Fumonisin B1 Production by Fusarium Species and Mycotoxigenic Effect on Larval Zebrafish

Main Article Content

Najihah Azman
Nur Ain Izzati Mohd Zainudin
Wan Norhamidah Wan Ibrahim

Abstract


Fumonisin B1 (FB1) is a common mycotoxin produced by Fusarium species particularly F. proliferatum and F. verticillioides. The toxin produced can cause adverse effects on humans and animals. The objectives of this study were to detect the production of FB1 based on the amplification of FUM1 gene, to quantify FB1 produced by the isolates using Ultra-fast Liquid Chromatography (UFLC) analysis, to examine the embryotoxicity effect of FB1 and to determine EC50 toward the larvae of zebrafish (Danio rerio). Fifty isolates of Fusarium species were isolated from different hosts throughout Malaysia. Successful amplification of the FUM1 gene showed the presence of this gene (800 bp) in the genome of 48 out of 50 isolates. The highest level of FB1 produced by F. proliferatum isolate B2433 was 6677.32 ppm meanwhile F. verticillioides isolate J1363 was 954.01 ppm. From the assessment of embryotoxicity test of FB1 on larvae of zebrafish, five concentrations of FB1 (0.43 ppm, 0.58 ppm, 0.72 ppm, 0.87 ppm and 1.00 ppm) were tested. Morphological changes of the FB1 exposed-larvae were observed at 24 to 168 hpf. The mortality rate and abnormality of zebrafish larvae were significantly increased at 144 hpf exposure. Meanwhile, the spontaneous tail coiling showed a significant difference. There were no significant differences in the heartbeat rate. As a conclusion, the presence of FUM1 in every isolate can be detected by FUM1 gene analysis and both of the species produced different concentrations of FB1. This is the first report of FB1 produced by Fusarium species gave a significant effect on zebrafish development.


Article Details

How to Cite
Fumonisin B1 Production by Fusarium Species and Mycotoxigenic Effect on Larval Zebrafish. (2020). Tropical Life Sciences Research, 31(3), 91–107. https://doi.org/10.21315/tlsr2020.31.3.7
Section
Original Article

References

Bakos K, Kovacs R, Staszny A, Sipos D K, Urbanyi B, Muller F, Csenki Z and Kovacs B. (2013). Developmental toxicity and estrogenic potency of zearalenone in zebrafish (Danio rerio). Aquatic Toxicology 136–137: 13–21. https://doi.org/10.1016/j.aquatox.2013.03.004

Brustein E, Saint-Amant L, Buss R R, Chong M, McDearmid J R and Drapeau P. (2003). Steps during the development of the zebrafish locomotor network. Journal of Physiology-Paris 97(1): 77–86. https://doi.org/10.1016/j.jphysparis.2003.10.009

Chakraborty A, Uechi T, Higa S, Torihara H and Kenmochi N. (2009). Loss of ribosomal protein L11 affects zebrafish embryonic development through a p53-dependent apoptotic response. PLOS ONE 4(1): e4152. https://doi.org/10.1371/journal.pone.0004152

Choi J H, Lee S, Nah J Y, Kim H K, Paek J S and Lee S. (2018). Species composition of and fumonisin production by the Fusarium fujikuroi species complex isolated from Korean cereals. International Journal of Food Microbiology 267: 62–69. https://doi.org/10.1016/j.ijfoodmicro.2017.12.006

Dissanayake M L M C, Tanaka S and Ito S. (2009). Fumonisin B1 production by Fusarium proliferatum strains isolated from Allium fistulosum plants and seeds in Japan. Letters in Applied Microbiology 48(5): 598–604. https://doi.org/10.1111/j.1472-765X.2009.02576.x

Glenn A E, Zitomer N C, Zimeri A M, Williams L D, Riley R T and Proctor R H. (2008). Transformation-mediated complementation of a FUM gene cluster deletion in Fusarium verticillioides restores both fumonisin production and pathogenicity on maize seedlings. Molecular Plant Microbe Interactions 21(1): 87–97. https://doi.org/10.1094/MPMI-21-1-0087

Go K, Horikawa Y, Garcia R and Villarreal F J. (2008). Fluorescent method for detection of cleaved collagens using O-phthaldialdehyde (OPA). Journal of Biochemical and Biophysical Methods 70(6): 878–882. https://doi.org/10.1016/j.jbbm.2007.05.004

