EJBR2017v7i3art207-222 ISSN 2449-8955 European Journal of Biological Research Review Article European Journal of Biological Research 2017; 7 (3): 207-222 Incidence and significance of black aspergilli in agricultural commodities: a review, with a key to all species accepted to-date M. A. Ismail Department of Botany and Microbiology, Faculty of Science, Assiut University, P.O. Box 71526, Assiut, Egypt Assiut University Mycological Centre, Assiut University, P.O. Box 71526, Assiut, Egypt E-mail: ismailmady60@yahoo.com ABSTRACT Black aspergilli (Aspergillus species of Section Nigri) present dark colonies, often black, and uniseriate or biseriate conidial heads. Currently 26 species and one variety are accepted within this section. They have been isolated from a wide variety of food worldwide and are considered as common causes of food spoilage and biodeterioration of other materials. They are commonly present in cereals and vineyards and have the ability to cause Aspergillus rot of black berry. Some species of this section, like A. niger and A. awamori, are a common source of extracellular enzymes such as amylases and lipases, and organic acids, such as citric and gluconic acid, used as additives in food processing and are used for biotechnological purposes. These products hold the GRAS (Generally Recognised as Safe) status. Other species are able to produce ochratoxins (OTA) and fumonisins. This review briefly shedlighted on the taxonomy of this important group of Aspergillus along with the species incidence, mycotoxin production in agricultural commodities as well as their significance as plant pathogens. A provisional key for identification (based on phenotypic characteristics) is provided for all described species to-date. Keywords: Ochratoxins; Fumonisins; Biotechnology; Aspergillus carbonarius; Cereals; Grapes. 1. TAXONOMICAL OVERVIEW Thom and Raper [1] and Raper and Fennell [2] published major monographic treatments on the genus Aspergillus and respectively accepted 89 and 150 species. Now the genus comprises 339 species [3] or 344 [4]. Many of these species can be conveniently separated into several distinct morphospecies, and several of these are based on colors according to the earlier classification [2]. However, phylogenetic analyses of sequence data resulted in separating the Aspergillus genus into eight subgenera [5]. Following these analyses, the economically important species that produce the ochratoxins were divided to include those species of the subgenus Circumdati, the sections Circumdati (=Aspergillus ochraceus group) and Nigri (A. niger group). There are no known teleomorphic species of section Nigri. In recent years, members of the Aspergillus section Nigri have undergone an Received: 04 April 2017; Revised submission: 14 July 2017; Accepted: 24 July 2017 Copyright: © The Author(s) 2017. European Journal of Biological Research © T.M.Karpiński 2017. This is an open access article licensed under the terms of the Creative Commons Attribution Non-Commercial 4.0 International License, which permits unrestricted, non-commercial use, distribution and reproduction in any medium, provided the work is properly cited. DOI: http://dx.doi.org/10.5281/zenodo.834504 208 | Ismail Incidence and significance of black aspergilli in agricultural commodities European Journal of Biological Research 2017; 7 (3): 207-222 extensive taxonomic revision resulting in several new taxa. Mosseray [6] described 35 black aspergilli species, while Raper and Fennell [2] reduced this number to 12. Later, Al-Musallam [7] revised the taxonomy of the A. niger group and recognized seven species, based on morphological features, and described A. niger as an aggregate consisting of seven varieties and two formae. The black Aspergillus species were classified into the Section Nigri in the subgenus Circumdati by Gams et al. [8], formerly ‘A. niger species group’ by Raper and Fennell [2]. They present dark colonies, often black, and uniseriate or biseriate conidiophores. In 1989, Kozakiewicz [9] suggested 17 taxa in the A. niger group and distinguished two groups: echinulate and verrucose, depending on their conidial ornamen- tations. In the past, it was very common that all Aspergillus isolates developing black colonies were identified as A.niger by non-taxonomists, because of the similarities in morphology. To solve this problem, Abarca et al. [10] published a review in the taxonomy of black aspergilla and proposed an identification key to distinguish the most common taxa based on uniseriate and biseriate character of the conidial heads. A provisional key of section Nigri, based on phenotypic characteristics, extrolites and β-tubulin sequencing, was also proposed [11] who accepted 15 species in this section: A. aculeatus, A. brasilensis, A. carbonarius, A. costaricaensis, A. ellipticus, A. foetidus, A. heteromorphus, A. homomorphus, A. japonicus, A. lacticoffeatus, A. niger, A. piperis, A. sclero- tioniger, A. tubingensis and A. vadensis. Later on some more new species were described: A. ibericus [12], A. aculeatinus, A. sclerotiocarbonarius [13], A. uvarum [14], A. saccharolyticus [15]. Also in 2011, 4 additional species were described: A. fijien- sis, A. indologenus, A. eucalypticola, A. neoniger and 2 others were validated; A. violaceofuscus and A. acidus, however A. foetidus was synonymized to A. niger based on molecular and physiological data and 2 other species described previously, A. coreanus and A. lacticoffeatus, were found to be colour mutants of A. acidus and A. niger, respectively [16]. Also in the study of Hubka and Kolarik [17] on β-tubulin paralogue tubC, stated that A. japonicus should be treated as a synonym with A. violaceofuscus, and A. fijiensis is reduced to synonymy with A. brunneoviolaceus. In 2012, two uniseriate species were described from indoor air (A. floridensis and A. trinidadensis) and A. fijien- sis was confirmed as a synonym with A. brunneo- violaceus [18]. Currently and after these revisions, Aspergillus section Nigri is considered to comprise 26 defined species and one variety [5, 10, 11, 13, 14, 16-19] (refer to Table 1), although it remains under investigation, which may result in further changes. 2. DISTRIBUTION AND INCIDENCE OF THE BLACK ASPERILLI IN AGRICULTURAL COMMODITIES It was indicated that most members of the genus Aspergillus occurred in the tropical latitudes below 25 degree north and south, with greater than expected frequencies in the subtropical to warm temperate zones at latitudes between 26 and 35 degrees [20]. Also, it was suggested that species abundance peaked in the subtropics is attributed to several biotic and abiotic interacting factors with the major factor temperature [20]. In general, the black species of aspergilli (particularly A. niger var. niger) were found to occur more frequently in forest and cultivated soils and less frequency in desert soils [20, 21]. A.niger is one of the most common species of the genus Aspergillus. It is one of the fungi that have been labelled with the GRAS (generally recognized as safe) status from the US Food and Drug Administration [22]. But instead of the safe categorization, A. niger has been found to be an opportunistic reason for infections of humans. If inhaled, in sufficient quantity it can cause severe lung problems i.e., aspergillosis in humans. It is also associated with various plant diseases resulting in huge economic loss. It is also reported to produce ochratoxin A and fumonisin B2 in stored commo- dities [10, 23]. Black Aspergillus species were found as dominant in almost all agricultural commodities in all continents such as cereals (maize, wheat, barley, sorghum, millet, rye, oat, etc.), cereal products, beans, nuts (peanuts, almond and hazelnuts, coconut etc.), grape and grape products, fruits and fruit juices, and vegetables (refer to Table 2). 209 | Ismail Incidence and significance of black aspergilli in agricultural commodities European Journal of Biological Research 2017; 7 (3): 207-222 Table 1. List of species accepted to-date (ordered alphabetically). 