Вестник Томского государственного университета. Биология. 2019; : 6-33
Токсигенные свойства микроскопических грибов
https://doi.org/10.17223/19988591/45/1Аннотация
Микроскопические грибы, инфицирующие растения в период вегетации, а также сельскохозяйственную продукцию при хранении, могут попадать в пищевые продукты и корма для животных и загрязнять их своими токсичными метаболитами – микотоксинами. Видовой состав и доля каждого из видов в комплексе выявляемых грибов могут меняться с изменением условий выращивания или хранения, что сопровождается изменениями в спектре микотоксинов. Наряду с известными и контролируемыми загрязнителями этого рода могут повышаться уровни содержания ранее не учитываемых токсичных грибных метаболитов, нуждающихся в дальнейшем изучении и оценке опасности их появления в продуктах питания. Обзор посвящен рассмотрению грибов из родов Fusarium, Aspergillus и Penicillium, представители которых могут продуцировать как уже регламентируемые в продуктах растениеводства микотоксины, так и прогнозируемые. В обзор включены также виды Alternaria spp., изучение которых выявило частую встречаемость и широкий спектр продуцируемых токсичных метаболитов, пока не нормируемых в пищевых продуктах.
Список литературы
1. Тутельян В.А., Кравченко Л.В. Микотоксины (Медицинские и биологические аспекты). М. : Медицина, 1985. 320 с.
2. Покровский А.А., Кравченко Л.В., Тутельян В.А. Афлатоксины. М. : ВИНИТИ АН СССР. Токсикология. 1977. Т. 8. 107 с.
3. Билай В.И. Пидопличко Н.М. Токсинообразующие микроскопические грибы. Киев : Наукова думка, 1970. 291 с.
4. Cousin M.A., Riley R.T., Pestka G.G. Foodborne mycotoxins: chemistry, biology, ecology and toxicology // In: Foodborne Pathogens : Microbiology and Molecular Biology. 2005. UK, Caister Academic Press. 164 p.
5. Папуниди К.Х., Тремасов М.Я., Фисинин В.И., Никитин А.И., Семёнов Э.И. Микотоксины (в пищевой цепи). Издание второе, переработанное и дополненное. Казань : ФЦТРБ-ВНИВИ, 2017. 188 с.
6. Кравченко Л.В., Тутельян В.А. Биобезопасность. Микотоксины – природные контаминанты пищи // Вопросы питания. 2005. Т. 74, № 3. C. 3–13.
7. Alshannaq A., Yu J.-H. Occurrence, Toxicity, and Analysis of Major Mycotoxins in Food // Int. J. Environ. Res. Public Health. 2017. Vol. 14. P. 632.
8. Richard J.L. Some major mycotoxins and their mycotoxicoses – An overview // International Journal of Food Microbiology. 2007. Vol. 119. PP. 3–10.
9. Egmond H.P. van, Schothorst R.C., Jonker M.A. Regulations relating to mycotoxins in food // Analytical and Bioanalytical Chemistry. 2007. Vol. 389. PP. 147–157. doi: 10.1007/s00216-007-1317-9
10. Gruber-Dorninger C., Novak B., Nagl V., Berthiller F. Emerging Mycotoxins: Beyond Traditionally Determined Food Contaminants // Journal of Agricultural and Food Chemistry. 2017. Vol. 65, № 33. PP. 7052–7070.
11. Marroquín-Cardona A.G., Johnson N.M., Phillips T.D. Hayes A.W. Mycotoxins in a changing global environment – A review // Food and Chemistry Toxicology. 2014. Vol. 69. PP. 220–230. doi: https://doi.org/10.1016/j.fct.2014.04.025
12. Medina A., Rodríguez A., Magan N. Climate change and mycotoxigenic fungi: impacts on mycotoxin production // Current Opinion in Food Science. 2015. Vol. 5. PP. 99–104. doi: https://doi.org/10.1016/j.cofs.2015.11.002
13. Jestoi M. Emerging Fusarium – Mycotoxins Fusaproliferin, Beauvericin, Enniatins, And Moniliformin – A Review // Critical Reviews in Food Science and Nutrition. 2008. Vol. 48, № 1. PP. 21–49. doi: http://dx.doi.org/10.1080/10408390601062021
14. Zinedine A., Fernandez-Franzon M., Manes J., Manyes L. Multi-mycotoxin contamination of couscous semolina commercialized in Morocco // Food Chemistry. 2017. Vol. 214. PP. 440–446.
15. Juan C., Covarelli L., Beccari G., Colasante V., Manes J. Simultaneous analysis of twentysix mycotoxins in durum wheat grain from Italy // Food Control. 2016. Vol. 62. PP. 322–329.
16. Fraeyman S., Croubels S., Devreese M., Antonissen G. Emerging Fusarium and Alternaria Mycotoxins : Occurrence, Toxicity and Toxicokinetics // Toxins. 2017. Vol. 9. PP. 228–257. doi: https://doi.org/10.3390/toxins9070228
17. Serrano A.B., Capriotti A.L., Cavaliere C., Piovesana S., Samperi R., Ventura S., Laganà A. Development of a Rapid LC-MS/MS Method for the determination of emerging Fusarium mycotoxins enniatins and beauvericin in human biological fluids // Toxins. 2015. Vol. 7. PP. 3554–3571. doi: https://doi.org/10.3390/toxins7093554
18. Varga E., Wiesenberger G., Hametner C., Ward T.J., Dong Y., Schöfbeck D., McCormick S., Broz K., Stückler R., Schuhmacher R., Krska R., Kistler H.C., Berthiller F., Adam G. New tricks of an old enemy: isolates of Fusarium graminearum produce a type A trichothecene mycotoxin // Environ. Microbiol. 2015. Vol. 17. PP. 2588–2600. doi: http://dx.doi.org/10.1111/1462-2920.12718
19. Lofgren L., Riddle J., Dong Y., Kuhnem P.R., Cummings J.A., Del Ponte E.M., Bergstrom G.C., Kistler H.C. A high proportion of NX-2 genotype strains are found among Fusarium graminearum isolates from northeastern New York State // Eur. J. Plant Pathol. 2018. doi: https://doi:10.1007/s10658-017-1314-6
20. O’Donnell K., Rooney A.P., Proctor R.H., Brown D.W., McCormick S.P., Ward T.J., Frandsen R.J.N., Rehner S.A. Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria // Fungal Genetics and Biology. 2013. Vol. 52. PP. 20–31.
