European Journal of Plant Pathology

, Volume 132, Issue 3, pp 419–429 | Cite as

Deadly strains of Kenyan Aspergillus are distinct from other aflatoxin producers

  • C. Probst
  • K. A. Callicott
  • P. J. Cotty


Aflatoxin contamination of crops is a world-wide problem. Lethal aflatoxicosis of humans has been associated with maize produced in Kenya for over three decades. The S strain morphotype of Aspergillus flavus was identified as the primary cause of aflatoxin contamination events occurring between 2004 and 2006 in Kenya. Because the S strain was first described in the U.S., it was suggested that the agent causing lethal levels of aflatoxins was introduced to Kenya with maize. DNA sequence comparisons among 68 S strain isolates from Kenya, the Americas, Asia, and Australia suggest the Kenyan isolates are distinct from those causing aflatoxin contaminations in the U.S. Analyses of 4.06 kb representing three loci from distinct chromosomes indicate that most S strain isolates from the U.S. resolved into a clade distinct from one containing the 30 Kenyan isolates. S strain isolates from Kenya were more closely related to the recently described species A. minisclerotigenes than to A. flavus. Furthermore, failure of the Kenyan isolates to produce G aflatoxins was attributed to a previously undescribed deletion in the cypA gene, suggesting that different deletion events led to loss of G aflatoxin production in S strain isolates from the U.S. and Kenya. Thus, although the Kenyan isolates have S strain morphology and produce large quantities of only B aflatoxins like A. flavus S strain isolates, these isolates are phylogenetically divergent from those described from other regions. The molecular characteristics of the Kenyan S strain isolates described herein are valuable tools to identify and track these highly aflatoxigenic fungi.


