Saturday, 9 February 2019

Toxins of Penicillium

Toxins of Penicillium

The chaetoglobosins are toxic compounds that may be involved in mycotoxicosis. They are produced by common food-borne Penicillia and have been found to occur naturally (Andersen et al., 2004).Major sources. Penicillium expansum and P. discolor are major sources of the chaetoglobosins. Both species cause spoilage in fruits and vegetables, and the latter species also occurs on cheese (Frisvadand Samson, 2004b). Minor sources. Chaetomium globosum and P. marinum are probably not of significance in foods.

Citreoviridin was reported as a cause of acute cardiac beriberi (Ueno, 1974), but a more in depth toxicological evaluation of this metabolite is needed. It has been associated with yellow rice disease,but this disease has also been associated with P. islandicum and its toxic metabolites cyclic peptides cyclochlorotine and islanditoxin, and anthraquinones luteoskyrin and rugulosin (Enomoto and Ueno, 1974).

Major sources. Eupenicillium cinnamopurpureum has been found in cereals in USA and in Slovakia (Labuda and Tancinova, 2003) and is an efficient producer of citreoviridin. P. citreonigrum may be of some importance in yellowed rice. Minor sources. P. smithii, P. miczynskii and P. manginii (Frisvad and Filtenborg, 1990) have most often been recovered from soil and only rarely from foods. Aspergillus terreus has occasionally been reported from foods, but is primarily a soil-borne fungus.

Citrinin is a nephrotoxin, but probably of less importance than ochratoxin A (Reddy and Berndt, 1991), however, producers of citrinin are widespread and common in foods. Citrinin has been found in cereals, peanuts and meat products (Reddy and Berndt, 1991). Major sources. P. citrinum is an efficient and consistent producer of citrinin and has been found in foods world-wide (Pitt and Hocking, 1997). P. verrucosum is predominantly cereal-borne in Europe and often produces citrinin as well as ochratoxin A (Frisvad et al., 2005b). P. expansum, common in fruits and other foods, sometimes produces citrinin. P. radicicola is commonly found in onions, carrots and potatoes (Overy and Frisvad, 2003). Minor sources. Aspergillus terreus, A. carneus, P. odoratum and P. westlingii have been reported as producers of citrinin, but are not likely to occur often in foods.

Cyclopiazonic acid
Major sources. Penicillium commune and its domesticated form P. camemberti, and the closely related species P. palitans, are common on cheese and meat products and may produce cyclopiazonic acid in these products (Frisvad et al., 2004c). P. griseofulvum is also a major producer of cyclopiazonic acid, and may occur in long stored cereals and cereal products such as pasta (Pitt and Hocking, 1997). Minor sources. P. dipodomyicola occurs in the environs of the kangaroo rat in the USA, but has also been reported from rice in Australia and in a chicken feed mixture in Slovakia (Frisvad and Samson, 2004b).

Mycophenolic acid
Despite having a low acute toxicity, mycophenolic acid may be a very important indirect mycotoxin as it highly immunosuppressive, perhaps influencing the course of bacterial and fungal infections (Bentley, 2000). Major sources. Penicillium brevicompactum is a ubiquitous species and may produce mycophenolic acid in foods, e.g. ginger (Overy and Frisvad, 2005). Two other major species producing mycophenolic acid are P. roqueforti and P. carneum. Another important producer is Byssochlamys nivea (Puel et al., 2005). Mycophenolic acid has been found to occur naturally in blue cheeses (Lafont et al., 1979). Minor sources. The soil-borne species Penicillium fagi also produces mycophenolic acid (Frisvad and Filtenborg, 1990, as P. raciborskii). Septoria nodorum (Devys et al., 1980) is another source but is unimportant as a food contaminant.

Ochratoxin A
Major sources. Penicillium verrucosum (Frisvad, 1985; Pitt, 1987) is the major producer of ochratoxin A in cool climate stored cereals (Lund and Frisvad, 2003). Penicillium nordicum (Larsen et al., 2001) is the main OA producer found in manufactured meat products such as salami and ham. Both OA producing Penicillium species have been found on cheese also, but have only been reported to be of high occurrence on Swiss hard cheeses (as P. casei Staub, 1911). The ex type culture of P. casei is a P. verrucosum (Larsen et al., 2001).

Patulin is generally very toxic for both prokaryotes and eukaryotes, but the toxicity for humans has not been conclusively demonstrated. Several countries in Europe and the USA have now set limits on the level of patulin in apple juice. Major sources. Penicillium expansum is by far the most important source of patulin. P. expansum is the major species causing spoilage of apples and pears, and is the major source of patulin in apple juice and other apple and pear products.

Byssochlamys nivea may be present in pasteurised fruit juices and may produce patulin and mycophenolic acid (Puel et al., 2005). Penicillium griseofulvum is a very efficient producer of high levels of patulin in pure culture, and it may potentially produce patulin in cereals, pasta and similar products. P. carneum may produce patulin in beer, wine, meat products and rye-bread as it has been found in those substrates (Frisvad and Samson, 2004b), but there are no reports yet on patulin production by this species in those foods. P. carneum also produces mycophenolic acid, roquefortine C and penitrem A (Frisvad et al., 2004c). P. paneum occurs in ryebread (Frisvad and Samson, 2004b), but again actual production of patulin in this product has not been reported. P. sclerotigenum is common in yams and has the ability to produce patulin in laboratory cultures.