1. A. aculeatinus Noonim, Frisvad, Varga & Samson 2008 2. A. aculeatus Lizuka 1953 3. A. brasiliensis Varga, Frisvad & Samson 2007 4. A. brunneoviolaceus Bat. & H. Maia 1955 (=A. fijiensis Varga, Frisvad & Samson 2011) 5. A. carbonarius (Bainier) Thom 1916 6. A. ellipticus Raper & Fennell 1965 7. A. eucalypticola Varga, Frisvad & Samson 2011 8. A. floridensis Ž. Jurjević, G. Perrone & S.W. Peterson 2012 9. A. helicothrix Al-Musallam 1980 10. A. heteromorphus Batista & Maia 1957 11. A. homomorphus Steiman, Guiraud, Sage & Seigle-Mur. ex Samson & Frisvad 2004 12. A. ibericus Serra, Cabanes & Perrone 2006 13. A. indologenus Frisvad, Varga & Samson 2011 14. A. luchuensis Inui 1901 (=A. acidus Kozak. 1989, =Aspergillus awamori Nakaz 1907) 15. A. neoniger Varga, Frisvad & Samson 2011 16. A. niger van Tieghem 1867 (=A. foetidus Thom & Raper 1945) 17. A. niger var. taxi Zhou, Zhao & Ping 2009 18. A. piperis Samson & Frisvad 2004 19. A. saccharolyticus Sørensen, Lubeck & Frisvad 2011 20. A. sclerotiocarbonarius Noonim, Frisvad, Varga & Samson 2008 21. A. sclerotioniger Samson & Frisved 2004 22. A. trinidadensis Ž. Jurjević, G. Perrone & S. W. Peterson 2012 23. A. tubingensis (Schober) Mosseray 1934 24. A. uvarum Perrone, Varga & Kozakiewicz 2007 25. A. vadensis Samson, de Vries, Frisvad & Visser 2005 26. A. violaceofuscus Gasperini 1887 (=A. japonicus Saito 1906) 27. A. welwitschiae (Bres.) Henn. apud Wehmer 1907 (=A. awamori sensu Perrone et al. 2011) 3. OCHRATOXIN PRODUCTION IN AGRI- CULTURAL COMMODITIES AND BY THE ASSOCIATED BLACK ASPERGILLI Ochratoxin A (OTA, Fig. 1) is a very strong nephrotoxin and potential carcinogen, teratogenic and immunosuppressive, classified as Group 2B by the International Agency for Research on Cancer [60]. The Joint FAO/WHO Expert Committee on Food Additives (JECFA) established 100 ng kg-1 bw as the tolerable weekly intake (PTWI) recom- mended for OTA [61], which is also regulated by the European Commission. The regulation levels in food and feed products are established at 10 μg kg-1 in dry grapes, 2 μg kg-1 in grape juice, must and wine, and 0.5 μg kg-1 in food for babies and infants. Figure 1. Chemical structure of OTA. 210 | Ismail Incidence and significance of black aspergilli in agricultural commodities European Journal of Biological Research 2017; 7 (3): 207-222 Dichotomous key for identification of species of section Nigri (based on phenotypic characteristics, designed by MA Ismail) 1. Uniseriate (all species with no growth at 40 ºC) …………................................................. 2 1. Biseriate (growth at 40 ºC) …….......................................................................................... 9 2. Versicle size up to 80 µ m or more ……………………….……………............................. 3 2. Versicle size not exceed 45 µ m ……………………………………................................... 7 3. Stipe width up to 30 µ m, conidia 3.5-5 µ m, sclerotia if present cream, up to 0.5 mm diam ..................................................................................................................................... A. aculeatus 3. Stipe width not exceed 20 µ m .……..………………………………….............................. 4 4. Conidia large 4-7(8) x 3.5-7, up to 13 x 10 µ m if from monophialide ............................... A. trinidadensis 4. Conidia small, less than 6 µ m in length ……………………………….............................. 5 5. Conidia 2.5-4.5 µ m, sclerotia if present white to cream, 0.4-0.6 mm diam ….................... A. aculeatinus 5. Conidia smaller, globose to ellipsoidal 3.5-5.0(6) x 3.5-5.0 (5.5) µ m …............................ 6 6. Sclerotia if present buff to orange brown up to 0.8 mm diam …………............................ A. brunneoviolaceus (=A. fijiensis) 6. Sclerotia if present buff yellowish, 0.2-1.1 mm diam ………………................................. A. floridensis 7. Stipe width (5-)10-18 (-24) µm, vesicle 20-30 µ m, conidia globose-ellipsoidal (3-) 4-7 (-9) x 3.0-7.0 µ m, sclerotia if present dark brown to black, 0.5-0.8 mm diam ……….... .. A. uvarum 7. Not as above (stipe width and conidia smaller, vesicles larger) ......................................... 