21. Leggieri M.C., Decontardi S., Bertuzzi T., Pietri A., Battilani P. Modeling growth and toxin production of toxigenic fungi signaled in cheese under different temperature and water activity regimes // Toxins. 2017. Vol. 9, № 1. PP. 4–21.
22. Perrone G., Gallo A., Susca A. Aspergillus // In: Molecular Detection of Foodborne Pathogens, edited by Dongyou L., CRC Press, Taylor & Francis Group, USA. 2010. 879 р.
23. Levasseur-Garcia C. Updated Overview of Infrared Spectroscopy Methods for Detecting Mycotoxins on Cereals (Corn, Wheat, and Barley) // Toxins. 2018. Vol. 10, № 1. PP. 3–51. doi: 10.3390/toxins10010038
24. Mayer Z., Bagnara A., Farber P., Geisen R. Quantifcation of the copy number of nor-1, a gene of the aflatoxin biosynthetic pathway by real-time PCR, and its correlation to the cfu of Aspergillus flavus in foods // International Journal of Food Microbiology. 2003. Vol. 82, № 2. PP. 143–151.
25. Mayer Z., Farber P., Geisen R. Monitoring the production of aflatoxin B1 in wheat by measuring the concentration of nor-1 mRNA // Applied and Environmental Microbiology. 2003. Vol. 69, № 2. PP. 1154–1158.
26. European Food Safety Authority. EFSA on Contaminants in the Food Chain (CONTAM): Scientifc Opinion on the risks for animal and public health related to the presence of Alternaria toxins in feed and food // EFSA Journal. 2011. Vol. 9, № 10. PP. 2407–2504. doi: doi.org/10.2903/j.efsa.2011.2407. URL: www.efsa.europa.eu/efsajournal.
27. Liu D. Pruett S.B., Coyne C. Alternaria // In: Molecular Detection of Foodborne Pathogens, edited by Dongyou L., CRC Press, Taylor & Francis Group. USA. 2010. 879 p.
28. Ганнибал Ф.Б. Виды рода Alternaria, обнаруженные в России и на некоторых соседних территориях // Микология и фитопатология. 2015. Т. 49, № 6. C. 374–385.
29. Solfrizzo M. Recent advances on Alternaria mycotoxins // Current Opinion in Food Science. 2017. Vol. 17. PP. 57–61. doi: https://doi.org/10.1016/j.cofs.2017.09.012
30. Müller M.E.H., Korn U. Alternaria mycotoxins in wheat – A 10 years survey in the Northeast of Germany // Food Control. 2013. Vol. 34, № 1. PP. 191–197.
31. Romano C., Vanzi L., Massi D., Difonzo E.M. Subcutaneous alternariosis // Mycoses. 2005. Vol. 48, № 6. PP. 408–412.
32. Robertshaw H., Higgins E. Cutaneous infection with Alternaria tenuissima in an immunocompromised patient // British Journal of Dermatology. 2005. Vol. 153, № 5. PP. 1047–1049.
33. Sood N., Gugnani H.C., Guarro J., Palival-Joshi A., Vijayan V.K. Subcutaneous phaeohyphomycosis caused by Alternaria alternata in an immunocompetent patient // International Journal of Dermatology. 2007. Vol. 46, № 4. PP. 412–413. doi: https://doi.org/10.1111/j.1365-4632.2006.03053.x
34. López P., Venema D., Rijk T., Kok A., Scholten J.M., Hans G.J., Nijs M.M. Occurrence of Alternaria toxins in food products in the Netherlands // Food Control. 2016. Vol. 60. PP. 196–204.
35. Hickert S., Bergmann M., Ersen S., Cramer B., Hump H.-U. Survey of Alternaria toxin contamination in food from the German market, using a rapid HPLC-MS/MS approach // Mycotoxin Research. 2016. Vol. 32, № 1. PP. 7–18.
36. Walravens J., Micula H., Rychlik M., Asam S., Devos T., Ediage E.N., Mavungu J.D.D., Jacxsens L., Van Landschoot A., Vanhaecke L., De Saeger S. Validated UPLC-MS/MS methods to quantitate free and conjugated Alternaria toxins in commercially available tomato products and fruit and vegetable juices in Belgium // Journal of Agricultural and Food Chemistry. 2016. Vol. 64, № 24. PP. 5101–5109. doi: http://doi:10.1021/acs.jafc.6b01029
37. Iram S., Ahmad I. Analysis of variation in Alternaria alternata by pathogenicity and RAPD study // Polish Journal of Microbiology. 2005. Vol. 54, № 1. PP. 13–19.
38. Andersen B., Smedsgaard J., Jørring I., Skouboe P., Pedersen L.H. Real-time PCR quantifcation of the AM-toxin gene and HPLC qualifcation of toxigenic metabolites from Alternaria species from apples // Int. J. Food Microbiol. 2006. Vol. 111, № 2. PP. 105–111.
39. Технический регламент Таможенного союза «О безопасности пищевых добавок, ароматизаторов и технологических вспомогательных средств» (ТР ТС 029/2012). URL: http://www.eurasiancommission.org/ru/act/texnreg/deptexreg/tr/Documents/P_58.pdf
40. Andersen B., Thrane U. Foodborne fungi in fruit and cereals and their production of mycotoxins // Advances in Food Mycology. N.Y., 2006. PP. 137–152.
41. Воробьев А.А. Микробиология и иммунология / под ред. А.А. Воробьева. М. : Медицина, 1999. 464 с.
42. Varga J., Juhasz A., Kevei F., Kozakiewich Z. Molecular diversity of agriculturally important Aspergillus species // European Journal of Plant Pathology. 2004. Vol. 110. PP. 627–640.
43. Kensler T.W., Roebuck B.D., Wogan G.N., Groopman J.D. Aflatoxin: a 50-year odyssey of mechanistic and translational toxicology // Toxicology Sciences. 2011. Vol. 120. Suppl. 1 PP. 28–48.
