Sains Malaysiana 43(1)(2014): 89–94

 

Production of Major Mycotoxins by Fusarium Species Isolated  from

Wild Grasses in Peninsular Malaysia

(Penghasilan Mikotoksin Utama oleh Spesies Fusarium yang Dipencilkan daripada Rumput

Liar di Semenanjung Malaysia)

 

I. NOR AZLIZA, R. HAFIZI, M. NURHAZRATI & B. SALLEH*

School of Biological Sciences, Universiti Sains Malaysia, 11800 Minden,

Penang, Malaysia

 

Received: 11 September 2012/Accepted: 19 April 2013

 

ABSTRACT

The Fusarium species are notoriously known for causing various plants and animal diseases and producing a number of harmful mycotoxins. The mycotoxins production by species recovered from non-agricultural hosts such as wild grasses have hitherto never been given attention. We examined 30 strains representing 12 Fusarium species i.e. F. oxysporum, F. solani, F. semitectum, F. nelsonii, F. compactum, F. equiseti, F. chlamydosporum, F. proliferatum, F. subglutinans, F. sacchari, F. lateritium and F. incarnatum-equiseti species complex isolated from wild grasses in Peninsular Malaysia for the production of four major mycotoxins i.e. moniliformin (MON), fumonisin B1 (FB1), zearalenone (ZEN) and beauvericin (BEA) using TLC and HPLC techniques. BEA was the highest frequency of mycotoxin detected, followed by MON, ZEN and FB1. This study also presented the first report of BEA production by F. solani, F. compactum and F. chlamydosporum. All mycotoxins were not produced by F. nelsonii and F. lateritium. All Fusarium species were isolated from asymptomatic grasses, hence they are likely to exist as endophytes or latent pathogens.

 

Keywords: Fusarium; grasses; mycotoxins; Peninsular Malaysia

 

ABSTRAK

Spesies Fusarium dikenali sebagai penyebab pelbagai penyakit tumbuhan dan haiwan serta menghasilkan beberapa mikotoksin yang berbahaya. Penghasilan mikotoksin oleh spesies yang dipencilkan daripada perumah bukan pertanian seperti rumput liar, sehingga kini tidak pernah diberi perhatian. Kami memeriksa 30 strain mewakili 12 spesies Fusarium iaitu F. oxysporum, F. solani, F. semitectum, F. nelsonii, F. compactum, F. equiseti, F. chlamydosporum, F. proliferatum, F. subglutinans, F. sacchari, F. lateritium dan F. incarnatum-equiseti kompleks spesies yang dipencilkan daripada rumput liar di Semenanjung Malaysia untuk penghasilan empat mikotoksin utama iaitu moniliformin (MON), fumonisin B1 (FB1), zearalenon (ZEN) dan beauvericin (BEA) menggunakan teknik kromatografi lapisan nipis (TLC) dan kromatografi cecair berprestasi tinggi (HPLC). BEA merupakan mikotoksin yang paling kerap dikesan, diikuti oleh MON, ZEN dan FB1. Kajian ini juga merupakan laporan pertama penghasilan BEA oleh F. solani, F. compactum dan F. chlamydosporum. Kesemua mikotoksin tidak dihasilkan oleh F. nelsonii dan F. lateritium. Semua spesies Fusarium tersebut dipencilkan daripada rumput yang tidak menunjukkan gejala penyakit, maka ia mungkin wujud sebagai endofit atau patogen pendam.

 

Kata kunci: Fusarium; mikotoksin; rumput; Semenanjung Malaysia

REFERENCES

Bottalico, A., Visconti, A., Logrieco, A., Solfrizzo, M. & Mirocha, J. 1985. Occurrence of zearalenols (diastereomeric mixture) in corn stalk rot and their production by associated Fusarium species. Applied and Environmental Microbiology 49: 547- 551.

Burmeister, H.R., Ciegler, A. & Vesonder, R.F. 1979. Moniliformin, a metabolite of Fusarium moniliforme NRRL 6322 - purification and toxicity. Applied and Environmental Microbiology 37: 11-13.

Bushnell, G.W., Li, Y.L. & Poulton, G.A. 1984. Pyrones. X. Lateropyrone, a new antibiotic from the fungus Fusarium lateritium Nees. Canadian Journal of Chemistry 62: 2101- 2106.

Chelkowski, J., Zawadzki, M., Zajkowski, P., Logrieco, A. & Bottalico, A. 1990. Moniliformin production by Fusarium species. Mycotoxin Research 6: 41-45.