8 8. Stipe width 2-5 µ m, vesicles 10-30 (-45) µ m, conidia 3.5-4.0 x 4.0-5.5 µ m, sclerotia if present white to cream, up to 0.5 mm diam. …................................................................... A. violaceofuscus (=A. japonicas) 8. Stipe width 5-7 µ m, vesicles 25-40 µ m, conidia 5.0-6.2 µ m, sclerotia absent ................... A. saccharolyticus 8. Stipe width 5-11 µ m, vesicles 20-45 µ m, conidia 3-4 µ m, sclerotia absent…………….... A. indologenus 9. Conidial small, never exceed 5µ m………………………………….….............................. 10 9. Conidia large, exceed 5 µ m………………………………………….................................. 20 10. Vesicle not exceed 45 µ m………………………………………………............................ 11 10. Vesicles larger……………………………………………………….................................. 13 11. No growth at 40 ºC, vesicles up to 30 µ m, stipe width not exceed 7 µ m; sclerotia 300- 600 mm diam., white when young …………………………….......................................... A. heteromorphous 11. Growth at 40 ºC, vesicles up to 35 or 45 µ m, stipe width up to 13 or 15 µ m….................. 12 12. Vesicles not exceed 35 µ m, stipe brown to black, short, not exceed 150 µ m, sclerotia absent……………………………………………............................................................... A. vadensis 12. Vesicles up to 45 µ m, stipe pale brown, long, up to 1700 µ m, sclerotia produced by some strains, white ………………………….……............................................................. A. brasiliensis 12. Vesicles 30-55 µ m, stipe hyaline, stipe width 8-14 µ m, sclerotia absent, conidia globose 2.5-3.5 µ m………………………………............................................................................ A. eucalypticola 12. Vesicles 30-50 µ m, stipe hyaline, stipe width 8-12µm, sclerotia absent, conidia 3.5-5.0 µ m ....................................................................................................................................... A. neoniger 12. Vesicle 20-40 µ m, stipe hyaline, stipe width 10-13 (up to 30) µ m, sclerotia absent, conidia 3.5-4.5 µ m ………………………………….......................................................... A. luchuensis (=A.acidus) 13. Sporulation abundant & heavy, vesicles up to 80 µ m………………….............................. 14 13. Sporulation poor …………………………………………………….................................. 18 211 | Ismail Incidence and significance of black aspergilli in agricultural commodities European Journal of Biological Research 2017; 7 (3): 207-222 Dichotomous key for identification of species of section Nigri (based on phenotypic characteristics, designed by MA Ismail) 14. Sclerotia absent…………………………………………………….................................... 15 14. Sclerotia present………………………………………………………............................... 17 15. Stipe length up to 1000 µ m & width up to 12 µ m…………………................................... A. foetidus 15. Stipe width 8-12 µ m, sclerotia absent, vesicle 30-50 µ m ……………............................... A. niger 15. Stipe width up to 14 µ m, conidia 2.5-3.5 µ m ………………………................................. A. eucalypticola 15. Stipe width 10-13 (-30) µ m, conidia 3.5-4.5 µ m, vesicle 20-40 µ m ….............................. A. luchuensis (=A.acidus) 15. Stipe longer, up to 3000 µ m or more, stipe width up to 20 µm or more ............................. 16 16. Stipe smooth, colorless or brownish only in the upper portion; stipe width 15-20 µ m ..... A. niger 16. Stipe very rough, brown on ageing; stipe width 20-33 µ m…………….............................. A. niger var. taxi 16. Stipes longer up to 6000 µ m, smooth to coarse, brownish, stipe width 15-20 (-30) µ m .... A. tubingensis 17. Sclerotia white, 1200-1800 µm; reverse yellow to orange to reddish brown in age, stipe width up to 12 µ m ………………………………............................................................... A. foitidus 17. Sclerotia white to pink to black, 500-800 µ m, reverse white; stipe width 15-20 (30) µ m . A. tubingensis 18. Sclerotia present, yellowish or pinkisk; stipes hyaline………………................................ 