Aspergillus species in retail samples of pistachio, walnut, and hazelnut in Kerman, Iran

Document Type : Original Article

Author

Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran

Abstract

Nuts are among Iran’s most important crops consumed by many people due to their nutritional and nutraceutical properties. Fungi from the genus Aspergillus contaminate them during pre- and post-harvest stages. Aspergillus species are responsible for various agricultural products' secondary spoilage, and they can produce mycotoxins harmful to humans and animals. The present study evaluated the fungal contamination of nuts marketed in local stores in Kerman. Samples of pistachio, walnut, and hazelnut were collected throughout Kerman province, Iran, to characterize Aspergillus species contaminating nuts marketed in retail shops. Aspergillus species were examined by morphological and molecular criteria to explore the diversity of this genus. The phylogenetic relationships of these species were determined using sequences from partial β-tubulin and calmodulin sequences. Aspergillus species were identified as A. flavus, A. parasiticus, A. arachidicola, A. tamarii, A. caelatus, A. nomius, A. leporis, A. quadrilineatus, A. unguis, A. spelunceus, A.ochraceus, A. auricomus, A. westerdijkiae, A. montevidensis, A. pseudoglaucus, A. subalbidus and A. taichungensis. Populations of Aspergillus species on nuts, how these populations vary among different types of nuts, and their mycotoxin production potential are discussed.