44. Седова И.Б., Захарова Л.П., Киселева М.Г., Чалый З.А., Тутельян В.А. Фузариотоксины и афлатоксин В1 в продовольственном зерне кукурузы в Российской Федерации // Научные труды Северо-Кавказского федерального научного центра садоводства, виноградарства, виноделия. 2018. Т. 21. С. 129–137.
45. RASFF Annual Report 2016, European Union, 2017. 64 р. URL: https://ec.europa.eu/food/sites/food/fles/safety/docs/rasff_annual_report_2016.pdf
46. RASFF Preliminary Annual Report 2017, European Union, 2018. 58 p. URL: https://ec.europa.eu/food/sites/food/fles/safety/docs/rasff_annual_report_2017.pdf
47. Gul O., Dervisoglu M. Occurrence of Aflatoxin M1 in vacuum packed kashar cheeses in Turkey // International Journal of Food Properties. 2014. Vol. 17, № 2. PP. 273–282. doi: http://dx.doi.org/10.1080/10942912.2011.631247
48. Taniwaki M.H., Dender A.G.F. van. Occurrence of toxigenic molds in Brazilian cheeses // Journal of Food Protection. 1992. Vol. 55, № 3. PP. 187–191.
49. Malir F., Ostry V., Pfohl-Leszkowicz A., Malir J., Jakub T. Ochratoxin A: 50 Years of Research // Toxins. 2016. Vol. 8, № 7. P. 191. doi: http://doi:10.3390/toxins8070191
50. Седова И.Б., Киселева М.Г., Чалый З.А., Аксенов И.В., Захарова Л.П., Тутельян В.А. Анализ результатов мониторинга загрязнения микотоксинами продовольственного зерна урожаев 2005–2016 гг. // Успехи медицинской микологии. 2018. Т. 19. С. 329–330.
51. Аксенов И.В. Изучение содержания микотоксина охратоксина А в виноградных винах // Вопросы питания. 2018. Т. 87, № 5. Приложение. С. 174.
52. European Food Safety Authority. Opinion of the Scientifc panel on contaminants in the Food Chain of the EFSA on the request from the Commission related to ochratoxin A in food // EFSA Journal. 2006. Vol. 365. PP. 1–56.
53. Morello L.G., Sartori D., Oliveiro Martinez A.L. de, Vieira M.L.C., Taniwaki M.H., Pelegrinelli Fungaro M.H. Detection and quantifcation of Aspergillus westerdijkiae in coffee beans based on selective amplifcation of β-tubulin gene by using real-time PCR // International Journal of Food Microbiology. 2007. Vol. 119, № 3. PP. 270–276.
54. Sartori D., Furlaneto M.C., Martins M.K., Ferreira de Paula M.R., Pizzirani-Kleiner A.A., Taniwaki M.H., Pelegrinelli Fungaro M.H. PC method for the detection of potential ochratoxin-producing Aspergillus species in coffee beans // Research in Microbiology. 2006. Vol. 157, № 4. PP. 350–354. doi: https://doi.org/10.1016/j.resmic.2005.09.008
55. Rodríguez A., Rodríguez M., Luque M.I., Justesen A.F., Córdoba J.J. Quantifcation of ochratoxin A-producing molds in food products by SYBR Green and TaqMan real-time PCR methods // International Journal of Food Microbiology. 2011. Vol. 149, № 3. PP. 226–235.
56. Стахеев А.А., Самохвалова Л.В., Рязанцев Д.Ю., Завриев С.К. Молекулярногенетические методы в исследовании таксономии и специфической идентификации токсинпродуцирующих грибов рода Fusarium: успехи и проблемы // Сельскохозяйственная биология. 2016. Т. 51, № 3. C. 275–284.
57. Stakheev A.A., Ryazantsev D.Yu., Gagkaeva T.Yu., Zavriev S.K. PCR detection of Fusarium fungi with similar profles of the produced mycotoxins // Food Control. 2011. Vol. 22. PP. 462–468.
58. Waalwijk C. Quantitative detection of Fusarium spp. and its correlation with fumonisin content in maize from South African subsistence farmers // World Mycotoxin Journal. 2008. Vol. 1, № 1. PP. 39–47.
59. Минаева Л.П., Короткевич Ю.В., Захарова Л.П., Седова И.Б., Шевелева С.А. Прямое определение продуцентов Т-2 и НТ-2 микотоксинов – грибов рода Fusarium в продовольственном зерне методом ПЦР (Сообщение 2) // Вопросы питания. 2013. Т. 82, № 4. C. 48–54.
60. Moss M.O., Thrane U. Fusarium taxonomy with relation to trichothecene formation // Toxicology Letters. 2004. Vol. 153. PР. 23–28.
61. Соколова Г.Д. Внутривидовое разнообразие фитопатогенного гриба Fusarium graminearum // Микология и фитопатология. 2015. Т. 49, № 2. C. 71–79.
62. Gale L.R., Harrison S.A., Ward T.J., O’Donnell K., Milus E.A., Gale S.W., Kistler H.C. Nivalenol-type populations of Fusarium graminearum and F. asiaticum are prevalent on wheat in Southern Louisiana // Phytopathology. 2011. Vol. 101. PP. 124–134.
63. Kongkapan J., Polapothep A., Owen H. and Giorgi M. A brief overview of our current understanding of nivalenol: A growing potential danger yet to be fully investigated // Israel Journal of Veterinary Medicine. 2016. Vol. 71, № 1. PP. 3–9.
64. Vanheule A., De Boevre M., Moretti A., Scauflaire J., Munaut F., De Saeger S., Bekaert B., Haesaert G., Waalwijk C., van der Lee T., Audenaert K. Genetic Divergence and Chemotype Diversity in the Fusarium Head Blight Pathogen Fusarium poae // Toxins. 2017. Vol. 9, № 9. E255.