19 18. Sclerotia absent, vesicle 40-65 µ m, stipes orange brown………………............................ A. lacticoffeatus 19. Vesicle 40-55 µ m, stipe width 7-10 µ m, metulae 20-35 µ m long …….............................. A. piperis 19. Vesicles 40-80 (-90) µ m; stipe width 12-22 µ m, metulae 30-60 µ m long ……................. A. costaricaensis 20. Growth at 40 ºC, sclerotia absent…………………………….………................................ A. ibericus 20. No growth at 40 ºC…………………………………………………................................... 21 21. Sclerotia absent……………………………………………..………….............................. 22 21. Sclerotia present………………………………………………………............................... 24 22. Conidia strongly ellipsoidal, 7-10 X 2.5-3, spinulose; vesicles 75-100 µ m; stipe long up to 5000-8000 (-1 cm) X 12-20 µ m…………………........................................................... A. ellipticus 22. Conidia not ellipsoidal…………………………………………………............................. 23 23. Stipe width 35-40 µ m, conidia globose, 7-9 µ m, metulae length less than 15 µ m, vesicle 40-80 (-100) µ m………………………………................................................................... A. carbonarius 23. Stipe width9-15 µ m, conidia 5-7 (-9) µ m, metulae length less than 15 µ m, vesicles not exceed 50-65 µ m……………………………….………..................................................... A. homomorphus 24. Sclerotia cup-shaped with coiled setae; stipe width 8.5-13.5 µ m, (with brownish stipe, vesicle, conidia, setae & sclerotia) ………………….......................................................... A. helicothrix 24. Characters not as above…………………………………………….................................... 25 25. Conidia strongly ellipsoidal, 7-10 X 2.5-3 µ m, spinulose, sclerotia dull yellow to brown in age, 500-1500 µ m………………………………............................................................ A. ellipticus 25. Conidia globose………………………………….………………....................................... 26 26. Conidia 4.5-6.5µ m, vesicle pyriform 30-50 µ m, sclerotia yellow to orange to red brown; sporulation poor, stipe width less than 18 µ m …................................................................. A. sclerotioniger 26. Conidia up to 9 µ m; vesicle up to 100 µ m, stipe width wider …………............................ 27 27. Sclerotia yellow to orange to red brown, no growth at 9 ºC, stipe width 13-27 µ m ……………………………………………………………................................................. A. sclerotiocarbonarius 27. Sclerotia pink to yellow, growth at 9 ºC, stipe width 35-40, sporulation abundant ............ A. carbonarius 212 | Ismail Incidence and significance of black aspergilli in agricultural commodities European Journal of Biological Research 2017; 7 (3): 207-222 Table 2. Black aspergilli in agricultural commodities. Commodity Species Country References Grape & grape products A. brasiliensis, A. niger, A. awamori, A. aculeatus, A. tubingensis, A. ibericus, A, carbonarius, A. japonicus, A. uvarum, A. acidus, Worldwide [12, 14, 24-29] Grapes A. carbonarius, A. tubingensis, A. japonicus, A. ibericus, A. niger aggregate Greece [30] Grapes A. carbonarius, A. niger aggregate Italy [31, 32] Wine grapes A. niger var. niger, A. niger var. awamori, A. foetidus Argentina [33] Maize A. japonicus, A. niger var. niger Worldwide [27, 34-36] Maize A. niger aggregate Portugal [37] Maize kernels A. heteromorphus, A. carbonarius, A. aculeatus, A. niger, A. japonicus, A. brasiliesis Kenya [38] Wheat A. niger Egypt [39] Sorghum A. niger Egypt [36] Milled rice A. niger Uganda & Pakistan [40-42] Paddy & mild rice A. niger Uganda [43] Peanuts A. japonicus, A. niger var. niger, A. carbonarius, A. niger var. awamori Worldwide [27, 35, 44] Peanuts A. niger, A. carbonarius Uganda & Kenya [45] Peanuts A. niger Egypt [39] Lentil & sesame A. niger Egypt [36] Coffee bean A. aculeatus, A. aculeatinus, A. carbonarius, A. sclerotiocarbonarius, A. sclerotioniger, A. niger, A. lacticoffeatus, A. japonicus, A. tubingensis