Hanke N, Staggs L, Schroder P, Littarel J, Heig S, Kaufeld J, Pauli C, Haller H and Schiffer M. (2013). Zebrafishing for novel genes relevant to the glomerular filtration barrier. BioMed Research International 2013: 1–12. https://doi.org/10.1155/2013/658270

Hill A J, Bello S M, Prasch A L, Peterson R E and Heideman W. (2004). Water permeability and TCDD-induced edema in zebrafish early-life stages. Toxicological Science 78(1): 78–87. https://doi.org/10.1093/toxsci/kfh056

Hill A J, Heiden T C, Heideman W and Peterson R E. (2009). Potential roles of arnt2 in zebrafish larval development. Zebrafish 6(1): 79–91. https://doi.org/10.1089/zeb.2008.0536

Hirata H, Saint-Amant L, Downes G B, Cui W W, Zhou W, Granato M and Kuwada J Y. (2005). Zebrafish bandoneon mutants display behavioral defects due to a mutation in the glycine receptor ?-subunit. Proceedings of the National Academy of Sciences of the United States of America 102(23): 8345–8350. https://doi.org/10.1073/pnas.0500862102

Howe K, Clark M D, Torroja C F, Torrance J, Berthelot C and Muffato M. (2013). The zebrafish reference genome sequence and its relationship to the human genome. Nature 496: 498–503.

Jimenez M, Mateo J J, Hinojo M J and Mateo R. (2003). Sugars and amino acids as factors affecting the synthesis of fumonisins in liquid cultures by isolates of the Gibberella fujikuroi complex. International of Food Microbiology 89(2–3): 185–193. https://doi.org/10.1016/S0168-1605(03)00120-X

Jurado M, Marin P, Magan N and Gonzalez-Jaen M T. (2008). Relationship between solute, matric potential stress, temperature, growth and FUM1 gene expression in two Fusarium verticillioides strains from Spain. Applied and Environmental Microbiology 74(7): 2032–2036. https://doi.org/10.1128/AEM.02337-07

Kalueff A V, Gebhardt M, Stewart A M, Cachat J M, Brimmer M, Chawla J S, Craddock C et al. (2013). Towards a comprehensive catalog of zebrafish behaviour 1.0 and beyond. Zebrafish 10(1): 70–86. https://doi.org/10.1089/zeb.2012.0861

Kemp C D and Conte J V. (2012). The pathophysiology of heart failure. Cardiovascular Pathology 21(5): 365–371. https://doi.org/10.1016/j.carpath.2011.11.007

Kohut G, Adam A L, Fazekas B and Hornok L. (2009). N-starvation stress induced FUM gene expression and fumonisin production is mediated via the HOG-type MAPK pathway in Fusarium proliferatum. International Journal of Food Microbiology 130(1): 65–69. https://doi.org/10.1016/j.ijfoodmicro.2009.01.002

Lee S H, Kim J H, Son S W, Lee T and Yun S H. (2012). Fumonisin production by field isolates of the Gibberella fujikuroi species complex and Fusarium commune obtained from rice and corn in Korea. Research in Plant Disease 18(4): 310–316. https://doi.org/10.5423/RPD.2012.18.4.310

Logrieco A, Mule G, Moretti A and Bottalico A. (2002). Toxigenic Fusarium species and mycotoxins associated with maize ear rot in Europe. European Journal of Plant Pathology 108: 597–609. https://doi.org/10.1007/978-94-010-0001-7_1

Maharajan K, Muthulakshmi S, Nataraj B, Ramesh M and Kadirvelu K. (2018). Toxicity assessment of pyriproxyfen in vertebrate model zebrafish embryos (Danio rerio): A multi biomarker study. Aquatic Toxicology 196: 132–145. https://doi.org/10.1016/j.aquatox.2018.01.010

Marasas W F O. (2001). Discovery and occurrence of the fumonisins: A historical perspective. Environmental Health Perspective 109(Suppl. 2): 239–243. https://doi.org/10.1289/ehp.01109s2239

Matthews M, Trevarrow B and Matthews J. (2002). A virtual tour of the guide for zebrafish users. Lab Animal 31: 34–40.

