Temperature influences on interactions among aflatoxigenic species of aspergillus section flavi during maize colonization

Authors: CHING'ANDA, CONNEL - University Of Arizona; ATEHNKENG, JOSEPH - International Institute Of Tropical Agriculture (IITA); BANDYOPADHYAY, RANAJIT - International Institute Of Tropical Agriculture (IITA); Callicott, Kenneth; ORBACH, MARC - University Of Arizona; Cotty, Peter; Mehl, Hillary

Submitted to: Frontiers in Fungal Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/26/2021
Publication Date: 8/26/2021
Citation: Ching'Anda, C., Atehnkeng, J., Bandyopadhyay, R., Callicott, K.A., Orbach, M.J., Cotty, P.J., Mehl, H.L. 2021. Temperature influences on interactions among aflatoxigenic species of aspergillus section flavi during maize colonization. Frontiers in Fungal Biology. 2. Article 720276. https://doi.org/10.3389/ffunb.2021.720276.
DOI: https://doi.org/10.3389/ffunb.2021.720276

Interpretive Summary: Aflatoxins are toxic, carcinogenic fungal metabolites produced by certain Aspergillus species that infect and contaminate food and feed crops. Species of Aspergillus vary in the types and quantities of aflatoxins that they produce. In addition, Aspergillus species can be subdivided into S and L morphotypes based on spore production and sclerotial morphology, and these morphological differences suggest species may be adapted to different environments or life strategies. In this study, interactions between different Aspergillus species during infection of maize kernels were characterized at two temperatures (25C and 30C). The two S morphology species were more competitive than L morphology species at the higher temperature, and total aflatoxin production increased at 30C compared to 25C. When grown individually, S morphology species typically produce numerous small sclerotia and relatively small quantities of spores, whereas L morphology fungi produce few large sclerotia and large quantities of spores. However, during co-infection of maize kernels at 30C, sporulation by S morphology fungi was generally enhanced and sporulation by L morphology fungi was suppressed. Results indicate that both fungal competition and temperature can modulate the composition and aflatoxin-producing potential of crop-associated fungal communities. Thus, seasonal temperature fluctuations and overall warming trends in certain regions can alter the risk and severity of aflatoxin contamination.

Technical Abstract: Fungal species within Aspergillus section Flavi contaminate food and feed with aflatoxins. These toxic fungal metabolites compromise human and animal health and disrupt trade. Genotypically and phenotypically diverse species co-infect crops, but temporal and spatial variation in frequencies of different lineages suggests that environmental factors such as temperature may influence structure of aflatoxin-producing fungal communities. Furthermore, though most species within Aspergillus section Flavi produce sclerotia, divergent sclerotial morphologies (small or S-type sclerotia vs. large or L-type sclerotia) and differences in types and quantities of aflatoxins produced suggest lineages are adapted to different life strategies. Temperature is a key parameter influencing pre- and post-harvest aflatoxin contamination of crops. We tested the hypothesis that species of aflatoxin-producing fungi that differ in sclerotial morphology will vary in competitive ability and that outcomes of competition and aflatoxin production will be modulated by temperature. Paired competition experiments between highly aflatoxigenic S-type species (A. aflatoxiformans and Lethal Aflatoxicosis Fungus) and L-type species (A. flavus L morphotype and A. parasiticus) were conducted on maize kernels at 25 and 30°C. Proportions of each isolate growing within and sporulating on kernels were measured using quantitative pyrosequencing. At 30°C, S-type fungi were more effective at host colonization compared to L-type isolates. Total aflatoxins and the proportion of B vs. G aflatoxins were greater at 30°C compared to 25°C. Sporulation by L-type isolates was reduced during competition with S-type fungi at 30°C, while relative quantities of conidia produced by S-type species either increased or did not change during competition. Results indicate that both species interactions and temperature can shape population structure of Aspergillus section Flavi, with warmer temperatures favoring growth and dispersal of highly toxigenic species with S-type sclerotia.