Kenya Aflatoxin contamination Maize Phylogeny Aspergillus S morphotype 


  1. Atehnkeng, J., Cotty, P. J., & Bandyopadhyay, R. (2010). Mitigation of aflatoxin contamination in Nigerian maize with atoxigenic strain mixtures (Abstract). Phytopathology, 100, S8.Google Scholar
  2. Atehnkeng, J., Ojiambo, P. S., Donner, M., Ikotun, T., Sikora, R. A., Cotty, P. J., et al. (2008). Distribution and toxigenicity of Aspergillus species isolated from maize kernels from three agro-ecological zones in Nigeria. International Journal of Food Microbiology, 122, 74–84.PubMedCrossRefGoogle Scholar
  3. Cardwell, K. F., & Cotty, P. J. (2002). Distribution of Aspergillus Section Flavi among soils from the four agroecological zones of the Republic of Benin, West Africa. Plant Disease, 86, 434–439.CrossRefGoogle Scholar
  4. Centers for Disease Control and Prevention. (2004). Outbreak of aflatoxin poisoning – Eastern and Central Provinces, Kenya, January-July 2004. Morbidity and Mortality Weekly Report, 53, 790–793.Google Scholar
  5. Chang, P. K., Ehrlich, K. C., & Hua, S.-S. T. (2006). Cladal relatedness among Aspergillus oryzae isolates and Aspergillus flavus S and L morphotype isolates. International Journal of Food Microbiology, 108, 172–177.PubMedCrossRefGoogle Scholar
  6. Cotty, P. J. (1989). Virulence and cultural characteristics of two Aspergillus flavus strains pathogenic on cotton. Phytopathology, 79, 808–814.CrossRefGoogle Scholar
  7. Cotty, P. J., Antilla, L., & Wakelyn, P. J. (2007a). Competitive exclusion of aflatoxin producers: Farmer-driven research and development. In C. Vincent, M. S. Goettel, & G. Lazarovits (Eds.), Biological control: A global perspective. Oxfordshire: CAB International.Google Scholar
  8. Cotty, P. J., Antilla, L., & Wakelyn, P. J. (2007b). Competitive exclusion of aflatoxin producers: farmer driven research and development. In C. Vincent, N. Goettel, & G. Lazarovits (Eds.), Biological control: A global perspective. Oxfordshire: CAB International.Google Scholar
  9. Cotty, P. J., & Cardwell, K. F. (1999). Divergence of West African and North American communities of Aspergillus section Flavi. Applied and Environmental Microbiology, 65, 2264–2266.PubMedGoogle Scholar
  10. Cotty, P. J., & Mellon, J. E. (2006). Ecology of aflatoxin producing fungi and biocontrol of aflatoxin contamination. Mycotoxin Research, 22, 110–117.CrossRefGoogle Scholar
  11. Cotty, P. J., Probst, C., & Jaime-Garcia, R. (2008). Etiology and management of aflatoxin contamination. In J. F. Leslie, R. Bandyopadhyay, & A. Visconti (Eds.), Mycotoxins: Detection methods, management, public health and agricultural trade. Oxfordshire: CAB International.Google Scholar
  12. Donner, M. (2009). Distribution and molecular characterization of aflatoxin-producing and nonproducing isolates of Aspergillus section Flavi for biological control of aflatoxin contamination in maize in Nigeria. Institut für Nutzpflanzenwissenschaften und Ressourcenschutz. Ph.D. Thesis. Bonn: University of Bonn.Google Scholar
  13. Donner, M., Atehnkeng, J., Sikora, R. A., Bandyopadhyay, R., & Cotty, P. J. (2009). Distribution of Aspergillus section Flavi in soils of maize fileds in three agroecological zones of Nigeria. Soil Biology and Biochemistry, 41, 37–44.CrossRefGoogle Scholar
  14. Donner, M., Sikora, R. A., Bandyopadhyay, R., & Cotty, P. J. (2010). Molecular characterization of atoxigenic strains (VCGs) for biological control of aflatoxins in Nigeria. Food Additives and Contaminants, 27, 576–590.CrossRefGoogle Scholar
  15. Egel, D. S., Cotty, P. J., & Elias, K. S. (1994). Relationships among isolates of Aspergillus sect. Flavi that vary in aflatoxin production. Phytopathology, 84, 906–912.Google Scholar
  16. Ehrlich, C. K., & Yu, J. (2010). Aflatoxin-like gene clusters and how they evolved. In M. Rai & A. Varma (Eds.), Mycotoxins in food, feed and bioweapons. Berlin: Springer.Google Scholar
  17. Ehrlich, K. C., Chang, P. K., Yu, J., & Cotty, P. J. (2004). Aflatoxin biosynthesis cluster gene cypA is required for G aflatoxin formation. Journal of Applied and Environmental Microbiology, 70, 6518–24.CrossRefGoogle Scholar
  18. Ehrlich, K. C., Kobbeman, K., Montalbano, B. G., & Cotty, P. J. (2007). Aflatoxin-producing Aspergillus species from Thailand. International Journal of Food Microbiology, 114, 153–159.PubMedCrossRefGoogle Scholar
  19. Ehrlich, K. C., Montalbano, B. G., & Cotty, P. J. (2003). Sequence comparison of aflR from different Aspergillus species provides evidence for variability in regulation of aflatoxin production. Fungal Genetics and Biology, 38, 63–74.PubMedCrossRefGoogle Scholar