65. Kelly A., Proctor R.H., Belzile F., Chulze S.N., Clear R.M., Cowger C., Elmer W., Lee T., Obanor F., Waalwijk C., Ward T.J. The geographic distribution and complex evolutionary history of the NX-2 trichothecene chemotype from Fusarium graminearum // Fungal Genet. Biol. 2016. Vol. 95. PP. 39–48. doi: http://dx.doi.org/10.1016/j.fgb.2016.08.003
66. SCOOP Task 3.2.10, 2003 Collection of occurrence data of Fusarium toxins in food and assessment of dietary intake by the population of EU Member States http://europa.eu/int/ comm./food/fs/scoop/task3210.pdf.; Scientifc Committee on Food, 2005. Opinion on Fusarium Toxins, Part 5: T-2 toxin and HT-2 toxin. URL: http://europa.eu.int/comm./food/fs/sc/out88-en.pdf
67. Ferrigo D., Raiola A., Causin R. Fusarium toxins in cereals: occurrence, legislation, factors promoting the appearance and their management // Molecules. 2016. Vol. 21, № 5. E627.
68. Shi W., Tan Y., Wang S., Gardiner D.M., De Saeger S., Liao Y., Wang C., Fan Y., Wang Z., Wu A. Mycotoxigenic potentials of Fusarium species in various culture matrices revealed by mycotoxin profling // Toxins. 2017. Vol. 9, № 6. E6. doi: 10.3390/toxins9010006
69. Gavrilova O., Skritnika A., Gagkaeva T. Identifcation and characterization of spontaneous auxotrophic mutants in Fusarium langsethiae // Microorganisms. 2017. Vol. 5. Е14. doi: 10.3390/microorganisms502001
70. Stakheev A., Khairulina D.R., Zavriev S.K. Four-locus phylogeny of Fusarium avenaceum and related species and their species-specifc identifcation based on partial phosphate permease gene sequences // Int. J. Food Microbiol. 2016. Vol. 225. PP. 27–37.
71. Минаева Л.П., Короткевич Ю.В., Шевелева С.А. Ускоренный метод определения зараженности продовольственного зерна грибами рода Fusarium и их видовой идентификации (Сообщение 1) // Вопросы питания. 2013. T. 82, № 3. C. 61–66.
72. Гагкаева Т.Ю., Гаврилова О.П., Орина А.С., Казарцев И.А., Ганнибал Ф.Б. Сравнение методов выявления в зерне токсинопродуцирующих грибов рода Fusarium // Микология и фитопатология. 2017. T. 51, № 5. C. 292–298.
73. Стахеев А.А., Звездина Ю.К., Микитюк О.Д., Завриев С.К. Изучение токсинообразования и полиморфизма трихотеценовых генов у грибов рода Fusarium российских коллекций // Успехи медицинской микологии. 2018. T. 19. C. 337–343.
74. Dupont J. Penicillium // Molecular Detection of Foodborne Pathogens, edited by Dongyou L., CRC Press. Taylor & Francis Group, USA. 2010. 879 р.
75. Громовых Т.И., Кузнецова Л.С., Жилинская Н.В., Лушина К.В. Оценка фунгицидной активности штаммов базидиомицетов в отношении индукторов плесневения пищевых продуктов грибами из рода Penicillium Link // Проблемы медицинской микологии. 2014. T. 16, № 1. С. 40–45.
76. Кузнецова Л.С., Михеева Н.В., Казакова Е.В., Озерская С.М., Иванушкина Н.Е. Состав плесневых грибов, поражающих поверхность мясной продукции // Мясная индустрия. 2009. № 3. C. 28–30.
77. Torović L., Dimitrov N., Lopes A., Martins C., Alvito P., Assunção R. Patulin in fruit juices: occurrence, bioaccessibility, and risk assessment for Serbian population // Food Additives & Contaminants: Part A. 2018. Vol. 35, № 5. PP. 985–995. doi: https://doi.org/10.1080/19440049.2017.1419580
78. Ratnasingham S., Hebert P.D. BOLD: The Barcode of Life Data System // Molecular Ecology Notes. 2007. Vol. 7, № 3. PP. 335–364.
79. Luque M.I., Córdoba J.J., Rodríguez A., Núñez F., Andrade M.A. Development of a PCR protocol to detect ochratoxin A producing moulds in food products // Food Control. 2013. Vol. 29, № 1. PP. 270–278. doi: https://doi.org/10.1016/j.foodcont.2012.06.023
80. Paterson R.R. Identifcation and quantifcation of mycotoxigenic fungi by PCR // Process Biochemistry. 2006. Vol. 41, № 7. PP. 1467–1474.
81. Atoui A., Khoury A.I., Kallassy M., Lebrihi A. Quantifcation of Fusarium graminearum and Fusarium culmorum by real-time PCR system and zearalenone assessment in maize / / International Journal of Food Microbiology. 2012. Vol. 154, № 1–2. PP. 59–65.