Najihah A, Nur Ain Izzati M Z, Yong S Y C and Nik Mohd Izham M N. (2017). Characterization of Fusarium proliferatum and Fusarium verticillioides based on species-specific gene and microsatellite analysis. Sains Malaysiana 46(12): 2425–2432. https://doi.org/10.17576/jsm-2017-4612-18

Nor Azliza I, Masratul Hawa M, Nik Mohd Izham M N and Latiffah Z. (2017). Fumonisin B1- producing Fusarium species from agricultural crops in Malaysia. Crop Protection 98: 70–75. https://doi.org/10.1016/j.cropro.2017.03.014

Nur Ain Izzati M Z and Nithiyaa P. (2015). Mycotoxins production by Fusarium and Aspergillus species isolated from cornmeal. International Journal of Microbiology of Agriculture & Biology 17: 440–448. https://doi.org/10.17957/IJAB/17.3.14.170

Nur Ain Izzati M Z, Azmi A R and Baharuddin S. (2008). Secondary metabolite profiles and mating populations of Fusarium species in section Liseola associated with bakanae disease of rice. Malaysian Journal of Microbiology 4(1): 6–13. https://doi.org/10.21161/mjm.01708

Proctor R H, Desjardins A E, Plattner R D and Hohn T M. (1999). A polyketide synthase gene required for biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal Genetics and Biology 27(1): 100–112. https://doi.org/10.1006/fgbi.1999.1141

Proctor R H, Plattner R D, Brown D W, Seo J A and Lee Y W. (2004). Discontinuous distribution of fumonisin biosynthetic genes in the Gibberella fujikuroi species complex. Mycological Research 108(7): 815–822. https://doi.org/10.1017/S0953756204000577

Organisation for Economic Co-operation and Development (OECD). (2012). Validation report (Phase 2) for the zebrafish embryo toxicity test: Part I and Part II. Series on Testing and Assessment No. 179, OECD, Paris.

Samapundo S, Devliehgere F, De Meulenaer B and Debevere J (2005). Effect of water activity and temperature on growth and the relationship between fumonisin production and the radial growth of Fusarium verticillioides and Fusarium proliferatum on corn. Journal of Food Protection 68(5): 1054–1059. https://doi.org/10.4315/0362-028X-68.5.1054

Scherz P J, Huisken J, Sahai-Hernandez P and Stainier D Y. (2008). High-speed imaging of developing heart valves reveals interplay of morphogenesis and function. Development 135: 1179–1187. https://doi.org/10.1242/dev.010694

Shephard G S. (1998). Chromatographic determination of the fumonisins mycotoxins. Journal of Chromatography A 815(1): 31–39. https://doi.org/10.1016/S0021-9673(98)00187-3

Tsai Y J, Pan H, Hung C M, Hou P T, Li Y C, Lee, Y J, Shen Y T, Wu T T and Li C. (2011). The predominant protein arginine methyltransferase PRMT1 is critical for zebrafish convergence and extension during gastrulation. The FEBS Journal 278(6): 905– 917. https://doi.org/10.1111/j.1742-4658.2011.08006.x

WHO/FAO. (2001). Safety evaluation of certain mycotoxins in food. WHO Food Addictive Series 47/FAO Food and Nutrition Paper. Geneva: WHO.

Wu T S, Yang J J, Yu F Y and Liu B H. (2013). Cardiotoxicity of mycotoxin citrinin and involvement of microRNA-138 in zebrafish embryos. Toxicological Sciences 136(2): 402–412. https://doi.org/10.1093/toxsci/kft206

Wu T S, Yang J J, Wang Y W, Yu F Y and Liu B H. (2016). Mycotoxin ochratoxins A disrupts renal development via a miR-731/prolactin receptor axis in zebrafish. Toxicology Research 5(2): 519–529. https://doi.org/10.1039/C5TX00360A

Yang Y, Qi S, Wang D, Wang K, Zhu L, Chai T and Wang C. (2016). Toxic effects of thifluzamide on zebrafish (Danio rerio). Journal of Hazardous Materials 307: 127– 136. https://doi.org/10.1016/j.jhazmat.2015.12.055

Yin E S, Rakhmankulova M, Kucera K, de Sena Filho J G, Portero C E, Narvaez-Trujillo A, Holley S A and Strobel S. (2015). Fusaric acid induces a notochord malformation in zebrafish via copper chelation. Biometals 28: 783–789. https://doi.org/10.1007/s10534-015-9855-7

Yuan G, Wang Y, Yuan X, Zhang T, Zhao J, Huang L and Peng S. (2014). T-2 toxin induces developmental toxicity and apoptosis in zebrafish embryos. Journal of Environmental Sciences 26(4): 917–925. https://doi.org/10.1016/S1001-0742(13)60510-0

Zain M E. (2011). Impacts of mycotoxins on humans and animals. Journal of Saudi Chemical Society 15(2): 129–144. https://doi.org/10.1016/j.jscs.2010.06.006