Keywords


Ait Mimoune N, Arroyo-Manzanares N, Gámiz-Gracia L, García- Campaña AM, Bouti K, Sabaou N, Riba A. 2018. Aspergillus section Flavi and aflatoxins in dried figs and nuts in Algeria. Food Additives and Contaminants, Part B surveillance 11:119–125.
Amiri MJ, Karami M, Sadeghi E. 2013. Determination of AFB1 in peanut, almond, walnut, and hazelnut in kermanshah markets, Iran. International Journal of Agriculture and Crop Sciences 6: 1199–1202.
Baltaci C, İlyasoğlu H, Cavrar S. 2012. Aflatoxin levels in raw and processed hazelnuts in Turkey. Food Additives and Contaminants: Part B 5: 83-86.
Bayman P, Baker JL, Mahoney NE.  2002. Aspergillus on tree nuts: incidence and associations. Mycopathologia 155: 161-169
Chen A, Hubka V, Frisvad JC, Visagie CM, Houbraken J, Meijer M, Varga J, Demirel R, Jurjević Z, Kubátová A, Sklenár F, Zhou YG, Samson RA. 2017. Polyphasic taxonomy of Aspergillus section Aspergillus (formerly Eurotium), and its occurrence in indoor environments and food. Studies in Mycology 88: 37-135.
Cotty PJ, Jaime-Garcia R. 2007. Influences of climate on aflatoxin producing fungi and aflatoxin contamination. International Journal of Food Microbiology 119: 109-115.
Dijksterhuis J. 2007. Heat-resistant ascospores. In: Food Mycology, eds Dijksterhuis J, Samson RA. Boca Raton, FL: CRC Press, 115–132.
Doster M, Michailides T. 1994. Aspergillus molds and aflatoxins in pistachio nuts in California. Phytopathology 84: 583-590
Fani A,  Rezaei M, Moini A, Fani p, Mirzajani P, Malekirad A, Rafeie M, Atabak N.  2013. Aflatoxin occurrence in nuts consumed in Arak, Iran. International Journal of Food Nutrition and Safety 4: 91-97.
Ghitakou S, Koutras K, Kanellou E, Markaki P. 2006. Study of aflatoxin B1 and ochratoxin A production by natural microflora and Aspergillus parasiticus in black and green olives of Greek origin. Food Microbiology 23: 612-621.
Gholami-Shabani M, Shams–Ghahfarokhi M, Razzaghi–Abyaneh M. 2017. Aflatoxins and aflatoxigenic fungi in Iran: A systematic review of the past, present, and future. Mycologia Iranica 4: 65-84.
Glass NL, Donaldson GC. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61:1323–1330.
Habibi A, Afzali D. 2021. Aspergillus Section Flavi from Four Agricultural Products and Association of Mycotoxin and Sclerotia Production with Isolation Source. Current Microbiology 78: 3674-3685.
Hong SB, Cho HS, Shin HD, Frisvad JC, Samson RA. 2006. Novel Neosartorya species isolated from soil in Korea. International Journal of Systematic and Evolutionary Microbiology 56: 477–486.
Houbraken J, Kocsubé S, Visagie C, Yilmaz N, Wang X-C, Meijer M, Kraak B, Hubka V, Bensch K, Samson RA, Frisvad JC. 2020. Classification of Aspergillus, Penicillium, Talaromyces and related genera (Eurotiales): an overview of families, genera, subgenera, sections, series and species. Studies in Mycology 95: 5–169.
Houshyarfard M, Rouhani H, Falahati–Rastegar M, Malekzadeh–Shafaroudi S, Mehdikhani–Moghaddam E, Probst C. 2014. Characterization of Aspergillus section Flavi from pistachio soils in Iran. Journal of Plant Protection Research 54: 354–362.
Imani Nejad MI, Farahani AD. 2012. Aflatoxin in raw walnut kernels marketed in Tehran, Iran. Food Additives and Contaminants: Part B 5: 8-10.
Jamali M, Ebrahimi MA, Karimipour M, Shams–Ghahfarokhi M, Dinparast–Djadid N, Kalantari S, Pilehvar-Soltanahmadi Y, Amani A, Razzaghi-Abyaneh M. 2012. An insight into the distribution, genetic diversity, and mycotoxin production of Aspergillus section Flavi in soils of pistachio orchards. Folia Microbiologica 57: 27–36.
King AD, Hocking AD, Pitt JI. 1979. Dichloran-rose Bengal medium for enumeration and isolation of molds from foods. Applied and Environmental Microbiology 37: 959–964.
Klich MA, Pitt JI. 1988. A laboratory guide to common Aspergillus species and their teleomorphs. Commonwealth Scientific and Industrial Research Organization 15p.
Klich MA. 2002. Identification of common Aspergillus species. Centraalbureau voor Schimmelcultures, Utrecht.
Lombardi SJ,  Pannella G, Tremonte P, Mercurio I,  Vergalito F,  Caturano C,  Maiuro L,  Iorizzo M,  Succi M,  Sorrentino E, Coppola R. 2022. Fungi Occurrence in Ready-to-Eat Hazelnuts (Corylus avellana) From Different Boreal Hemisphere Areas. Frontiers in Microbiology 13: 900876-900876.
