manufacture and Key words: Cheese, Penicillium roqueforti , play a decisive role in the ripening of some Roquefortine C, PR toxin, Mycophenolic acid. 1Dipartimento di Scienze Veterinarie per cheeses, such as Gorgonzola, Roquefort, la Salute, la Produzione Animale e la Stilton and Danablu. Inoculating the milk with Conflict of interests: the authors declare no Sicurezza Alimentare, Università di potential conflict of interests. pure cultures of P. roqueforti is essential to Milano; 2Centro Sperimentale del Latte obtain the characteristic flavours and aromas S.r.l., Zelo Buon Persico (LO), Italy Received for publication: 18 November 2013. of these cheeses, due to the strong lipolytic Revision received: 27 January 2014. activity of the moulds and to the production of Accepted for publication: 27 January 2014. short chain fatty acids (acetic, butyric, capry - lic, and caproic acid). Fatty acids are oxidised This work is licensed under a Creative Commons Abstract to produce methylketone, which improves fla - Attribution 3.0 License (by-nc 3.0). vour (Caridi, 1996; Tiecco, 2001). Typically, in ©Copyright L. Vallone et al., 2014 The presence of mold in food, although spicy Gorgonzola and blue cheeses production, Licensee PAGEPress, Italy necessary for production, can involve the pre - P. roqueforti is used as a unique culture. In Italian Journal of Food Safety 2014; 3:2118 sence of secondary metabolites, which are sweet Gorgonzola production, P. glabrum and P. doi:10.4081/ijfs.2014.2118 sometimes toxic. Penicillium roqueforti is a crustosum cultures are used on their own or in common saprophytic fungus but it is also the association with P. roqueforti . The use of diffe - essential fungus used in the production of rent mixtures of Penicilli confers the blue- Roquefort cheese and other varieties of blue green marbling characteristics and creami - PR-toxin cheese containing internal mold. The study ness of each particular cheese (Finoli et al ., PR-toxin is one of the metabolites produced was conducted on industrial batches of 2001). However, some species of Penicillium by P. roqueforti having acute toxicity (Scott, Penicillium roqueforti starters used in the pro - can produce toxic metabolites. The toxigenici - 1984): it is lethal to rats, mice, and cats and is duction of the Gorgonzola cheese, with the aim ty of Penicillium species is known about since mutagenic in the Ames test (Fog Nielsen et al ., to verify the production of secondary metaboli - 1913, when penicillic acid was isolated from 2006). In mice, the ip LD 50 is 5.8 mg/kg (Chen tes. Nine Penicillium roqueforti strains were cultures of P. puberulum Bain (Frisvad and et al ., 1982). It has often been found in mar - tested. The presence of roquefortine C, PR Filtemborg, 1989). P. roqueforti is known to bled cheeses (Wei et al ., 1985). Polonelli et al . toxin and mycophenolic acid was tested first in produce the following toxins: roquefortine C, (1982) speculate that microaerophilic condi - vitro , then on bread-like substrate and lastly in PR-toxin, patulin, penicillic acid, mycophenolic tion prevails in most cheeses, which may vivo in nine cheese samples produced with the explain why the PR-toxin is not generally same starters and ready to market. In vitro , acid and isofumigaclavine A and B (Frisvad et al ., 2004; O’Brien et al ., 2006). found in the final product. However, PR-toxin only Penicillium out of nine produced roque - is unstable because it quickly reacts with fortine C, four starters showed mycophenolic Roquefortine C nitrogen compounds such as ammonia and acid production, while no significant amounts Roquefortine is an alkaloid with neurotoxic ammonia salts, amino acids (lysine and cystei - of PR toxin were detected. In the samples activity that causes paralysis in guinea pigs. ne), amines, casein and the decomposition grown on bread-like substrate, Penicillium did Roquefortine has antibacterial properties and products resulting in a less toxic PR imine not produce secondary metabolites, likewise is Ames test negative. There are no studies of (Erdogan et al ., 2003). with each cheese samples tested. To protect its toxicity in laboratory animals that meet consumers’ health and safety, the presence of Patulin good laboratory practice standards. Older data mycotoxins needs to be verified in food which Patulin is a toxic secondary metabolite pro - suggest roquefortine toxicity (ip) is in the is widely consumed, above all for products pro - duced by certain species of the genera tected by the protected denomination of origin range of 15-100 mg/kg of body weight (Scott, Aspergillus , Penicillium , and Byssochlamys . It (DOP) label ( i.e. a certificate guaranteeing