Tomsk State University Journal of Biology. 2019; : 6-33
Toxigenic properties of mycotoxin-producing fungi
https://doi.org/10.17223/19988591/45/1Abstract
Microscopic fungi that infect plants during the growing season and agricultural products during storage can get into food and animal feed and pollute them with their toxic metabolites – mycotoxins. The species composition and proportion of each species in the complex of fungi may vary with changes in growing or storage conditions, which is accompanied by changes in the spectrum of mycotoxins. In addition to known and controlled pollutants of this kind, the levels of previously unaccounted toxic fungal metabolites may increase, requiring a further study and assessment of the risk of their occurrence in food. The review is devoted to the consideration of fungi from the genera Fusarium, Aspergillus and Penicillium, whose representatives can produce mycotoxins both already regulated in plant products and predicted. The review also includes species Alternaria spp., the study of which revealed a frequent occurrence and a wide range of produced toxic metabolites, not yet normalized in food. Most mycotoxic fungi can multiply and accumulate toxic metabolites in a wide range of habitats of these microorganisms. We showed that microorganisms are extremely widespread in nature, and under favorable conditions with high humidity and optimal temperature (See Table 1) can affect various food products, animal feed and vegetable resources causing signifcant economic damage. Since it is diffcult to identify toxin-producing fungi contaminating different substrates including food products and animal feed, mycotoxinology studies are conducted in accordance with a strict procedure including detection of species composition of fungi and their distribution by geographical zones, and determination of substrates contaminated with mycotoxins, as well as the composition of mycotoxins and the mechanism of their action on humans and animals. The paper presents data on the properties of toxigenic fungi of the genera Aspergillus, Alternaria, Fusarium and Penicillium, the most important from the point of view of food and animal feed safety. A special attention is paid to the problem of detecting producers of emerging mycotoxins among these fungi (See Table 2), which include fusaproliferin, beauvericin, enniatins, moniliformin, tenuazonic acid, tentoxin, alternariol and its methyl ether, mycophenolic acid, citrinin, fusaric acid, sterigmatocystin, emodin and asperglaucid (Gruber-Dorninger C et al., 2017, Jestoi M, 2008, Fraeyman S et al., 2017, Serrano AB, 2015). The review discusses the problems and prospects of applying the methods of DNAidentifcation of toxigenic fungi, touched upon in works of Gagkaeva TYu et al., 2017, Stakheev AA et al., 2018, Dupont J, 2010, Gromovykh TI et al., 2014, Rodríguez A et al., 2011. We enumerate the diffculties that prevent a widespread introduction of PCR- diagnostics including the specifcs of fungal DNA extraction, peculiarities of qualitative PCR for multinuclear cells of flamentous fungi, and the necessity to differentiate inactivated and viable mold forms. We showed that molecular methods of micromycete identifcation should be improved in order to search for target DNA sequences and markers which correlate with mycotoxigenic strains in the studied substrate. An important part of the research was to identify mycotoxin biosynthesis genes and evaluate their expression. Selection and improvement of DNA methods of food control for toxigenic fungi are needed for adequate risk evaluation of food contamination with mycotoxins, ensuring its safety and preventing mycotoxicosis. The paper contains 2 Tables and 81 References.
References
1. Tutel'yan V.A., Kravchenko L.V. Mikotoksiny (Meditsinskie i biologicheskie aspekty). M. : Meditsina, 1985. 320 s.
2. Pokrovskii A.A., Kravchenko L.V., Tutel'yan V.A. Aflatoksiny. M. : VINITI AN SSSR. Toksikologiya. 1977. T. 8. 107 s.
3. Bilai V.I. Pidoplichko N.M. Toksinoobrazuyushchie mikroskopicheskie griby. Kiev : Naukova dumka, 1970. 291 s.
4. Cousin M.A., Riley R.T., Pestka G.G. Foodborne mycotoxins: chemistry, biology, ecology and toxicology // In: Foodborne Pathogens : Microbiology and Molecular Biology. 2005. UK, Caister Academic Press. 164 p.
5. Papunidi K.Kh., Tremasov M.Ya., Fisinin V.I., Nikitin A.I., Semenov E.I. Mikotoksiny (v pishchevoi tsepi). Izdanie vtoroe, pererabotannoe i dopolnennoe. Kazan' : FTsTRB-VNIVI, 2017. 188 s.
6. Kravchenko L.V., Tutel'yan V.A. Biobezopasnost'. Mikotoksiny – prirodnye kontaminanty pishchi // Voprosy pitaniya. 2005. T. 74, № 3. C. 3–13.
7. Alshannaq A., Yu J.-H. Occurrence, Toxicity, and Analysis of Major Mycotoxins in Food // Int. J. Environ. Res. Public Health. 2017. Vol. 14. P. 632.
8. Richard J.L. Some major mycotoxins and their mycotoxicoses – An overview // International Journal of Food Microbiology. 2007. Vol. 119. PP. 3–10.
9. Egmond H.P. van, Schothorst R.C., Jonker M.A. Regulations relating to mycotoxins in food // Analytical and Bioanalytical Chemistry. 2007. Vol. 389. PP. 147–157. doi: 10.1007/s00216-007-1317-9
10. Gruber-Dorninger C., Novak B., Nagl V., Berthiller F. Emerging Mycotoxins: Beyond Traditionally Determined Food Contaminants // Journal of Agricultural and Food Chemistry. 2017. Vol. 65, № 33. PP. 7052–7070.
11. Marroquín-Cardona A.G., Johnson N.M., Phillips T.D. Hayes A.W. Mycotoxins in a changing global environment – A review // Food and Chemistry Toxicology. 2014. Vol. 69. PP. 220–230. doi: https://doi.org/10.1016/j.fct.2014.04.025
12. Medina A., Rodríguez A., Magan N. Climate change and mycotoxigenic fungi: impacts on mycotoxin production // Current Opinion in Food Science. 2015. Vol. 5. PP. 99–104. doi: https://doi.org/10.1016/j.cofs.2015.11.002
13. Jestoi M. Emerging Fusarium – Mycotoxins Fusaproliferin, Beauvericin, Enniatins, And Moniliformin – A Review // Critical Reviews in Food Science and Nutrition. 2008. Vol. 48, № 1. PP. 21–49. doi: http://dx.doi.org/10.1080/10408390601062021
14. Zinedine A., Fernandez-Franzon M., Manes J., Manyes L. Multi-mycotoxin contamination of couscous semolina commercialized in Morocco // Food Chemistry. 2017. Vol. 214. PP. 440–446.
15. Juan C., Covarelli L., Beccari G., Colasante V., Manes J. Simultaneous analysis of twentysix mycotoxins in durum wheat grain from Italy // Food Control. 2016. Vol. 62. PP. 322–329.