Minor sources. The coprophilous fungi P. concentricum, P. clavigerum, P. coprobium, P. formosanum, P. glandicola, P. vulpinum, Aspergillus clavatus, A. longivesica and A. giganteus are very efficient producers of patulin in the laboratory, but only A. clavatus may play any role in human health, as it may be present in beer malt (LopezDiaz and Flannigan, 1997). Aspergillus terreus, Penicillium novae-zeelandiae, P. marinum, P. melinii and other soil-borne fungi may produce patulin in pure culture, but are less likely to occur in any foods.

Penicillic acid
Penicillic acid (Alsberg and Black, 1911) and dehydropenicillic acid (Obana et al., 1995) are small toxic polyketides, but their major role in mycotoxicology may be in their possible synergistic toxic effect with OA (Lindenfelser at al., 1973; Stoev et al., 2001) and possible additive or synergistic effect with the naphtoquinones hepatotoxins xanthomegnin, viomellein and vioxanthin.

Major sources. Penicillic acid is likely to co-occur with OA, xanthomegnin, viomellein and vioxanthin produced by members of Aspergillus section Circumdati and Penicillium series Viridicata (which often co-occur with P. verrucosum). The Aspergillus species often occur in coffee and the Penicillia are common in cereals. The major sources of penicillic acid are P. aurantiogriseum, P. cyclopium, P. melanoconidium and P. polonicum (Frisvad and Samson, 2004b) and all members of Aspergillus section Circumdati (Frisvad and Samson, 2000). Penicillic acid is produced by P. tulipae and P. radicicola, which are occasionally found on onions, carrots and potatoes (Overy and Frisvad, 2003). Minor sources. Penicillic acid has been found in one strain of P. carneum (Frisvad and Samson, 2004b).

Penitrem A
Penitrem A is a highly toxic tremorgenic indol-terpene. It has primarily been implicated in animal mycotoxicoses (Rundberget and Wilkins, 2002), but has also been suspected to cause tremors in humans (Cole et al., 1983; Lewis et al., 2005). Major sources. Penicillium crustosum is the most important producer of penitrem A (Pitt, 1979). This species is of world-wide distribution and often found in foods. This mycotoxins is produced by all isolates of P. crustosum examined (Pitt, 1979; Sonjak et al., 2005). P. melanoconidium is common in cereals (Frisvad and Samson, 2004b), but it is not known whether this species can produce penitrem A in infected cereals. Minor sources. P. glandicola, P. clavigerum, and P. janczewskii are further producers of penitrem A (Ciegler and Pitt, 1970; Frisvad and Samson, 2004b; Frisvad and Filtenborg, 1990), but have been recovered from foods only sporadically.

PR toxin
PR toxin is a mycotoxin that is acutely toxic and can damage DNA and proteins (Moule et al., 1980; Arnold et al., 1987). It is unstable in cheese (Teuber and Engel, 1983), but it may be produced in silage and other substrates. Major sources. Penicillium roqueforti is the major source of PR toxin. It has been reported also from P. chrysogenum (Frisvad and Samson, 2004b).

Roquefortine C
The status of roquefortine C as a mycotoxin has been questioned, but it is a very widespread fungal metabolite, and is produced by a large number of species. The acute toxicity of roquefortine C is not very high (Cole and Cox, 1981), but it has been reported as a neurotoxin. Major sources. Penicillium albocoremium, P. atramentosum, P. allii, P. carneum, P. chrysogenum, P. crustosum, P. expansum, P. griseofulvum, P. hirsutum, P. hordei, P. melanoconidium, P. paneum, P. radicicola, P. roqueforti, P. sclerotigenum, P. tulipae and P. venetum are all producers that have been found in foods, but the natural occurrence of roquefortine C has been reported only rarely.

Rubratoxin is a potent hepatotoxin (Engelhardt and Carlton, 1991) and is of particular interest as it has been implicated in severe liver damage in three Canadian boys, who drank rhubarb wine contaminated with Penicillium crateriforme. One of the boys needed to have the liver transplanted (Richer et al., 1997). Major producers. P. crateriforme is the only known major producer of rubratoxin A and B (Frisvad, 1989).

Secalonic Acid D
The toxicological data on secalonic acid D and F are somewhat equivocal (Reddy and Reddy, 1991), so the significance of this metabolite in human and animal health is somewhat uncertain. Major sources. Claviceps purpurea, Penicillium oxalicum, Phomaterrestris and Aspergillus aculeatus produce large amounts of secalonic acid D and F in pure culture. Secalonic acid D has been found to occur in grain dust in USA (Palmgren, 1985; Reddy and Reddy, 1991)

Verrucosidin is a of the mycotoxin from species in Penicillium series Viridicata that has been claimed to cause mycotoxicosis in animals (Burka et al., 1983). Major sources. Penicillium polonicum, P. aurantiogriseum and P. melanoconidium are the major known sources of verrucosidin (Frisvad and Samson, 2004b).

Xanthomegnin, Viomellein and Vioxanthin
These toxins have been reported to cause experimental mycotoxicosis in pigs and they apparently are more toxic to the liver than to kidneys in mammals (Zimmerman et al., 1979). They have been found
to be naturally occurring in cereals (Hald et al., 1983; Scudamore et al., 1986). Major sources. P. cyclopium, P. freii, P. melanoconidium, P. tricolor and P. viridicatum are common in cereals. A. ochraceus, A. wester dijkiae and possibly A. steynii are common in green coffee beans and are occasionally found in grapes and on rice. Minor sources. P. janthinellum and P. mariaecrucis are soil-borne species producing these hepatotoxins (Frisvad and Filtenborg, 1990).

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