  20. Ellis, W. O., Smith, J. P., Simpson, B. K., & Oldham, J. H. (1991). Aflatoxins in food: occurrence, biosynthesis, effects on organisms, detection, and methods of control. Critical Reviews in Food Science and Nutrition, 30, 403–439.PubMedCrossRefGoogle Scholar
  21. Felsenstein, J. (1989). PHYLIP - Phylogeny inference package (Version 3.2). Cladistics, 5, 164–166.Google Scholar
  22. Geiser, D. M., Dorner, J. W., Horn, B. W., & Taylor, J. W. (2000). The phylogenetics of mycotoxin and sclerotium production in Aspergillus flavus and Aspergillus oryzae. Fungal Genetics and Biology, 31, 169–179.PubMedCrossRefGoogle Scholar
  23. Hesseltine, C. W., Shotwell, O. L., Smith, M. L., Shannon, G. M., Vandergraft, E. E., & Goulden, M. L. (1968). Laboratory studies on the formation of aflatoxin in forages. Mycologia, 60, 304–312.PubMedCrossRefGoogle Scholar
  24. Hesseltine, C. W., Shotwell, O. T., Smith, M., Ellis, J. J., Vandegraft, E., & Shannon, G. (1970). Production of various aflatoxins by strains of the Aspergillus flavus series. In: INTERIOR, U. J. P. O. T. M. A. T. U. D. O. T. (Ed.) Proceedings of the First US-Japan Conference on Toxic Microorganisms. Hawaii.Google Scholar
  25. Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES:bayesian inference of phylogeny. Bioinformatics, 17, 754–755.PubMedCrossRefGoogle Scholar
  26. Kurtzman, C. P., Horn, B. W., & Hesseltine, C. W. (1987). Aspergillus nomius, a new aflatoxin-producing species related to Aspergillus flavus and Aspergillus tamarii. Antonie Van Leeuwenhoek, 53, 147–158.PubMedCrossRefGoogle Scholar
  27. Ngindu, A., Johnson, B. K., Kenya, P. R., Ngira, J. A., Ocheng, D. M., Nandwa, H., et al. (1982). Outbreak of acute hepatitis caused by aflatoxin poisoning in Kenya. Lancet, 1, 1346–1348.PubMedCrossRefGoogle Scholar
  28. Pildain, M. B., Frisvad, J. C., Vaamonde, G., Cabral, D., Varga, J., & Samson, R. A. (2008). Two novel aflatoxin-producing Aspergillus species from Argentinean peanuts. International Journal of Systematic and Evolutionary Microbiology, 58, 725–735.PubMedCrossRefGoogle Scholar
  29. Pildain, M. B., Vaamonde, G., & Cabral, D. (2004). Analysis of population structure of Aspergillus flavus from peanut based on vegetative compatibility, geographic origin, mycotoxin and sclerotia production. International Journal of Food Microbiology, 93, 31–40.PubMedCrossRefGoogle Scholar
  30. Probst, C., Bandyopadhyay, R., Price, L. E., & Cotty, P. J. (2011). Identification of atoxigenic Aspergillus flavus isolates to reduce aflatoxin contamination of maize in Kenya. Plant Disease, 95, 212–218.CrossRefGoogle Scholar
  31. Probst, C., Njapau, H., & Cotty, P. J. (2007). Outbreak of an acute aflatoxicosis in Kenya in 2004: identification of the causal agent. Applied and Environmental Microbiology, 73, 2762–2764.PubMedCrossRefGoogle Scholar
  32. Probst, C., Schulthess, F., & Cotty, P. J. (2010). Impact of Aspergillus section Flavi community structure on the development of lethal levels of aflatoxins in Kenyan maize (Zea mays). Journal of Applied Microbiology, 108, 600–610.PubMedCrossRefGoogle Scholar
  33. Rambo, G. W., Tuite, J., & Crane, P. (1974). Preharvest inoculation and infection of dent corn ears with Aspergillus flavus and A. parasiticus. Phytopathology, 64, 797–800.CrossRefGoogle Scholar
  34. Saito, M., & Tsuruta, O. (1993). A new variety of A. flavus from tropical soil in Thailand and its aflatoxin productivity. Proceedings of the Japan Association of Mycotoxicology, 37, 31–36.Google Scholar
  35. Swofford, D. L. (1998). PAUP*. Phylogenetic analysis using parsimony (*and other methods). Sunderland: Sinauer Associates.Google Scholar
  36. Williams, J. H., Phillips, T. D., Jolly, P. E., Stiles, J. K., Jolly, C. M., & Aggarwal, D. (2004). Human aflatoxicosis in developing countries: a review of toxicology, exposure, potential health consequences, and interventions. American Journal of Clinical Nutrition, 80, 1106–22.PubMedGoogle Scholar
  37. Wu, F., & Khlangwiset, P. (2010). Health economic impacts and cost-effectiveness of aflatoxin reduction strategies in Africa: case studies in biocontrol and postharvest interventions. Food Additives and Contaminants, 27, 496–509.CrossRefGoogle Scholar

Copyright information

© KNPV 2011

Authors and Affiliations

  1. 1.The University of Arizona, School of Plant SciencesTucsonUSA
  2. 2.USDA-ARSThe University of Arizona, School of Plant SciencesTucsonUSA

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