16. Fraeyman S., Croubels S., Devreese M., Antonissen G. Emerging Fusarium and Alternaria Mycotoxins : Occurrence, Toxicity and Toxicokinetics // Toxins. 2017. Vol. 9. PP. 228–257. doi: https://doi.org/10.3390/toxins9070228
17. Serrano A.B., Capriotti A.L., Cavaliere C., Piovesana S., Samperi R., Ventura S., Laganà A. Development of a Rapid LC-MS/MS Method for the determination of emerging Fusarium mycotoxins enniatins and beauvericin in human biological fluids // Toxins. 2015. Vol. 7. PP. 3554–3571. doi: https://doi.org/10.3390/toxins7093554
18. Varga E., Wiesenberger G., Hametner C., Ward T.J., Dong Y., Schöfbeck D., McCormick S., Broz K., Stückler R., Schuhmacher R., Krska R., Kistler H.C., Berthiller F., Adam G. New tricks of an old enemy: isolates of Fusarium graminearum produce a type A trichothecene mycotoxin // Environ. Microbiol. 2015. Vol. 17. PP. 2588–2600. doi: http://dx.doi.org/10.1111/1462-2920.12718
19. Lofgren L., Riddle J., Dong Y., Kuhnem P.R., Cummings J.A., Del Ponte E.M., Bergstrom G.C., Kistler H.C. A high proportion of NX-2 genotype strains are found among Fusarium graminearum isolates from northeastern New York State // Eur. J. Plant Pathol. 2018. doi: https://doi:10.1007/s10658-017-1314-6
20. O’Donnell K., Rooney A.P., Proctor R.H., Brown D.W., McCormick S.P., Ward T.J., Frandsen R.J.N., Rehner S.A. Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria // Fungal Genetics and Biology. 2013. Vol. 52. PP. 20–31.
21. Leggieri M.C., Decontardi S., Bertuzzi T., Pietri A., Battilani P. Modeling growth and toxin production of toxigenic fungi signaled in cheese under different temperature and water activity regimes // Toxins. 2017. Vol. 9, № 1. PP. 4–21.
22. Perrone G., Gallo A., Susca A. Aspergillus // In: Molecular Detection of Foodborne Pathogens, edited by Dongyou L., CRC Press, Taylor & Francis Group, USA. 2010. 879 r.
23. Levasseur-Garcia C. Updated Overview of Infrared Spectroscopy Methods for Detecting Mycotoxins on Cereals (Corn, Wheat, and Barley) // Toxins. 2018. Vol. 10, № 1. PP. 3–51. doi: 10.3390/toxins10010038
24. Mayer Z., Bagnara A., Farber P., Geisen R. Quantifcation of the copy number of nor-1, a gene of the aflatoxin biosynthetic pathway by real-time PCR, and its correlation to the cfu of Aspergillus flavus in foods // International Journal of Food Microbiology. 2003. Vol. 82, № 2. PP. 143–151.
25. Mayer Z., Farber P., Geisen R. Monitoring the production of aflatoxin B1 in wheat by measuring the concentration of nor-1 mRNA // Applied and Environmental Microbiology. 2003. Vol. 69, № 2. PP. 1154–1158.
26. European Food Safety Authority. EFSA on Contaminants in the Food Chain (CONTAM): Scientifc Opinion on the risks for animal and public health related to the presence of Alternaria toxins in feed and food // EFSA Journal. 2011. Vol. 9, № 10. PP. 2407–2504. doi: doi.org/10.2903/j.efsa.2011.2407. URL: www.efsa.europa.eu/efsajournal.
27. Liu D. Pruett S.B., Coyne C. Alternaria // In: Molecular Detection of Foodborne Pathogens, edited by Dongyou L., CRC Press, Taylor & Francis Group. USA. 2010. 879 p.
28. Gannibal F.B. Vidy roda Alternaria, obnaruzhennye v Rossii i na nekotorykh sosednikh territoriyakh // Mikologiya i fitopatologiya. 2015. T. 49, № 6. C. 374–385.
29. Solfrizzo M. Recent advances on Alternaria mycotoxins // Current Opinion in Food Science. 2017. Vol. 17. PP. 57–61. doi: https://doi.org/10.1016/j.cofs.2017.09.012
30. Müller M.E.H., Korn U. Alternaria mycotoxins in wheat – A 10 years survey in the Northeast of Germany // Food Control. 2013. Vol. 34, № 1. PP. 191–197.
31. Romano C., Vanzi L., Massi D., Difonzo E.M. Subcutaneous alternariosis // Mycoses. 2005. Vol. 48, № 6. PP. 408–412.
32. Robertshaw H., Higgins E. Cutaneous infection with Alternaria tenuissima in an immunocompromised patient // British Journal of Dermatology. 2005. Vol. 153, № 5. PP. 1047–1049.
33. Sood N., Gugnani H.C., Guarro J., Palival-Joshi A., Vijayan V.K. Subcutaneous phaeohyphomycosis caused by Alternaria alternata in an immunocompetent patient // International Journal of Dermatology. 2007. Vol. 46, № 4. PP. 412–413. doi: https://doi.org/10.1111/j.1365-4632.2006.03053.x
34. López P., Venema D., Rijk T., Kok A., Scholten J.M., Hans G.J., Nijs M.M. Occurrence of Alternaria toxins in food products in the Netherlands // Food Control. 2016. Vol. 60. PP. 196–204.
35. Hickert S., Bergmann M., Ersen S., Cramer B., Hump H.-U. Survey of Alternaria toxin contamination in food from the German market, using a rapid HPLC-MS/MS approach // Mycotoxin Research. 2016. Vol. 32, № 1. PP. 7–18.
36. Walravens J., Micula H., Rychlik M., Asam S., Devos T., Ediage E.N., Mavungu J.D.D., Jacxsens L., Van Landschoot A., Vanhaecke L., De Saeger S. Validated UPLC-MS/MS methods to quantitate free and conjugated Alternaria toxins in commercially available tomato products and fruit and vegetable juices in Belgium // Journal of Agricultural and Food Chemistry. 2016. Vol. 64, № 24. PP. 5101–5109. doi: http://doi:10.1021/acs.jafc.6b01029
37. Iram S., Ahmad I. Analysis of variation in Alternaria alternata by pathogenicity and RAPD study // Polish Journal of Microbiology. 2005. Vol. 54, № 1. PP. 13–19.
38. Andersen B., Smedsgaard J., Jørring I., Skouboe P., Pedersen L.H. Real-time PCR quantifcation of the AM-toxin gene and HPLC qualifcation of toxigenic metabolites from Alternaria species from apples // Int. J. Food Microbiol. 2006. Vol. 111, № 2. PP. 105–111.
