PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

doi: 10.15389/agrobiology.2024.3.550eng

UDC: 636.085.19:636.086.1/.3:632.4

Acknowledgements:
The work was carried out in accordance with the State Task on the topic: FGUG-2022-0008 “To scientifically substantiate and develop new methods, tools and technologies for ensuring sustainable veterinary and sanitary welfare of animal husbandry”, R&D registration number in CITIS 122042700106-1.

 

PRODUCTION OF OCHRATOXIN A, FUMONISINS AND EMODIN BY Aspergillus niger ISOLATES FROM FEED PRODUCTS

G.P. Kononenko ✉, E.A. Piryazeva, A.A. Burkin, E.V. Zotova

All-Russian Research Institute of Veterinary Sanitation, Hygiene, and Ecology—Branch of FSC ARRIEV RAS, 5, Zvenigorodskoe sh., Moscow, 123022 Russia, e-mail kononenkogp@mail.ru (✉ corresponding author), piryazeva01@yandex.ru, aaburkin@mail.ru, zotelena63@mail.ru

ORCID:
Kononenko G.P. orcid.org/0000-0002-9144-615X
Burkin A.A. orcid.org/0000-0002-5674-2818
Piryazeva E.A. orcid.org/0000-0002-9144-615X
Zotova E.V. orcid.org/0000-0002-9144-615X

Final revision received February 19, 2024
Accepted May 17, 2024

Micromycetes of one of the most complex taxonomically complex Aspergillus niger (the A. niger “aggregate”) in recent decades have invariably remained the object of close attention of researchers due to the risks of negative effects on humans and animals. For industrial and collection strains, the ability to synthesize toxic metabolites with particularly dangerous forms of action has been established — ochratoxin A (M.L. Abarca et al., 1994; J. Téren et al., 1996; J. Varga et al., 2002), group B fumonisins (J.C. Frisvad et al., 2007; J.M. Mogensen et al., 2010; M. Månsson et al., 2010) and emodin (A.A. Ismaiel et al. 2016). Strains producing ochratoxin A and fumonisins have been identified in food (P. Noomin et al., 2009; M. Storari et al., 2012; M. Yanai et al., 2013) and feed products (A. Dalcero et al., 2002; F. Accensi et al., 2004). In Russia, priority in the study of these fungi was given to assessing their danger as pathogens of mycoses in the human environment (A.B. Kulko, 2012; O.E. Marfenina et al., 2014). In this work, for the first time for A. niger from domestic grain feed products and storaged grass feeds (E.A. Piryazeva, L.S. Malinovskaya, 2013, 2014), the features of mycotoxin production was established, the influence of the type of substrate on the intensity of toxin formation in vitro was shown, and it was confirmed that it belongs to the species A. niger as part of A. niger “aggregate” (R.A. Samson et al., 2007). The purpose of the study was to assess the ability of A. niger cultures isolated from combined feed, five types of feed raw materials and hay of different botanical composition and territorial origin to produce B group fumonisins (FUM), ochratoxin A (OA), emodin (EMO), as well as to clarify their species according to the totality of morphological, physiological characteristics and composition of metabolites. For 12 monoconidial strains, toxin production was assessed on sucrose agar with yeast extract (YES), Czapek agar with yeast autolysate extract and 20% sucrose (CYA20S) and on rice grain. After incubation (7 days, 25ºC), the extracts were analyzed using test systems for enzyme-linked immunosorbent determination of mycotoxins (STO VNIIVSGE). According to morphological criteria (diameter of colonies, growth pattern, color, consistency of colonies, shape and width of the growing edge, shape of the conidial head, structure and pigmentation of conidiophores, size, shape and color of vesicles, metulae, phialids and conidia), according to the absence of sclerotia, results of Ehrlich test and the ability to produce OA and FUM, their belonging to the species A. niger in the clade of biseriate species was confirmed (R.A. Samson et al., 2007; J. Varga et al., 2011). The accumulation of FUM in 7 strains was 0.2 to 630 μg/g and absent in 5; all strains produced OA (from 0.005 to 0.064 μg/g) and EMO (from 0.004 to 0.9 μg/g). The difference in the accumulation of mycotoxins on agar media and grain substrate confirms the influence of substrate components on the activity of determinant gene clusters. Due to the weak potential for producing OA, EMO and the small proportion of active FUM producers, the contribution of A. niger to the contamination of grain feed and hay, even with intensive infestation, is unlikely to be significant.