Worldwide [11, 27, 35] Coffee beans A. niger group Colombia [46] Coffee beans A. niger, A. carbonarius Saudi Arabia [47] Beans, wheat, millet A. niger Nigeria [48] Cereal products (baby foods) A. niger, A. carbonarius Canada, England & Kenya [49, 50] Cereal products (baby foods) A. carbonarius, A. niger, A. phoenicis Uganda [51, 52] Spices A. niger var. niger Worldwide [27, 35, 53] Black pepper A. piperis Worldwide [27, 35] Desiccated coconut A. niger, A. carbonarius, A. japonicus Uganda & Kenya [45] Fruit juice & beverages A. niger, A. japonicus Egypt [54] Apricot, fig, grapes & plum A. awamori, A. carbonarius, A. japonicus, A. niger, A. tubingensis, A. sclerotioniger, A. aculeatus, A. aculeatinus Iraq [55] Cocoa bean, coffee bean & dried cassava A. carbonarius, A. niger, A. tubingensis, A. aculeatus Indonesia [56] Cocoa beans A. carbonarius, A. tubingensis, A. niger Sierra Leona, Equatorial Guinea & Ecuador [57] Olive oil A. niger Morocco [58] Vegetables A. brasiliensis, A. niger, A. japonicus, A. vadensis Egypt [59] 213 | Ismail Incidence and significance of black aspergilli in agricultural commodities European Journal of Biological Research 2017; 7 (3): 207-222 Table 3. Ochratoxins produced naturally in agricultural commodities due to infection by black aspergilla (A. carbonarius and A. niger). Commodities Country Reference Grape Worldwide [28, 31, 73-76] Grape Italy [32] Grape juice Europe [77] Wine Europe, worldwide [28, 74, 77] Raisins California, USA [29] Dried vine fruits Worldwide [7, 28, 76] Cereals Europe [77] Coffee Europe [74, 77] Dry fruits Europe [77] Cocoa Europe [77] Figs Central Europe [74] Peanuts Argentina [44] Rice and rice products* Worldwide [78-83] Cereal grains (wheat, barley, corn, oats, sorghum)* Worldwide (UK, Italy, Ivory Coast, Japan, Tunesia) [81, 84-88] Cereal flour (wheat, rye, maize, oats)* Worldwide [78, 82, 88- 90] Infant cereal food* Worldwide [86, 91, 92] *Means that aspergilli and penicillia may be involved in ohratoxin production. OTA is produced by fungi of the genera Aspergillus and Penicillium. The major species implicated in OTA production includes Aspergillus ochraceus, A. sulphureus, Petromyces alliaceus, Penicillium verrucosum, A. carbonarius, and to a lesser extent A. niger [62, 63]. Ueno et al. [64] were the first to report on ochratoxin A (OA) production by a black Aspergillus species, A. foetidus. This was later confirmed [33, 65]. OTA is a frequent natural contaminant of many foodstuffs such as cocoa beans, coffee beans, cassava flour, cereals, peanuts, dried fruits and wine [66]. Studies revealed that whenever OTA was detected in high levels, AFB1 was absent or present at very low levels and vice versa which suggests some sort of competition between these toxins at the production level in foodstuffs. OTA has also been reported as a contaminant of tiger nuts and fermented maize dough in West Africa [67]. Ochratoxin A contamination of agricultural products including cereals and grains influences chronic effect on human exposure [68]. Natural occurrence of mould infection and OTA conta- mination in maize and maize-based products is a worldwide problem [69]. A. niger is commonly isolated from maize [70] and a high incidence of A. carbonarius has been also reported [71]. Both species are the main source of ochratoxins in corn and other food products in both subtropical and tropical zones of the world [35] and to a lesser extent in grapes, wine, dried vine fruits and grape juice [72] (refer to Table 3). A. carbonarius was recognized as the major OTA-producer [65, 93-96], near 100% of isolaes produce OTA when grown in pure culture [97-101]. The closely related species A. niger has also been reported reliably as a producer [64, 97, 98, 102]. However all reports agree that OTA production by A. niger is very uncommon. Also, it was obser- ved that A. niger “aggregate”, although the most common, showed a low percentage of OTA producing strains, from 4 to 10% [101, 103]; none of