39. Tekhnicheskii reglament Tamozhennogo soyuza «O bezopasnosti pishchevykh dobavok, aromatizatorov i tekhnologicheskikh vspomogatel'nykh sredstv» (TR TS 029/2012). URL: http://www.eurasiancommission.org/ru/act/texnreg/deptexreg/tr/Documents/P_58.pdf
40. Andersen B., Thrane U. Foodborne fungi in fruit and cereals and their production of mycotoxins // Advances in Food Mycology. N.Y., 2006. PP. 137–152.
41. Vorob'ev A.A. Mikrobiologiya i immunologiya / pod red. A.A. Vorob'eva. M. : Meditsina, 1999. 464 s.
42. Varga J., Juhasz A., Kevei F., Kozakiewich Z. Molecular diversity of agriculturally important Aspergillus species // European Journal of Plant Pathology. 2004. Vol. 110. PP. 627–640.
43. Kensler T.W., Roebuck B.D., Wogan G.N., Groopman J.D. Aflatoxin: a 50-year odyssey of mechanistic and translational toxicology // Toxicology Sciences. 2011. Vol. 120. Suppl. 1 PP. 28–48.
44. Sedova I.B., Zakharova L.P., Kiseleva M.G., Chalyi Z.A., Tutel'yan V.A. Fuzariotoksiny i aflatoksin V1 v prodovol'stvennom zerne kukuruzy v Rossiiskoi Federatsii // Nauchnye trudy Severo-Kavkazskogo federal'nogo nauchnogo tsentra sadovodstva, vinogradarstva, vinodeliya. 2018. T. 21. S. 129–137.
45. RASFF Annual Report 2016, European Union, 2017. 64 r. URL: https://ec.europa.eu/food/sites/food/fles/safety/docs/rasff_annual_report_2016.pdf
46. RASFF Preliminary Annual Report 2017, European Union, 2018. 58 p. URL: https://ec.europa.eu/food/sites/food/fles/safety/docs/rasff_annual_report_2017.pdf
47. Gul O., Dervisoglu M. Occurrence of Aflatoxin M1 in vacuum packed kashar cheeses in Turkey // International Journal of Food Properties. 2014. Vol. 17, № 2. PP. 273–282. doi: http://dx.doi.org/10.1080/10942912.2011.631247
48. Taniwaki M.H., Dender A.G.F. van. Occurrence of toxigenic molds in Brazilian cheeses // Journal of Food Protection. 1992. Vol. 55, № 3. PP. 187–191.
49. Malir F., Ostry V., Pfohl-Leszkowicz A., Malir J., Jakub T. Ochratoxin A: 50 Years of Research // Toxins. 2016. Vol. 8, № 7. P. 191. doi: http://doi:10.3390/toxins8070191
50. Sedova I.B., Kiseleva M.G., Chalyi Z.A., Aksenov I.V., Zakharova L.P., Tutel'yan V.A. Analiz rezul'tatov monitoringa zagryazneniya mikotoksinami prodovol'stvennogo zerna urozhaev 2005–2016 gg. // Uspekhi meditsinskoi mikologii. 2018. T. 19. S. 329–330.
51. Aksenov I.V. Izuchenie soderzhaniya mikotoksina okhratoksina A v vinogradnykh vinakh // Voprosy pitaniya. 2018. T. 87, № 5. Prilozhenie. S. 174.
52. European Food Safety Authority. Opinion of the Scientifc panel on contaminants in the Food Chain of the EFSA on the request from the Commission related to ochratoxin A in food // EFSA Journal. 2006. Vol. 365. PP. 1–56.
53. Morello L.G., Sartori D., Oliveiro Martinez A.L. de, Vieira M.L.C., Taniwaki M.H., Pelegrinelli Fungaro M.H. Detection and quantifcation of Aspergillus westerdijkiae in coffee beans based on selective amplifcation of β-tubulin gene by using real-time PCR // International Journal of Food Microbiology. 2007. Vol. 119, № 3. PP. 270–276.
54. Sartori D., Furlaneto M.C., Martins M.K., Ferreira de Paula M.R., Pizzirani-Kleiner A.A., Taniwaki M.H., Pelegrinelli Fungaro M.H. PC method for the detection of potential ochratoxin-producing Aspergillus species in coffee beans // Research in Microbiology. 2006. Vol. 157, № 4. PP. 350–354. doi: https://doi.org/10.1016/j.resmic.2005.09.008
55. Rodríguez A., Rodríguez M., Luque M.I., Justesen A.F., Córdoba J.J. Quantifcation of ochratoxin A-producing molds in food products by SYBR Green and TaqMan real-time PCR methods // International Journal of Food Microbiology. 2011. Vol. 149, № 3. PP. 226–235.
56. Stakheev A.A., Samokhvalova L.V., Ryazantsev D.Yu., Zavriev S.K. Molekulyarnogeneticheskie metody v issledovanii taksonomii i spetsificheskoi identifikatsii toksinprodutsiruyushchikh gribov roda Fusarium: uspekhi i problemy // Sel'skokhozyaistvennaya biologiya. 2016. T. 51, № 3. C. 275–284.
57. Stakheev A.A., Ryazantsev D.Yu., Gagkaeva T.Yu., Zavriev S.K. PCR detection of Fusarium fungi with similar profles of the produced mycotoxins // Food Control. 2011. Vol. 22. PP. 462–468.
58. Waalwijk C. Quantitative detection of Fusarium spp. and its correlation with fumonisin content in maize from South African subsistence farmers // World Mycotoxin Journal. 2008. Vol. 1, № 1. PP. 39–47.
59. Minaeva L.P., Korotkevich Yu.V., Zakharova L.P., Sedova I.B., Sheveleva S.A. Pryamoe opredelenie produtsentov T-2 i NT-2 mikotoksinov – gribov roda Fusarium v prodovol'stvennom zerne metodom PTsR (Soobshchenie 2) // Voprosy pitaniya. 2013. T. 82, № 4. C. 48–54.
60. Moss M.O., Thrane U. Fusarium taxonomy with relation to trichothecene formation // Toxicology Letters. 2004. Vol. 153. PR. 23–28.
61. Sokolova G.D. Vnutrividovoe raznoobrazie fitopatogennogo griba Fusarium graminearum // Mikologiya i fitopatologiya. 2015. T. 49, № 2. C. 71–79.
