THE NATURAL OCCURRENCE OF PENICILLIUM SPP. METABOLITES IN MAIZE KERNELS ORIGINATING FROM SERBIA

  • Jovana Kos Institute of food technology in Novi Sad, University of Novi Sad
Keywords: safety, weather conditions, Vojvodina Province, LC-MS/MS, mycotoxins, oxaline

Abstract


Maize can be contaminated with a wide range of fungal secondary metabolites that decrease the quality and safety of maize and maize-derived products. The increase of natural fungal metabolites occurrence in maize, influenced by climate changes, is recognized as a significant issue in recent years. Therefore, the main aim of this study was to investigate the influence of weather conditions on the natural occurrence of Penicillium spp. metabolites in maize kernel samples. The survey was conducted for two maize vegetation seasons 2016 and 2017. In total 458 maize samples were analyzed by liquid chromatography-tandem mass spectrometry method. The samples originated from the Autonomous Province of Vojvodina, and regions of Bačka, Srem, and Banat. Among 45 Penicillium metabolites investigated 16 and 18 were detected in samples from 2016 and 2017, respectively. The most commonly occurring Penicillium metabolite in both years was oxaline, which was detected in more than 90% of analyzed samples. Questiomycin A, 7-hydroxypestalotin, pestalotin, and mycophenolic acid were also very frequently detec-ted Penicillium metabolites. This is one of the unique studies in the Republic of Serbia, as well as in this part of Europe, investigating the occurrence of a great number of Penicillium metabolites in maize samples.

References

Abdallah, M. F., Girgin, G., Baydar, T., Krska, R., & Sulyok, M. (2017). Occurrence of multiple mycotoxins and other fungal metabolites in animal feed and maize samples from Egypt using LC‐MS/MS. Journal of the Science of Food and Agriculture, 97(13), 4419-4428. https://doi.org/10.1002/jsfa.8293>

Barkai-Golan, R. (2008). Penicillium mycotoxins. In R. Barkai-Golan & N. Paster (Eds.), Mycotoxins in fruits and vegetables (pp. 153-183). Cambridge, MA: Academic Press.

Cline, J. C., Nelson, J. D., Gerzon, K., Williams, R. H., & Delong, D. C. (1969). In vitro antiviral activity of mycophenolic acid and its reversal by guanine-type compounds. Applied Microbiology, 18(1), 14-20. https://doi.org/10.1128/am.18.1.14-20.1969

Degani, O., Regev, D., & Dor, S. (2021). The microflora of maize grains as a biological barrier against the late wilt causal agent, Magnaporthiopsis maydis. Agronomy, 11(5), 965. https://doi.org/10.3390/agronomy11050965

EFSA Panel on Contaminants in the Food Chain (CONTAM). (2012). Scientific Opinion on the risks for public and animal health related to the presence of citrinin in food and feed. EFSA Journal, 10(3), 2605. https://doi.org/10.2903/j.efsa.2012.2605>

El Khoury, A., & Atoui, A. (2010). Ochratoxin A: General overview and actual molecular status. Toxins2(4), 461-493. https://doi.org/10.3390/toxins2040461

European Commission (2006). Commission Regulation 2006/401/EC of 23 February 2006 laying down the methods of sampling and analysis for the official control of the levels of mycotoxins in foodstuffs. Official Journal of the European Union, L 70, 12-34.

Frisvad, J. C. (2018). A critical review of producers of small lactone mycotoxins: Patulin, penicillic acid and moniliformin. World Mycotoxin Journal11(1), 73-100.  https://doi.org/10.3920/WMJ2017.2294>

Getachew, A., Chala, A., Hofgaard, I. S., Brurberg, M. B., Sulyok, M., & Tronsmo, A. M. (2018). Multimycotoxin and fungal analysis of maize grains from south and southwestern Ethiopia. Food Additives & Contaminants: Part B, 11(1), 64-74. https://doi.org/10.1080/19393210.2017.1408698

Gräbsch, C., Wichmann, G., Loffhagen, N., Herbarth, O., & Müller, A. (2006). Cytotoxicity assessment of gliotoxin and penicillic acid in Tetrahymena pyriformis. Environmental Toxicology: An International Journal, 21(2), 111-117. https://doi.org/10.1002/tox.20162

Houbraken, J., de Vries, R. P., & Samson, R. A. (2014). Modern taxonomy of biotechnologically important Aspergillus and Penicillium species. Advances in Applied Microbiology, 86, 199-249. https://doi.org/10.1016/B978-0-12-800262-9.00004-4" target="_blank" rel="noopener">https://doi.org/10.1016/B978-0-12-800262-9.00004-4>

IARC, International Agency for Research on Cancer (1986). Some naturally occurring and synthetic food components, coumarins ultraviolet radiation. In: Monographs of the evaluation of the carcinogenic risk of chemical to human, vol. 40. Lyon, France, pp. 83-98.

