Potential of atoxigenic Aspergillus flavus vegetative compatibility groups associated with maize and groundnut in Ghana as biocontrol agents for aflatoxin management

Authors: AGBETIAMEH, DANIEL - International Institute For Tropical Agriculture; ORTEGA-BELTRAN, ALEJANDRO - International Institute For Tropical Agriculture; AWUAH, RICHARD - Kwame Nkrumah University Of Science And Technology; ATENHKING, JOSEPH - International Institute For Tropical Agriculture; Islam, Md; Callicott, Kenneth; Cotty, Peter; BANDYOPADHYAY, RANAJIT - International Institute For Tropical Agriculture

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/22/2019
Publication Date: 9/6/2019
Citation: Agbetiameh, D., Ortega-Beltran, A., Awuah, R.T., Atenhking, J., Islam, M.S., Callicott, K.A., Cotty, P.J., Bandyopadhyay, R. 2019. Potential of atoxigenic Aspergillus flavus vegetative compatibility groups associated with maize and groundnut in Ghana as biocontrol agents for aflatoxin management. Frontiers in Microbiology. 10. https://doi.org/10.3389/fmicb.2019.02069.
DOI: https://doi.org/10.3389/fmicb.2019.02069

Interpretive Summary: In order to find fungi useful for biological control of aflatoxins (potent cancer-causing chemicals produced on food by some fungi in the species Aspergillus flavus and its close relatives), A. flavus fungi that cannot produce aflatoxins (called atoxigenic isolates) were identified from Ghana. Twelve genetic groups of these atoxigenic isolates were examined in the lab, and the best isolate from each of these groups used in field trials to test their usefulness in biological control. Singificantly lower aflatoxins were seen on peanut and corn grown in fields treated with these atoxigenic isolates. The eight best isolates were chosen to create two four-isolate mixtures for use a biological control of aflatoxins in corn and peanuts in Ghana.

Technical Abstract: Increasing knowledge of the deleterious health and economic impacts of aflatoxin in crop commodities has stimulated global interest in aflatoxin mitigation. Current evidence of the incidence of Aspergillus flavus isolates belonging to vegetative compatibility groups (VCGs) lacking the ability to produce aflatoxins (i.e., atoxigenic) in Ghana may lead to develop an aflatoxin biocontrol strategy to mitigate crop aflatoxin content. In this study, 12 genetically diverse atoxigenic African A. flavus VCGs (AAVs) were identified from fungal communities associated with maize and groundnut grown in Ghana. Representative isolates of the 12 AAVs were assessed for their ability to inhibit aflatoxin contamination by an aflatoxin-producing isolate in laboratory assays. Then, the 12 isolates were evaluated for their potential as biocontrol agents for aflatoxin mitigation when included in three experimental products (each containing four atoxigenic isolates). The three experimental products were evaluated in 50 maize and 50 groundnut farmers’ fields across three agroecological zones (AEZs) in Ghana during the 2014 cropping season. In laboratory assays, the atoxigenic isolates reduced aflatoxin biosynthesis by 87% to 98% compared to grains inoculated with the aflatoxin-producing isolate alone. In field trials, the applied isolates moved to the crops and had higher (P < 0.05) frequencies than other A. flavus genotypes. In addition, although at lower frequencies, most atoxigenic genotypes were repeatedly found in untreated crops. Aflatoxin levels in treated crops were lower by 70% to 100% in groundnut and by 50% to 100% in maize (P < 0.05) than in untreated crops. Results from the current study indicate that combined use of appropriate, well-adapted isolates of atoxigenic AAVs as active ingredients of biocontrol products effectively displace aflatoxin producers and in so doing limit aflatoxin contamination. A member each of eight atoxigenic AAVs with superior competitive potential and wide adaptation across AEZs were selected for further field efficacy trials in Ghana. A major criterion for selection was the atoxigenic isolate’s ability to colonize soils and grains after release in crop field soils. Use of isolates belonging to atoxigenic AAVs in biocontrol management strategies has the potential to improve food safety, productivity, and income opportunities for smallholder farmers in Ghana.