62. Gale L.R., Harrison S.A., Ward T.J., O’Donnell K., Milus E.A., Gale S.W., Kistler H.C. Nivalenol-type populations of Fusarium graminearum and F. asiaticum are prevalent on wheat in Southern Louisiana // Phytopathology. 2011. Vol. 101. PP. 124–134.
63. Kongkapan J., Polapothep A., Owen H. and Giorgi M. A brief overview of our current understanding of nivalenol: A growing potential danger yet to be fully investigated // Israel Journal of Veterinary Medicine. 2016. Vol. 71, № 1. PP. 3–9.
64. Vanheule A., De Boevre M., Moretti A., Scauflaire J., Munaut F., De Saeger S., Bekaert B., Haesaert G., Waalwijk C., van der Lee T., Audenaert K. Genetic Divergence and Chemotype Diversity in the Fusarium Head Blight Pathogen Fusarium poae // Toxins. 2017. Vol. 9, № 9. E255.
65. Kelly A., Proctor R.H., Belzile F., Chulze S.N., Clear R.M., Cowger C., Elmer W., Lee T., Obanor F., Waalwijk C., Ward T.J. The geographic distribution and complex evolutionary history of the NX-2 trichothecene chemotype from Fusarium graminearum // Fungal Genet. Biol. 2016. Vol. 95. PP. 39–48. doi: http://dx.doi.org/10.1016/j.fgb.2016.08.003
66. SCOOP Task 3.2.10, 2003 Collection of occurrence data of Fusarium toxins in food and assessment of dietary intake by the population of EU Member States http://europa.eu/int/ comm./food/fs/scoop/task3210.pdf.; Scientifc Committee on Food, 2005. Opinion on Fusarium Toxins, Part 5: T-2 toxin and HT-2 toxin. URL: http://europa.eu.int/comm./food/fs/sc/out88-en.pdf
67. Ferrigo D., Raiola A., Causin R. Fusarium toxins in cereals: occurrence, legislation, factors promoting the appearance and their management // Molecules. 2016. Vol. 21, № 5. E627.
68. Shi W., Tan Y., Wang S., Gardiner D.M., De Saeger S., Liao Y., Wang C., Fan Y., Wang Z., Wu A. Mycotoxigenic potentials of Fusarium species in various culture matrices revealed by mycotoxin profling // Toxins. 2017. Vol. 9, № 6. E6. doi: 10.3390/toxins9010006
69. Gavrilova O., Skritnika A., Gagkaeva T. Identifcation and characterization of spontaneous auxotrophic mutants in Fusarium langsethiae // Microorganisms. 2017. Vol. 5. E14. doi: 10.3390/microorganisms502001
70. Stakheev A., Khairulina D.R., Zavriev S.K. Four-locus phylogeny of Fusarium avenaceum and related species and their species-specifc identifcation based on partial phosphate permease gene sequences // Int. J. Food Microbiol. 2016. Vol. 225. PP. 27–37.
71. Minaeva L.P., Korotkevich Yu.V., Sheveleva S.A. Uskorennyi metod opredeleniya zarazhennosti prodovol'stvennogo zerna gribami roda Fusarium i ikh vidovoi identifikatsii (Soobshchenie 1) // Voprosy pitaniya. 2013. T. 82, № 3. C. 61–66.
72. Gagkaeva T.Yu., Gavrilova O.P., Orina A.S., Kazartsev I.A., Gannibal F.B. Sravnenie metodov vyyavleniya v zerne toksinoprodutsiruyushchikh gribov roda Fusarium // Mikologiya i fitopatologiya. 2017. T. 51, № 5. C. 292–298.
73. Stakheev A.A., Zvezdina Yu.K., Mikityuk O.D., Zavriev S.K. Izuchenie toksinoobrazovaniya i polimorfizma trikhotetsenovykh genov u gribov roda Fusarium rossiiskikh kollektsii // Uspekhi meditsinskoi mikologii. 2018. T. 19. C. 337–343.
74. Dupont J. Penicillium // Molecular Detection of Foodborne Pathogens, edited by Dongyou L., CRC Press. Taylor & Francis Group, USA. 2010. 879 r.
75. Gromovykh T.I., Kuznetsova L.S., Zhilinskaya N.V., Lushina K.V. Otsenka fungitsidnoi aktivnosti shtammov bazidiomitsetov v otnoshenii induktorov plesneveniya pishchevykh produktov gribami iz roda Penicillium Link // Problemy meditsinskoi mikologii. 2014. T. 16, № 1. S. 40–45.
76. Kuznetsova L.S., Mikheeva N.V., Kazakova E.V., Ozerskaya S.M., Ivanushkina N.E. Sostav plesnevykh gribov, porazhayushchikh poverkhnost' myasnoi produktsii // Myasnaya industriya. 2009. № 3. C. 28–30.
77. Torović L., Dimitrov N., Lopes A., Martins C., Alvito P., Assunção R. Patulin in fruit juices: occurrence, bioaccessibility, and risk assessment for Serbian population // Food Additives & Contaminants: Part A. 2018. Vol. 35, № 5. PP. 985–995. doi: https://doi.org/10.1080/19440049.2017.1419580
78. Ratnasingham S., Hebert P.D. BOLD: The Barcode of Life Data System // Molecular Ecology Notes. 2007. Vol. 7, № 3. PP. 335–364.
79. Luque M.I., Córdoba J.J., Rodríguez A., Núñez F., Andrade M.A. Development of a PCR protocol to detect ochratoxin A producing moulds in food products // Food Control. 2013. Vol. 29, № 1. PP. 270–278. doi: https://doi.org/10.1016/j.foodcont.2012.06.023
80. Paterson R.R. Identifcation and quantifcation of mycotoxigenic fungi by PCR // Process Biochemistry. 2006. Vol. 41, № 7. PP. 1467–1474.
81. Atoui A., Khoury A.I., Kallassy M., Lebrihi A. Quantifcation of Fusarium graminearum and Fusarium culmorum by real-time PCR system and zearalenone assessment in maize / / International Journal of Food Microbiology. 2012. Vol. 154, № 1–2. PP. 59–65.