the 1984). Arnold et al . (1987) report an oral LD 50 is considered neurotoxic, embryotoxic and geographic origin of the product), such as of 169 mg/kg in male and 184 mg/kg in female teratogenic (Dombrink-Kurtzman and Gorgonzola cheese. CR57 mice and a similar value for male and Blackburn, 2005) and has been classified by female Swiss Webster mice. The data on neu - IARC as category 3 unclassifiable as to carcino - rotoxicity of roquefortine are equivocal (Fog genicity in humans ; the evidence for carcino - Nielsen et al ., 2006). Several studies have genicity of patulin in experimental animals is Introduction revealed the presence of roquefortine C in considered inadequate and the results of geno - blue-veined cheeses (Ohmomo et al ., 1975; toxicity tests are non-conclusive (IARC, 1986). The genus Penicillium is widespread in Scott and Kennedy, 1976; Ware et al ., 1980; The carcinogenic activity in different animal nature and grows in many different habitats. López-Díaz, 1996). Finoli et al . (2001) reported models is still the subject of some controversy Most Penicilli are ubiquitous and generally roquefortine C concentrations ranging from 50 (Schumacher et al ., 2006). The LD 50 of patulin they are saprophytic organisms with signifi - to 1470 µg/kg after analysis of 30 blue-cheeses. ranges from 15 to 25 mg/kg and varies with cant usage in the industrial mycology for anti - Kokkonen et al . (2005) showed that the con - animal species and route of exposure (Yang et biotics (such as penicillin and griseofulvin) centration of this metabolite ranged from 600 al ., 2014). Few studies on the presence of this and enzymes (such as ribonuclease) produc - to 12,000 µg/kg in 9 blue cheeses. mycotoxin in cheese have been published: by tion, but they are also known as spoilage Spanish (López-Diaz et al ., 1996), by Turkish [page 173 ] [Italian Journal of Food Safety 2014; 3:2118] Article (Erdogan et al ., 2003) and by Italian resear - cheese (O’Connor and O’Brien, 2000). Based The lower secondary metabolite-containing chers (Pattono et al ., 2013). on these bibliographic evidence, the aim of methanol phase was filtered through disposa - this study was to evaluate the potential produc - ble filters (0.45 μm) before injection. Several Penicillic acid tion of secondary metabolites by fungal star - alkylphenones (acetophenone, propiopheno - Penicillic acid is a lactone substance and ters used in the production of Gorgonzola ne, butyrophenone, hexanophenone, valero - possesses a wide range of toxic properties cheese. phenone, octanophenone, decanophenone; including carcinogenicity (Klari Šegvi et al ., Sigma Aldrich, St. Louis, MO, USA) are used as 2013). However, IARC classified penicillic acid internal standards and are injected on a 100 as belonging to Group 3, which means that mm x 4 mm I.D. Nucleosil 5 μm C 18 column penicillic acid is not carcinogen to humans Materials and Methods (Waters Corporation, Milford, MA, USA) of (IARC, 1998). Studies on experimental ani - HPLC with diode-arrays detector (Hplc and mals revealed that penicillic acid induces The study was conducted on nine industrial diode- arrays detector system; Shimadzu, significant hepatobiliary excretory dysfunction batches of five Penicillium roqueforti starters Kyoto, Japan), initially in pure form and then in mouse and rats, while it did not provoke used in the production of the Gorgonzola chee - mixed at the fungal extract of each plate. The significant damage to internal organs in chic - se. The batches were all produced by the Centro mobile phases are the same pointed out by kens. The toxin has a LD of 100 mg/kg by sub - 50 Sperimentale del Latte S.r.l. [(Zelo Buon Frisvad (Frisvad and Thrane, 1987). All meta - cutaneous injection in mice (Sansing et al ., Persico (LO), Italy)] and were named: PV bolites were detected at 225 nm. 1976). The production of penicillic acid has 11104, NON 11203, PV 10704, NOC 09203, NON Both for detected alkylphenones and secon - been highlighted in two strains out of six 10803, NON 10804, NOPC 09103, NOPC 10902, dary metabolites, the retention index (RI) is selected among fungal isolates from Cheddar and PY 10604. The strains composition of each calculated from the following equation: cheese starter (Moubasher et al ., 1978). of the five starters (PV, NON, NOC, NOPC, and Mycophenolic acid PY) was characterised by PCR technique (data Mycophenolic acid is a metabolite produced not shown). The P. roqueforti metabolites of by P. roqueforti and other species of Penicillium interest were: PR toxin, roquefortine C and where Tsm=retention time of the secondary (Lafont et al ., 1979).
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