Dacasto, M., Rolando, P., Nachtmann, C., Ceppa, L. & Nebbia, C. 1995. Zearalenone mycotoxicosis in piglets suckling sows fed contaminated grain. Veterinary and Human Toxicology 37: 359-361.

Darnetty., Dian Mariana, M.N., Nur Ain Izzati, M.Z., Nor Azliza, I., Nik Mohd Izham, N.M. & Salleh, B. 2008. Diversity of Fusarium species associated with ear rot of corn in Indonesia and Malaysia. In Proceedings of 6th IMT-GT Conference, Penang, 26-28 August, edited by Abd Wahab, A.R., Chan, L.K., Shaida Fariza, S., Ahmad Ramli, M.Y., Amirul Al-Ashraf, B., Zairi, J., Rashidah, A.R., Sudesh, K., Siti Azizah, M.N., Darah, L., Zary Shariman, Y., Aileen, T.S.H. & Alexander, C.

Desjardins, A.E. 2006. Fusarium Mycotoxins: Chemistry, Genetics, and Biology. St. Paul, Minnesota: Amer Phytopathological Society.

Desjardins, A.E., Plattner, R.D. & Nelson, P.E. 1997. Production of fumonisin B1 and moniliformin by Gibberella fujikuroi from rice from various geographic areas. Applied and Environmental Microbiology 63: 1838-1842.

Engelhardt, J.A., Carlton, W.W. & Tuite, J.F. 1989. Toxicity of Fusarium moniliforme var. subglutinans for chicks, ducklings, and turkey poults. Avian Diseases 33: 357-360.

Frisvad, J.C. & Thrane, U. 2002. Mycotoxin production by common filamentous fungi. In Introduction to Food- and Air-borne Fungi, edited by Samson, R.A., Hoekstra, E.S., Frisvad, J.C., Filtenborg, O. Utrecht: Centraal bereau voor Schimmelcultures. pp. 321-331.

Gupta, S., Krasnoff, B., Underwood, N.L., Renwick, J.A.A. & Roberts, D.W. 1991. Isolation of beauvericin as an insect toxin from Fusarium semitectum and Fusarium moniliforme var. subglutinans. Mycopathologia 115: 185-189.

Hestbjerg, H., Nielsen, K.F., Thrane, U. & Elmholt, S. 2002. Production of trichothecenes and other secondary metabolites by Fusarium culmorum and Fusarium equiseti on common laboratory media and a soil organic matter agar: An ecological interpretation. Journal of Agricultural and Food Chemistry 50: 7593 -7599.

Jestoi, M. 2008. Emerging Fusarium-mycotoxins fusaproliferin, beauvericin, enniatins, and moniliformin: A review. Critical Reviews in Food Science and Nutrition 48: 21-49.

Jimenez, M., Huerta, T. & Mateo, R. 1997. Mycotoxin production by Fusarium species isolated from bananas. Applied and Environmental Microbiology 63: 364-369.

Jonsson, M., Jestoi, M., Nathanail, A.V., Kokkonen, U-M., Koivisto, P., Karhunen, P. & Peltonen, K. 2012. Application of OECD Guideline 423 in assessing the acute oral toxicity of moniliformin. Food and Chemical Toxicology 53: 27-32.

Kosiak, E.B., Holst-Jensen, A., Rundburget, T., Jaen, M.T.G. & Torp, M. 2005. Morphological, chemical and molecular differentiation of Fusarium equiseti isolated from Norwegian cereals. International Journal of Food Microbiology 99: 195-206.

Lee, K-E., Kim, B.H. & Lee, C. 2010. Occurrence of Fusarium mycotoxin beauvericin in animal feeds in Korea. Animal Feed Science and Technology 157: 190-194.

Lemmens-Gruber, R., Rachoy, B., Steininger, E., Kouri, K., Saleh, P., Krska, R., Josephs, R. & Lemmens, M. 2000. The effect of the Fusarium metabolite beauvericin on electromechanical and physiological properties in isolated smooth and heart muscle preparations of guinea pigs. Mycopathologia 49: 5-12.

Leslie, J.F. & Summerell, B.A. 2006. The Fusarium Laboratory Manual. UK: Blackwell Publishing Ltd.

Leslie, J.F., Marasas, W.F.O., Shephard, G.S., Sydenham, E.W., Stockenstrom, S. & Thiel, P.G. 1996. Duckling toxicity and the production of fumonisin and moniliformin by isolates in the A and F mating populations of Gibberella fujikuroi (Fusarium moniliforme). Applied and Environmental Microbiology 62: 1182-1187.