Keywords: Aspergillus niger, feed raw materials, combined feed, hay, B group fumonisins, ochratoxin A, emodin, ELISA.

 

REFERENCES

  1. Nielsen K.F., Morgensen J.M., Johansen M., Larsen Th.O., Frisvad J.C. Review of secondary metabolites and mycotoxins from the Aspergillus niger group. Analytical and Bioanalytical Chemistry, 2009, 395(5): 1225-1242 CrossRef
  2. Ismail M.A. Incidence and significance of black aspergilli in agricultural commodities: a review, with a key to all species accepted to-date. European Journal of Biological Research, 2017, 7(3): 207-222 CrossRef
  3. Kul’ko A.B. Atlas uslovno-patogennykh gribov roda Aspergillus — vozbuditeley bronkholegochnykh infektsiy [Atlas of opportunistic fungi of the genus Aspergillus causative agents of bronchopulmonary infections]. Moscow, 2012 (in Russ.).
  4. Marfenina O.I., Bubnova E.N., Semenova E.A., Ivanova A.E., Danilogorskaya A.A. Mikologiya i fitopatologiya, 2014, 48(3): 139-150 (in Russ.).
  5. Varga J., Kevei F., Fekete C., Coenen A., Kozakiewicz Z., Croft J.H. Restriction fragment length polymorphisms in the mitochondrial DNAs of the Aspergillus niger aggregate. Mycological Research, 1993, 97(10): 1207-1212 CrossRef
  6. Debets A.J.M., Swart K., Hoekstra R.F., Bos C.J. Genetic maps of eight linkage groups of Aspergillus niger based on mitotic mapping. Current Genetic, 1993, 23: 47-53 CrossRef
  7. Samson R.A., Noonim P., Meijer M., Houbraken J., Frisvad J.C., Varga J. Diagnostic tools to identify black aspergilli. Studies in Mycology, 2007, 59(1): 129-145 CrossRef
  8. Varga J., Frisvad J.C., Koksubé S., Brankovics B., Tóth B., Sziget G., Samson R.A. New and revisited species in Aspergillus section Nigri. Studies in Mycology, 2011, 69(1): 1-17 CrossRef
  9. Bian C., Kusuya Y., Sklenář F., D'hooge E., Yaguchi T., Ban S., Visagie C.M., Houbraken J., Takahashi H., Hubka V. Reducing the number of accepted in Aspergillus series Nigri. Studies in Mycology, 2020, 102(1): 95-132 CrossRef
  10. Abarca M.L., Bragulat M.R., Castella G., Cabañes F.J. Ochratoxin A production by strains of Aspergillus niger var. niger. Applied and Environmental Microbiology, 1994, 60(7): 2650-2652 CrossRef
  11. Téren J., Varga J., Hamari Z., Rinyo E., Kevei F. Immunochemical detection of ochratoxin A in black Aspergillus strains. Mycopathologia, 1996, 134(3): 171-176 CrossRef
  12. Ono H., Kataoka A., Koakutsu M., Tanaka K., Kawasugi S., Wakazawa M., Ueno Y., Manabe M. Ochratoxin A productibility by strains of Aspergillus niger group stored in IFO culture collection. Mycotoxins, 1995, 41: 47-51 CrossRef
  13. Frisvad J.C., Smedsgaard J., Samson R.A., Larsen T.O., Thrane U. Fumonisin B2 production by Aspergillus niger. Journal of Agricultural and Food Chemistry, 2007, 55(23): 9727-9732 CrossRef
  14. Månsson M., Klejnstrup M.L., Phipps R.K., Nielsen K.F., Frisvad J.C., Gotfredsen C.H., Larsen T.O. Isolation and NMR characterization of fumonisin B2 and B6, a new fumonisin from Aspergillus niger. Journal of Agricultural and Food Chemistry, 2010, 58(2): 949-953 CrossRef
  15. Chang M., Wang J., Tian F., Zhang Q., Ye B. Antibacterial activity of secondary metabolites from Aspergillus awamori F12 isolated from rhizospheric soil of Rhizophora stylosa Griff. Acta Microbiologica Sinica (Wei Sheng Wu Xue Bao), 2010, 50(10): 1385-1391.