Mao J, He B, Zhang L, Li P, Zhang Q, Ding X,  Zhang W. 2016. A structure identification and toxicity assessment of the degradation products of aflatoxin B1 in peanut oil under UV irradiation. Toxins 8: 332.
Mojtahedi H, Rabie CJ, Lubben A, Steyn M, Danesh D. 1979. Toxic aspergilli from pistachio nuts. Mycopathologia 67: 123–127.
Morello LG, Sartori D, Martinez ALO, Vieira MLC, Taniwaki MH, Fungaro MHP. 2007. Detection and quantification of Aspergillus westerdijkiae in coffee beans based on selective amplification of β-tubulin gene by using real-time PCR. International Journal of Food Microbiology 119: 270-276.
Norlia M, Jinap S, Nor-Khaizura M, Radu S, Samsudin NI P, Farah FA. 2019. Aspergillus section Flavi and aflatoxins: Occurrence, detection, and identification in raw peanuts and peanut-based products along the supply chain. Frontiers in Microbiology 10: 2602.
Ostadrahimi A, Ashrafnejad F, Kazemi A, Sargheini N, Mahdavi R, Farshchian M, Mahluji S. 2014. Aflatoxin in raw and salt-roasted nuts (pistachios, peanuts and walnuts) sold in markets of Tabriz. Jundishapur Journal of Microbiology 7: 8674.
Ozay G. 2007. Aflatoxins in Turkish hazelnuts (Corylus avellana L.): A comprehensive study from orchard to the storage. International IUPAC Symposium on Mycotoxin and Phycotoxins.
Palumbo JD, Baker JL, Mahoney NE. 2006. Isolation of bacterial antagonists of Aspergillus flavus from almonds. Microbial Ecology 52: 45–52.
Palumbo JD, O’keeffe TL, Ho YS, Santillan CJ. 2015. Occurrence of ochratoxin A contamination and detection of ochratoxigenic Aspergillus species in retail samples of dried fruits and nuts. Journal of food protection 78: 836-842.
Perrone G, Susca A, Cozzi G, Ehrlich K, Varga J, Frisvad JC, Meijer M, Noonim P, Mahakarnchanakul W, Samson RA. 2007. Biodiversity of Aspergillus species in some important agricultural products. Studies in Mycology 59: 53-66.
Pitt JI, Hocking AD. 2009. Fungi and food spoilage, 3rd ed. Springer, New York.
Rahimi p, Sharifnabi B, Bahar M. 2007. Aspergillus species isolated from pistachio and determination of their aflatoxin production. Rostaniha 8: 30-34.
Rezaei M, Karimi F, Parviz M, Behzadi AA, Javadzadeh M, Mohammadpourfard I, Fallahzadeh A,  Mohammadi Aghamirlou H, Malekirad AA. 2014. An empirical study on aflatoxin occurrence in nuts consumed in Tehran, Iran. Health 6: 649-653.
Saffari E, Madani M, Karbasizade VShakib S. 2021. Detection of fungal and bacterial contamination of hazelnut and determination of aflatoxin B by HPLC method in Isfahan, Iran. Current Medical Mycology 7: 1-5.
Saleemullah AI, Iqtidar A, Hamidullah Shah K. 2006. Aflatoxin contents of stored and artificially inoculated cereals and nuts. Food Chemistry 98: 699–703.
Samson RA, Visagie CM, Houbraken J, Hong SB, Hubka V, Klaassen CHW, Perrone G, Seifert KA, Susca A, Tanney JB, Varga J, Kocsubé S, Szigeti G, Yaguchi T, Frisvad JC. 2014. Phylogeny, identification and nomenclature of the genus Aspergillus. Studies in Mycology 78: 141–173.
Taghizadeh SF, Rezaee R, Badibostand H, Karimi G. 2020. Aflatoxin B1 in walnuts: a probabilistic cancer risk assessment for Iranians. Toxicological and Environmental Chemistry 102: 506-519.
Shakeri Z1, Rahimi E, Shakerian A. 2019. Evaluation of aflatoxin content in pistachio, almond, hazelnut and walnut in Isfahan. Journal of Food Hygiene 9: 61–69.
Swofford DL. 2002. PAUP*: phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland.
Turan A. 2018. Effect of drying methods on nut quality of hazelnuts (Corylus avellana L.). Journal of Food Science and Technology 55: 4554–4565.
Varga J, Juhász A, Kevei F, Kozakiewicz Z. 2004. Molecular diversity of agriculturally important Aspergillus species. European Journal of Plant Pathology 110: 627– 640.
Verweij PE, Varga J,  Houbraken J, Rijs AJMM, Verduynlunel FM, Blijlevens NMA, Shea YR, Holland SM, Warris A, Melchers WJG,  Samson RA. 2008. Emericella quadrilineata as cause of invasive aspergillosis. Emerging infectious diseases. 14: 566.
Visconti A, Perrone G, Cozzi G, Solfrizzo  M. 2008. Managing ochratoxin A risk in the grape-wine food chain. Food Additives and Contaminants 25: 193-202.