the strains belonging to A. uvarum was able to produce OTA [14]. A. lacticoffeatus and A. sclero- tioniger, both isolated from coffee [11], and from raisin samples [104], are also reported as OTA producers (Table 4). The most distinguishing characteristics to differentiate A. niger aggregate species (A. niger, A. tubingensis and Aspergillus awamori) from A. carbonarius are growth at 37°C and conidial diameter [19]. All 12 of the ochratoxigenic isolates of A. carbonarius showed restricted growth at 37°C, while all of the nonochratoxigenic isolates of A. niger aggregate grew well at 37°C. This effect was more pronounced at 40°C, at which the ochratoxigenic strains did not grow and the nonochratoxigenic strains grew well. In addition, all OTA-producing strains formed large (7-10 µ m diameter), and all OTA-nonproducing strains formed smaller conidia (<4 µ m diameter) [29] (refer to the Key). 214 | Ismail Incidence and significance of black aspergilli in agricultural commodities European Journal of Biological Research 2017; 7 (3): 207-222 Table 4. Ochratoxins produced by black aspergilli isolated from agricultural commodities. Species Ochratoxins References A. aculeatus + [10] A. carbonarius + [11, 17, 19, 24, 25, 27-31, 35, 44, 47, 56, 57, 73, 74] A. foetidus + [33] A. japonicus + [27, 35, 44] A. lacticoffeatus + [11] A. niger var. niger + [11, 24, 27, 28, 33, 35, 44, 47, 56-58, 73, 74, 102] A. niger aggregate/ Section Nigri + [31, 37, 106] A. sclerotioniger + [11, 19] A. tubingensis + [27, 30, 35, 57] A. welwitschiae (=A. awamori) + [19, 28, 33, 44, 107] Figure 2. Chemical structures of fumonisins [113]. 4. FUMONISINS PRODUCTION IN AGRI- CULTURAL COMMODITIES AND BY THE ASSOCIATED BLACK ASPERGILLI Fumonisins (Fig. 2) were discovered in South Africa in 1988 [108, 109]. They are known to be produced by Fusarium verticillioides (formerly known as F. moniliforme), F. proliferatum, F. oxy- sporum, F. globosum, several other Fusarium spp., and Alternaria alternata f. sp. lycopersici. Fumo- nisins are frequently found in corn and corn-based foods [110, 111]. FB1 is the most commonly found, not only in corn (maize) and corn-based foods, but also in rice, sorghum, cowpea seeds, beans, soybeans and beer. FB1 can cause two diseases of farm animals: leucoencephalomalacia in horses and porcine pulmonary oedema. It is also carcinogenic, hepatotoxic, nephrotoxic and embryo- toxic in laboratory animals. In humans fumonisins are associated with oesophageal cancer and neural tube defects based on studies in Transkei [109] and Texas [112]. The International Agency for Research on Cancer (IARC) designated FB1 in Group 2B as ‘possibly carcinogenic to humans’ [60]. Findings of fumonisins in agricultural commodities are shown in Table 5. In recent years fumonsins have been found in a wide variety of foods such as, cassava products in Tanzania [114], garlic and onion powders [115] and garlic bulbs [116], black radish [117], black tea [118, 119], figs in Turkey [120, 121], peanuts in Cote d’Ivoire, Cameroon and China [87, 122, 123], and soybeans in Japan [124]. Fumonisins have been found in dietary and medicinal wild plants in South Africa [125] and in other medicinal plants: leaves of orange tree, leaves/flowers of linden tree and chamomile in Portugal [118], mint and stinging nettle in Turkey [119]. Of particular note and interest is that for some foods, FB1 is not the major fumonisin as it is for maize and other grains. FB2 (without FB1) occurred in wine from several countries [126, 127], such as red wine must in Italy [126] and beer [128]. Table 5 shows some commodities contaminated with fumonisins. Fumonisin production has also been proved by A. niger isolates originating from coffee beans and grapes [129, 130]. Further reports claimed that A. niger and A. awamori from grapes, raisins and coffee beans produced fumonisins particularly FB2 [129, 131], B2 and B4 [107, 126, 130, 132], although other isomers in smaller quantities [107] and a FB1 isoform, named FB6 were also detected [131]. No