IARC, International Agency for Research on Cancer (2012). Chemical agents and related occupations, a review of human carcinogens in IARC monograph on the evaluation of carcinogenic risk to humans, Vol. 100F, 1-628.

Janić Hajnal, E., Kos, J., Malachová, A., Steiner, D., Stranska, M., Krska, R., & Sulyok, M. (2020). Mycotoxins in maize harvested in Serbia in the period 2012-2015. Part 2: Non-regulated mycotoxins and other fungal metabolites. Food Chemistry, 317, 126409. https://doi.org/10.1016/j.foodchem.2020.126409" target="_blank" rel="noopener">https://doi.org/10.1016/j.foodchem.2020.126409>

Kifer, D., Sulyok, M., Jakšić, D., Krska, R., & Šegvić Klarić, M. (2021). Fungi and their metabolites in grain from individual households in Croatia. Food Additives & Contaminants: Part B, 14(2), 98-109. https://doi.org/10.1080/19393210.2021.1883746

Kos, J., Hajnal, E. J., Malachová, A., Steiner, D., Stranska, M., Krska, R., Poschmaier, B., & Sulyok, M. (2020). Mycotoxins in maize harvested in Republic of Serbia in the period 2012-2015. Part 1: Regulated mycotoxins and its derivatives. Food Chemistry, 312, 126034. https://doi.org/10.1016/j.foodchem.2019.126034" target="_blank" rel="noopener">https://doi.org/10.1016/j.foodchem.2019.126034>

Kos, J., Janić Hajnal, E., Radić, B., Pezo, L., Malachová, A., Krska, R., & Sulyok, M. (2021). Two years study of Aspergillus metabolites prevalence in maize from the Republic of Serbia. Journal of Food Processing and Preservation, 46(10), e15897. https://doi.org/10.1111/jfpp.15897

Krnjaja, V., Lukić, M., Delić, N., Tomić, Z., Mandić, V., Bijelić, Z., & Gogić, M. (2015). Mycobiota and mycotoxins in freshly harvested and stored maize. Biotechnology in Animal Husbandry, 31(2), 291-302.  https://doi.org/10.2298/BAH1502291K

Labuda, R., Bacher, M., Rosenau, T., Gasparotto, E., Gratzl, H., Doppler, M., Sulyok, M., Kubatova, A., Berger, H., Cank, K., Raja, H., Oberlies, N., Schuller, C., & Strauss, J. (2021). Polyphasic approach utilized for the identification of two new toxigenic members of Penicillium section Exilicaulis, P. krskae and P. silybi spp. nov. Journal of Fungi, 7(7), 557. https://doi.org/10.3390/jof7070557

Ljubojević, D., Jakšić, S., Živkov-Balos, M., Mihaljev, Z., Puvača, N., Prica, N., & Kapetanov, M. (2014). Presence of aflatoxins, zearalenone, ochratoxin a, and trichothecenes in corn (Zea Mays) in Republic of Serbia. In Proceedings of the XVI International Symposium “Feed Technology”, (pp. 28-30), Novi Sad, Serbia.

Machihara, K., Tanaka, H., Hayashi, Y., Murakami, I., & Namba, T. (2017). Questiomycin A stimulates sorafenib-induced cell death via suppression of glucose-regulated protein 78. Biochemical and Biophysical Research Communications, 492(1), 33-40. https://doi.org/10.1016/j.bbrc.2017.08.042>

Maslac, T. (2019). Serbia/Grain and feed annual/ Annual report on wheat, corn and barley. GAIN Report. Global Agricultural Information Network. US Department of Agriculture (USDA) Foreign Agricultural Service. Retrieved from https://apps.fas.usda.gov/newgainapi/api/report/downloadreportbyfilename?filename=Grain%20and%20Feed%20Annual_Belgrade_Serbia_3-29-2019.pdf>

Maširević, S., Medić-Pap, S., & Birvalski, S. (2012). Mycoflora of maize seed. Research Journal of Agricultural Science, 44(2), 58-62.

Matić, J., Mandić, A., Mastilović, J., Mišan, A., Beljkaš, B., & Milovanović, I. (2008). Contaminations of raw materials and food products with mycotoxins in Serbia. Food and Feed Research, 35(2), 65-70.