Leslie, J.F., Zeller, K.A., Logrieco, A., Mulè, G., Moretti, A. & Ritieni, A. 2004. Species diversity and toxin production by strains in the Gibberella fujikuroi species complex isolated from native prairie grasses in Kansas. Applied and Environmental Microbiology 70: 2254-2262.

Ledoux, D.R., Bermudez, A.J., Rottinghaus, G.E., Broomhead, J. & Bennett, G.A. 1995. Effects of feeding Fusarium fujikuroi culture material, containing known levels of moniliformin, in young broiler chicks. Poultry Science 74: 297-305.

Lew, H., Chelkowski, J., Pronczuk, P. & Edinger, W. 1996. Occurrence of the mycotoxin moniliformin in maize (Zea mays L.) ears infected by Fusarium subglutinans (Wollenw. & Reinking). Food Additives and Contaminants 13: 321-324.

Li, Y.C., Ledoux, D.R., Bermudez, A.J., Fritsche, K.L. & Rottinghaus, G.E. 2000. The individual and combined effects of fumonisin B1 and moniliformin on performance and selected immune parameters in turkey poults. Poultry Science 79: 871-878.

Liew, K.W., Mak, C. & Ho, Y.W. 1998. Status of banana Fusarium wilt in Malaysia. In Proceedings of the First Banana Seminar, 23 – 25 November, edited by Zakaria, W., Mahmud, T.M.M., Siti, K.D., Nor ‘Aini, M.F. & Marziah, M.

Logrieco, A., Moretti, A., Castellá, G., Kostecki, M., Golinski, P., Ritieni, A. & Chelkowski, J. 1998. Beauvericin production by Fusarium species. Applied and Environmental Microbiology 64: 3084-3088.

Logrieco, A., Rizzo, A., Ferracane, R. & Ritieni, A. 2002. Occurrence of beauvericin and enniatins in wheat affected by Fusarium avenaceum head blight. Applied and Environmental Microbiology 68: 82-85.

Macchia, L., Caiffa, M.F., Fornelli, F., Calo, L., Nenna, S., Moretti, A., Logrieco, A. & Tursi, A. 2002. Apoptosis induced by the Fusarium mycotoxin beauvericin in mammalian cells. Journal of Applied Genetics 43: 363-371.

Marasas, W.F.O., Nelson, P.E. & Toussoun, T.A. 1984. Toxigenic Fusarium Species: Identity and Mycotoxicology. University Park, Pennsylvania: The Pennsylvania State University Press.

Marasas, W.F.O., Kellerman, T.S. & Gelderbom, W.C.A. 1988. Leukoencephalomalacia in a horse induced by fumonisin B1 isolated from Fusarium moniliforme. Onderstepoort Journal of Veterinary Research 43: 113-122.

Moretti, A., Belisario, A., Tafuri, A., Ritieni, A., Corazza, L. & Logrieco, A. 2002. Production of beauvericin by different races of Fusarium oxysporum f. sp. melonis, the Fusarium wilt agent of muskmelon. European Journal of Plant Pathology 108: 661-666.

Moretti, A., Logrieco, A., Bottalico, A., Ritieni, A., Fogliano, V. & Randazzo, G. 1996. Diversity in beauvericin and fusaproliferin production by different populations of Gibberella fujikuroi (Fusarium section Liseola). Sydowia 30: 44-56.

Mubatanhema, W., Moss, M.O., Frank, M.J. & Wilson, D.M. 1999. Prevalence of Fusarium species of the Liseola section on Zimbabwean corn and their ability to produce the mycotoxins zearalenone, moniliformin and fumonisin B1. Mycopathologia 148: 157-163.

Munkvold, G., Stahr, H.M., Logrieco, A., Moretti, A. & Ritieni, A. 1998. Occurrence of fusaproliferin and beauvericin in Fusarium-contaminated livestock feed in Iowa. Applied and Environmental Microbiology 64: 3923-3926.

Negedu, A., Atawodi, S.E., Ameh, J.B., Umoh, V.J. & Tanko, H.Y. 2011. Economic and health perspectives of mycotoxins: A review. Continental Journal of Biomedical Sciences 5: 5-26.

Nelson, P.E., Plattner, R.D., Shackelford, D.D. & Desjardins, A.E. 1992. Fumonisin B1 production by Fusarium species other than F. moniliforme in section Liseola and some related species. Applied and Environmental Microbiology 58: 984-989.

Nur Ain Izzati, M.Z. & Wan Hasmida, W.I. 2011. Isolation of microfungi from traditional vegetables and secondary metabolites produced by Fusarium species. Sains Malaysiana 40: 437-444.