  16. Ismaiel A.A., Rabie G.H., Abd El-Aal M.A. Antimicrobial and morphogenic effects of emodin produced by Aspergillus awamori WAIR 120. Biologia, 2016, 71(5): 464-474 CrossRef
  17. Logriego A., Ferracane R., Haydukowsky M., Cozzi G., Ritieni A. Fumonisin B2 production by Aspergillus niger from grapes and natural occurrence in must. Food Additives and Contaminant. Part A, 2009, 26(11): 1495-1500 CrossRef
  18. Noomin P., Mahakarnchanakul W., Nielsen K.F., Frisvad J.C., Samson R.A. Fumonisin B2 production by Aspergillus niger in Thai coffee beans. Food Additives and Contaminant. Part A, 2009, 26(1): 94-100 CrossRef
  19. Storari M., Dennert F.G., Bigler L., Gessler C., Broggini G.A.L. Isolation of mycotoxins producing black Aspergilli in herbal teas available on the Swiss market. Food Control, 2012, 26(1): 157-161 CrossRef
  20. Soares C., Calado T., Venâncio A. Mycotoxin production by Aspergillus niger aggregate strains isolated from harvested maize in three Portuguese regions. Revista Iberoamericana de Micologia, 2013, 30(1): 9-13 CrossRef
  21. Massi F.P., Sartori D., Ferranti L.S., Lamanaka B.T., Taniwaki M.H., Vieira M.L.C., Fungaro M.H.P. Prospecting for the incidence of genes involved in ochratoxin and fumonisin biosynthesis in Brazilian strains of Aspergillus niger and A. welwitschiae. International Journal of Food Microbiology, 2016, 221: 19-28 CrossRef
  22. Yanai M., Kajihara C., Kimura A., Motoki O., Hiroshi B., Shun'ichi U. Identification and fumonisin B2 production of black aspergilli isolated from moldy dried fruits. Japanese Journal of Food Microbiologi, 2013, 30: 33-38 CrossRef
  23. Onami J.-I., Watanabe M., Yoshinari T., Hashimoto R., Kitayama M., Kobayashi N., Sugita-Konishi Y., Kamata Y., Takahashi H., Kawakami H., Terajima J. Fumonisin-production by Aspergillus section Nigri isolates from Japanese foods and environments. Food Safety, 2018, 6(2): 74-82 CrossRef
  24. Gil-Serna J., García-Díaz M., Vázquez C., González-Jaén M.T., Patiño B. Significance of Aspergillus niger aggregate species as contaminants of food products in Spain regarding their occurrence and their ability to produce mycotoxins. Food Microbiology, 2019, 82: 240-248 CrossRef
  25. Mikušová P., Caboñ M., Melichárkova A., Urík M., Ritieni A., Slovák M. Genetic diversity, ochratoxin A and fumonisin profiles of strains of Aspergillus section Nigri isolated from dried vine fruits. Toxins, 2020, 12(9): 592 CrossRef
  26. Accensi F., Abarca M.L., Cabañes F.J. Occurrence of Aspergillus species in mixed feed and component raw materials and their ability to produce ochratoxin A. Food Microbiology, 2004, 21(5): 623-627 CrossRef
  27. Dalcero A., Magnoli C., Hallak C., Chiacchiera S.M., Palacio G., Rosa C.A.R. Detection of ochratoxin A in animal feeds and capacity to produce this mycotoxin by Aspergillus section Nigri in Argentina. Food Additive and Contaminants, 2002, 19(11): 1065-1072 CrossRef
  28. Raper K.B., Fennell D.I. The genus Aspergillus. The Williams & Wilkins Comp., Baltimore, 1965.
  29. Piryazeva E.A., Malinovskaya L.S. Rossiyskiy zhurnal «Problemy veterinarnoy sanitarii, gigieny i ekologii», 2013, 2(10): 28-31 (in Russ.).
  30. Piryazeva E.A., Malinovskaya L.S. Rossiyskiy zhurnal «Problemy veterinarnoy sanitarii, gigieny i ekologii», 2014, 2(12): 26-32 (in Russ.).