fumonisins were found in other black Aspergillus species from grapes, including A. carbonarius [126]. Whereas F. verticillioides produces fumo- nisins on agar media based on plant extracts such as barley malt, oat, rice, potatoes, and carrots, A. niger is able to produce fumonisins in high quantities on agar media with low water activity [63]. Recently, dried vine fruit samples (raisins, sultanas) were found contaminated with fumonisin-producing black aspergilli and several fumonisin isomers, including fumonisins B1-4, 3-epi-FB3, 3-epi-FB4, iso-FB1, and two iso-FB2,3 forms [107]. Several strains collected from figs, dates and onions were also able 215 | Ismail Incidence and significance of black aspergilli in agricultural commodities European Journal of Biological Research 2017; 7 (3): 207-222 to produce fumonisins, thus black aspergilla are suspected to be responsible for fumonisin conta- mination of grape-derived products, figs and onions. Figs and onions were also contaminated with low but significant amount of fumonisins [107]. Frisvad et al. [133] studied 180 strains of A. niger from various sources and found about 80% producing FB2 (refer to Table 6). Although the percentage of fumonisin-producing strains was very high, the absence of at least part of the fumonisin biosynthetic gene cluster has been reported in A. niger [134]. 5. ASPERILLUS NIGER AS A PLANT PATHOGEN A. niger has been identified as the responsible species in diseases of food crops, such as maize seedling blight, maize ear rot and seedling blight of peanuts. It causes also a disease called black mold on certain fruits and vegetables such as grapes, onions and peanuts [74, 141] (refer to Table 7). Table 5. Fumonisins B1 and B2 produced naturally from some agricultural commodities due to infection by black aspergilli (A. niger/A. awamori). Commodities Country Reference Grape, raisins, figs, onion Central Europe [74] Coffee beans Central Europe [63] Grapes, raisins & wine Central Europe [127, 130, 135, 136] Maize kernels South Africa [137] Table 6. Fumonisins produced by black aspergilli isolated from agricultural commodities. Species Fumonisins Reference A. carbonarius B1, B4 and several fumonisin isomers [74] A. niger var. niger B1, B4 [27, 35, 63, 126, 130, 131, 138] A. niger aggregate/ Section Nigri B2 [28, 37] A. welwitschiae (=A. awamori) + [19, 107, 139, 140] Table 7. Plant diseases caused by Aspergillus niger. Disease & host Reference Almond chlorosis [74, 142] Apricot, peach ripe fruit rot [74, 142] Bulb (black) rot of onions & garlic [74, 142] Black rot of cherry [143] Carrot sooty rot [74, 142] Citrus black mold [74, 142] Crown rot of peanuts [74, 142, 144] Fig smut [74, 142] Fruit rot of banana [145] Fruit rot of grapes [146] Grape bunch rot [74, 142] Kernel rot of maize [35] Mango black mold rot [74, 142, 147] Pistachio fruit rot [74, 142] Rot of tomatoes [148] Stem rot of Dracaena [149] Strawberry fruit rot [74, 142] Tuber rot of yam [150] Vine canker [74, 142] 6. CONCLUSION This review outlines a taxonomic overview on all described and accepted Asperillus species in section Nigri up-to-date with a key for identi- fication based on their phenotypic features, however these features are not enough for species delimi- tation and other tools (e.g. molecular techniques and/or some physiological and biochemical charac- teristics) are needed to support their identity. The incidence and implication of species in agricultural commodities are also discussed. Capabilities of some species of the section to produce ochratoxins and/or fumonisins are of special significance in these commodities due to their health hazard to human. TRANSPARENCY DECLARATION The author declares that has no conflict of interest. 216 | Ismail Incidence and significance of black aspergilli in agricultural commodities European Journal of Biological Research 2017; 7 (3): 207-222 REFERENCES 1. Thom C, Raper KB. A manual of the aspergilla. Williams & Wilkins, Baltimore, 1945. 2. 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