Matumba, L., Sulyok, M., Monjerezi, M., Biswick, T., & Krska, R. (2015). Fungal metabolites diversity in maize and associated human dietary exposures relate to micro-climatic patterns in Malawi. World Mycotoxin Journal, 8(3), 269-282. https://doi.org/10.3920/WMJ2014.1773

Medić-Pap, S., Maširević, S., & Šofhauzer, I. (2011). Mycoflora of commercial maize seed in 2010. Zbornik Matice srpske za prirodne nauke, 120, 127-133. https://doi.org/10.2298/ZMSPN1120129M>

Medina, Á., Rodríguez, A., & Magan, N. (2015). Climate change and mycotoxigenic fungi: Impacts on mycotoxin production. Current Opinion in Food Science, 5, 99-104. https://doi.org/10.1016/j.cofs.2015.11.002" target="_blank" rel="noopener">https://doi.org/10.1016/j.cofs.2015.11.002>

Pepeljnjak, S., & Cvetnić, Z. (1985). The mycotoxicological chain and contamination of food by ochratoxin A in the nephropathic and non-nephropathic areas in Yugoslavia. Mycopathologia, 90(3), 147-153. https://doi.org/10.1007/bf00436730>

Perrone, G., & Susca, A. (2017). Penicillium species and their associated mycotoxins. Mycotoxigenic Fungi, 1542, 107-119. https://doi.org/ style="background-image: initial; background-position: initial; background-size: initial; background-repeat: initial; background-attachment: initial; background-origin: initial; background-clip: initial;">10.1007/978-1-4939-6707-0_5

Pfohl-Leszkowicz, A., Petkova-Bocharova, T., Chernozemsky, I. N., & Castegnaro, M. (2002). Balkan endemic nephropathy and associated urinary tract tumours: a review on aetiological causes and the potential role of mycotoxins. Food Additives & Contaminants19(3), 282-302. https://doi.org/10.1080/02652030110079815

Plestina, R., Ceović, S., Gatenbeck, S., Habazin-Novak, V., Hult, K., Hökby, E., Krogh, P., & Radić, B. (1990). Human exposure to ochratoxin A in areas of Yugoslavia with endemic nephropathy. Journal of Environmental Pathology, Toxicology and Oncology: Official Organ of the International Society for Environmental Toxicology and Cancer10(3), 145-148.

Radić, B., Kos, J., Janić Hajnal, E., Malachová, A., Krska, R., & Sulyok, M. (2021). Fusarium metabolites in maize from regions of Northern Serbia in 2016-2017. Food Additives & Contaminants: Part B, 14(4), 295-305. https://doi.org/10.1080/19393210.2021.1961877

Republic Hydrometeorological Service of Serbia. (2016-2017). Agro-meteorological conditions in the 2016/2017 years in the territory of the Republic of Serbia. [accessed 2022 Dec 15]. http://www.hidmet.gov.rs/

Schneweis, I., Meyer, K., Hörmansdorfer, S., & Bauer, J. (2000). Mycophenolic acid in silage. Applied and Environmental Microbiology, 66(8), 3639-3641. https://doi.org/10.1128/AEM.66.8.3639-3641.2000>

Stiborová, M., Arlt, V. M., & Schmeiser, H. H. (2016). Balkan endemic nephropathy: an update on its aetiology. Archives of Toxicology90(11), 2595-2615. https://doi.org/ lang="EN-US" style="font-size: 10.0pt; font-family: 'Times New Roman','serif';">10.1007/s00204-016-1819-3

Sulyok, M., Krska, R., & Schuhmacher, R. (2007). A liquid chromatography/tandem mass spectrometric multi-mycotoxin method for the quantification of 87 analytes and its application to semi-quantitative screening of moldy food samples. Analytical and Bioanalytical Chemistry, 389(5), 1505-1523. https://doi.org/10.1007/s00216-007-1542-2>

Sulyok, M., Stadler, D., Steiner, D., & Krska, R. (2020). Validation of an LC-MS/MS-based dilute-and-shoot approach for the quantification of > 500 mycotoxins and other secondary metabolites in food crops: Challenges and solutions. Analytical and Bioanalytical Chemistry412(11), 2607-2620. https://doi.org/10.1007/s00216-020-02489-9

Toghueo, R. M. K., & Boyom, F. F. (2020). Endophytic Penicillium species and their agricultural, biotechnological, and pharmaceutical applications. 3 Biotech, 10(3), 1-35. https://doi.org/10.1007/s13205-020-2081-1>

Tola, M., & Kebede, B. (2016). Occurrence, importance and control of mycotoxins: A review. Cogent Food & Agriculture2(1), 1191103. https://doi.org/10.1080/23311932.2016.1191103>

Udovički, B., Audenaert, K., De Saeger, S., & Rajković, A. (2018). Overview on the Mycotoxins Incidence in Serbia in the Period 2004-2016. Toxins10(7), 279. https://doi.org/10.3390/toxins10070279

Van der Merwe, K. J., Steyn, P. S., Fourie, L., Scott, D. B., & Theron, J. J. (1965). Ochratoxin A, a toxic metabolite produced by Aspergillus ochraceus Wilh. Nature, 205(4976), 1112-1113.

Wierzbińska, A. (2017). Evaluation of bioactive potential of a secondary metabolite produced by Penicillium nordicum (Doctoral dissertation). Instituto Politécnico de Bragança; Portugal.

Published
2022/11/15
Section
Original research paper