  31. Samson R.A., Visagie C.M., Houbraken J., Hong S.-B., Hubka V., Klaassen C.H.W., Perrone G., Seifert K.A., Susca A., Tanney J.B., Varga J., Kocsube S., Szigeti G., Yaguchi T., Frisvad J.C. Phylogeny, identification and nomenclature of the genus Aspergillus. Studies in Mycology, 2014, 78(1): 141-173 CrossRef
  32. Frisvad J.C., Petersen L.M., Lyhne E.K., Larsen T.O. Formation of sclerotia and production of indoloterpenes by Aspergillus niger and other species in section Nigri. PLoS ONE,2014, 9(4): e94857 CrossRef
  33. Ellena V., Bucchieri D., Arcalis E., Sauer M., Steiger M.G. Sclerotia formed by citric acid producing strains of Aspergillus niger: induction and morphological analysis. Fungal Biology,2021, 125(6): 485-494 CrossRef
  34. Kononenko G.P., Piryazeva E.A., Zotova E.V., Burkin A.A. Species composition and toxicological characteristics of fungi of the genus Aspergillus isolated from coarse fodders. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2017, 52(6): 1279-1286 CrossRef
  35. Susca A., Proctor R.H., Morelli M., Haidukowski M., Gallo A., Logrieco A.F., Moretti A. Variation in fumonisin and ochratoxin production associated with differences in biosynthetic gene content in Aspergillus niger and A. welwitschiae isolates from multiple crop and geographic origins. Frontiers in Microbiology, 2016, 7: 1412 CrossRef
  36. Han X., Jiang H., Xu J., Zhang J., Li F. Dynamic fumonisin B2 production by Aspergillus niger intended used in food industry in China. Toxins, 2017, 9(7): 217 CrossRef
  37. Burkin A.A., Kononenko G.P. Immunologiya, allergologiya, infektologiya, 2010, 1: 187 (in Russ.).
  38. Palencia E.R., Mitchel T.R., Snook M.E., Glenn A.E., Gold S., Hinton D.M., Riley R.T., Bacon C.W. Analyses of black Aspergillus species of peanut and maize for ochratoxins and fumonisins. Journal of Food Protection, 2014, 77(5): 805-813 CrossRef
  39. Mogensen J.M., Frisvad J.C., Thrane U., Nielsen K.F. Production of fumonisin B2 and B4 by Aspergillus niger on grapes and raisins. Journal of Agricultural and Food Chemistry, 2010, 58(2): 954-958 CrossRef
  40. Fungi and food spoilage. 2nd edition. Pitt J.I., Hocking A.D. (eds.). Academic and Professional, London, 1997.
  41. Accensi F., Abarca M.L., Cano J., Figuera F., Cabañes F.J. Distribution of ochratoxin A producing strains in the A. niger aggregate. Antonie Van Leeuwenhoek, 2001, 79(3-4): 365-370 CrossRef
  42. Frisvad J.C., Larsen T.O., Thrane U., Meijer M., Varga J., Samson R.A., Nielsen K.F. Fumonisin and ochratoxin production in industrial Aspergillus niger strains. PLoS ONE, 2011, 6(8): e23496 CrossRef
  43. Logrieco A.F., Haidukowski M., Susca A., Mulè G., Munkvold G.P., Moretti A. Aspergillus section Nigri as contributor of fumonisin B2 contamination in maize. Food Additives & Contaminants: Part A, 2014, 31(1): 149-155 CrossRef
  44. Perrone G., Stea G., Epifani F., Varga J., Frisvad J.C., Samson R.A. Aspergillus niger contains the cryptic phylogenetic species A. awamori. Fungal Biology, 2011, 115(11): 1138-1150 CrossRef
  45. Palumbo J.D., O’Keeffe T.L. Detection and discrimination of four Aspergillus section Nigri species by PCR. Letters in Applied Microbiology, 2015, 60(2): 188-195 CrossRef
  46. Saadullah A.A., Abdullah S.K. Detection of ochratoxigenic potential in some Aspergillus and Penicillium isolates from vineyard soil, fresh and dried grapes by ELISA. Rafidain Journal of Science, 2018, 27(4): 1-7 CrossRef