Nur Ain Izzati, M.Z., Azmi, A.R. & Salleh, B. 2008. Bakanae disease of rice in Malaysia and Indonesia: Etiology of the causal agent based on morphological, physiological and pathogenicity characteristics. Journal of Plant Protection Research 48: 491-501.

Nur Ain Izzati, M.Z., Siti Nordahliawate, M.S., Nor Azliza, I. & Salleh, B. 2009. Distribution and diversity of Fusarium spp. associated with grasses in ten states throughout Peninsular Malaysia. Biotropia 16: 55-64.

O'Donnell, K., Kistler, H.C., Cigelnik, E. & Ploetz, R.C. 1998. Multiple evolutionary origins of the fungus causing Panama disease of banana: Concordant evidence from nuclear and mitochondrial gene genealogies. Proceedings of the National Academy of Sciences of the United States of America 95: 2044-2049.

Pieper, R., Kleinkauf, H. & Zocher, R. 1992. Enniatin synthetases from different Fusaria exhibiting distinct amino acid specificities. Journal of Antibiotics 45: 1273-1277.

Reddy, K.R.N. & Salleh, B. 2011. Co-occurrence of moulds and mycotoxins in corn grain used for animal feeds in Malaysia. Journal of Veterinary Advances 10: 668-673.

Reynoso, M.M., Torres, A.M. & Chulze, S.N. 2004. Fusaproliferin, beauvericin and fumonisin production by different mating populations among the Gibberella fujikuroi species complex isolated from maize. Mycological Research 108: 154-160.

Salleh, B. & Sulaiman, B. 1984. Fusaria associated with naturally diseased plants in Penang. Journal of Plant Protection in the Tropics 1: 47-53.

Sharma, D., Asrani, R.K., Ledoux, D.R., Rottinghaus, G.E. & Gupta, V.K. 2012. Toxic interaction between fumonisin B1 and moniliformin for cardiac lesions in Japanese quail. Avian Diseases 56: 545-554.

Shephard, G.S., Sewram, V., Nieuwoudt, T.W., Marasas, W.F.O. & Ritieni, A. 1999. Production of the mycotoxins fusaproliferin and beauvericin by South African isolates in the Fusarium section Liseola. Journal of Agriculture and Food Chemistry 47: 5111-5115.

Siti Nordahliawate, M.S., Nur Ain Izzati, M.Z., Azmi, A.R. & Salleh, B. 2008. Distribution, morphological characteristics and pathogenicity of Fusarium sacchari associated with pokkah boeng disease on sugarcane in Peninsular Malaysia. Pertanika Journal of Tropical Agricultural and Science 31: 271-278.

Smith, J.E., Lewis, C.W., Anderson, J.G. & Solomons, G.L. 1994. Mycotoxins in Human Nutrition and Health. Directorate General XII. Science, Research and Development. EUR 16048 EN.

Soleimany, F., Jinap, S., Rahmani, A. & Khatib, A. 2011. Simultaneous detection of 12 mycotoxins in cereals using RP-HPLC-PDA-FLD with PHRED and a post-column derivatization system. Food Additives and Contaminants 28: 494-501.

Sopterean, L.M & Puia, C. 2012. The major mycotoxins produced by Fusarium fungi and their effects. ProEnvironment 5: 55-59.

Sydenham, E.W., Thiel, P.G., Marasas, W.F.O., Shephard, G.S., van Schalkwyk, D.J. & Koch, K.R. 1990. Natural occurrence of some Fusarium mycotoxins in corn from low and high oesophageal cancer prevalence areas of the Transkei, Southern Africa. Journal of Agricultural and Food Chemistry 38: 1900-1903.

Tan, D.C., Flematti, G.R., Ghisalberti, E.L., Sivasithamparam, K., Chakraborty, S., Obanor, F., Jayasena, K. & Barbetti, M.J. 2012. Mycotoxins produced by Fusarium spp. associated with Fusarium head blight of wheat in Western Australia. Mycotoxin Research 28: 89-96.

Thrane, U. 1986. Detection of toxigenic Fusarium isolates by thin layer chromatography. Letters in Applied Microbiology 3: 93-96.

Tseng, T.C., Tu, J.C. & Tzean, S.S. 1995. Mycoflora and mycotoxins in dry bean (Phaseolus vulgaris) produced in Taiwan and in Ontario, Canada. Botanical Bulletin of Academia Sinica 36: 229-234.

 

 

*Corresponding author; email: sallehb@usm.my

 

previous