Aspergillus flavus resident in Kenya: High genetic diversity in an ancient population primarily shaped by clonal reproduction and mutation-driven evolution

Authors: Islam, Md; Callicott, Kenneth; MUTEGI, CHARITY - International Institute Of Tropical Agriculture (IITA); BANDYOPADHYAY, RANAJIT - International Institute Of Tropical Agriculture (IITA); Cotty, Peter

Submitted to: Fungal Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/30/2018
Publication Date: 5/30/2018
Publication URL: https://handle.nal.usda.gov/10113/6123112
Citation: Islam, M.S., Callicott, K.A., Mutegi, C., Bandyopadhyay, R., Cotty, P.J. 2018. Aspergillus flavus resident in Kenya: High genetic diversity in an ancient population primarily shaped by clonal reproduction and mutation-driven evolution. Fungal Ecology. 35:20-33. https://doi.org/10.1016/j.funeco.2018.05.012.
DOI: https://doi.org/10.1016/j.funeco.2018.05.012

Interpretive Summary: Aflatoxin is a major concern across Sub-Saharan Africa as its contamination in crops is widespread and often acute. Aflatoxin is the toxic and carcinogenic fungal metabolite, mostly produced by Aspergillus flavus, A. parasiticus and closely related species. Aflatoxins cause increased risk of liver cancer, stunting, immune suppression, and in cases of acute exposure, liver necrosis and death. The hot and humid tropical climate provides ideal condition for growth of aflatoxin-producing fungi, causing food and feed crops contamination to be widespread across sub-Saharan Africa. Liver cancer associated with chronic exposure of aflatoxin causes death for about 26,000 people annually in the southern part of Sahara. Aflatoxin management thus becomes one of the important issues across sub-Saharan Africa. Biocontrol technology has been proven to be an effective method for aflatoxin management in the U.S. over the last decade. The success of aflatoxin management through biocontrol in U.S. agriculture has led to development of aflatoxin biocontrol programs in several nations across sub-Sharan Africa. In Biocontrol technology, atoxigenic genotypes of A. flavus are used to modify fungal communities in agricultural fields to displace aflatoxin-producing fungi, thereby reducing the overall aflatoxin-contamination potentials of treated fields. However, biocontrol of aflatoxin-producing fungi requires locally adapted atoxigenic A. flavus genotypes for optimal efficacy and long-term success without potential negative environmental impacts that may result from externally-introduced organisms. In this study, 4,538 atoxigenic isolates of A. flavus recovered from eight countries and three regions across Sub-Sharan Africa were genetically characterized (based on DNA markers; SSR makers) to develop a germplasm pool of biocontrol isolates. Isolates in the study were recovered from Burkina Faso, Ghana (West Africa); Brundi, Rwanda, Tanzania (East Africa) and Malawi, Zambia, Mozambique (Southern Africa). Out of this number, 1,988 atoxigenic genotypes of potential value in biocontrol were characterized. Many genotypes identified were restricted locally/regionally. However, some genotypes were widely distributed. The biocontrol germplasm pool developed in this study will help develop local or regional biocontrol products for aflatoxin management in sub-Sharan Africa. The signature of clonal evolution within all the main genetic lineages of the study A. flavus population further preclude the potential for sexual recombination between introduced atoxigenic and naturally existing toxigenic lineages, and suggests sustainably of the modified community with significant reduction in the average aflatoxin contamination of food and feed crops.

Technical Abstract: Aspergillus flavus has long been considered to be an asexual species. Although a sexual stage was recently reported for this species from in vitro studies, the amount of recombination ongoing in natural populations and the genetic distance across which meiosis occurs is largely unknown. In the current study, genetic diversity, reproduction and evolution of natural A. flavus populations endemic to Kenya were examined. A total of 2744 isolates recovered from 629 maize-field soils across southern Kenya in two consecutive seasons were characterized at 17 SSR loci, revealing high genetic diversity (9-72 alleles/locus and 2140 haplotypes). Clonal reproduction and persistence of clonal lineages predominated, with many identical haplotypes occurring in multiple soil samples and both seasons. Genetic analyses predicted three distinct lineages with linkage disequilibrium and evolutionary relationships among haplotypes within each lineage suggesting mutation-driven evolution followed by clonal reproduction. Low genetic differentiation among adjacent communities reflected frequent short distance dispersal.