  47. Susca A., Stea G., Mulé G., Perrone G. Polymerase chain reaction (PCR) identification of Aspergillus niger and Aspergillus tubingensis based on the calmodulin gene. Food Additives and Contaminants, 2007, 24(10): 1154-1160 CrossRef
  48. Martins H.M., Martins H.L., Bernando F., Gimeno A. Ability of wild strains of Aspergillus niger to produce ochratoxin A in cracked maize. Revista Portuguesa de Ciȇncias Veterinárias, 2005, 100(555/556): 189-192.
  49. Susca A., Proctor R.H., Mulé G., Stea G., Ritieni A., Logrieco A.F., Moretti A. Correlation of mycotoxin fumonisin B2 production and presence of the fumonisin biosynthetic gene fum8 in Aspergillus niger from grape. Journal of Agricultural and Food Chemistry, 2010, 58(16): 9266-9272 CrossRef
  50. Gil-Serna J., García-Díaz M., González-Jaén M.T., Vázquez C., Patiño B. Description of an orthologous cluster of ochratoxin A biosynthetic genes in Aspergillus and Penicillium species. A comparative analysis. International Journal of Food Microbiology, 2018, 268: 35-43 CrossRef
  51. Fanelli F., Schmidt-Heydt M., Haidukowski M., Geisen R., Logrieco A., Mulé G. Influence of light on growth, conidiation and the mutual regulation of fumonisin B2 and ochratoxin A biosynthesis by Aspergillus niger. World Mycotoxin Journal, 2012, 5(2): 169-176 CrossRef
  52. Varga J., Rigó K., Lamper C., Téren J., Szabó G. Kinetics of ochratoxin A production in different Aspergillus species. Acta Biologica Hungarica,2002, 53(3): 381-388.
  53. Mogensen J.M., Nielsen K.F., Samson R.A., Frisvad J.C., Thrane U. Effect of temperature and water activity on the production of fumonisins by Aspergillus niger and different Fusarium species. BMC Microbiology, 2009, 9(1): 281 CrossRef
  54. Lasram S., Hamdi Z., Chenenaoui S., Mliki A., Ghorbel A. Comparative study of toxigenic potential of Aspergillus flavus and Aspergillus niger isolated from Barley as affected by temperature, water activity and carbon source. Journal of Stored Products Research,2016, 69: 58-64 CrossRef
  55. Yu R., Liu J., Wang Y., Wang H., Zhang H. Aspergillus niger as a secondary metabolite factory. Frontiers in Chemistry, 2021, 9: 701022 CrossRef
  56. Wani M.A., Sanjana K., Kumar D.M., Lal D.K. GC-MS analysis reveals production of 2-phenylethanol from Aspergillus niger endophytic in rose. Journal of Basic Microbiology, 2010, 50(1): 110-114 CrossRef
  57. Hiort J., Maksimenka K., Reichert M., Perović-Ottstadt S., Lin W.H., Wray V., Steube K., Schaumann K., Weber H., Proksch P., Ebel R., Müller W.E.G., Bringmann G. New natural products from the sponge-derived fungus Aspergillus niger. Journal of Natural Products, 2004, 67(9): 1532-1543 CrossRef
  58. Burkin A.A., Kononenko G.P. Mycotoxin contamination of meadow grasses in European Russia. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2015, 50(4): 503-512 CrossRef
  59. Kononenko G.P., Zotova E.V., Burkin A.A. Advances in mycotoxicological research of forage grain crops. Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2021, 56(5): 958-967 CrossRef
  60. Burkin A.A., Kononenko G.P., Volovik V.T., Sergeeva S.E. The complex of mycotoxins in oilseed rape and turnip rape during spring and summer seasons [Agricultural Biology], 2022, Vol. 57, № 5, p. 992-1000 CrossRef

 

back

 


CONTENTS

 

 

Full article PDF (Rus)