Carbohydrate, glutathione, and polyamine metabolism are central to Aspergillus flavus oxidative stress responses over time

Authors: FOUNTAIN, JAKE - University Of Georgia; YANG, LIMING - University Of Georgia; PANDEY, MANISH - International Crops Research Institute For Semi-Arid Tropics (ICRISAT) - India; BAJAJ, PRASAD - International Crops Research Institute For Semi-Arid Tropics (ICRISAT) - India; ALEXANDER, DANNY - Metabolon, Inc; CHEN, SIXUE - University Of Florida; KEMERAIT, ROBERT - University Of Georgia; VARSHNEY, RAJEEV - International Crops Research Institute For Semi-Arid Tropics (ICRISAT) - India; Guo, Baozhu

Submitted to: BMC Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/27/2019
Publication Date: 9/5/2019
Citation: Fountain, J.C., Yang, L., Pandey, M.K., Bajaj, P., Alexander, D., Chen, S., Kemerait, R.C., Varshney, R.K., Guo, B. 2019. Carbohydrate, glutathione, and polyamine metabolism are central to Aspergillus flavus oxidative stress responses over time. BMC Microbiology. https://doi.org/10.1186/s12866-019-1580-x.
DOI: https://doi.org/10.1186/s12866-019-1580-x

Interpretive Summary: Abiotic stresses such as drought and heat have significant effects on the growth of plant pathogenic fungi and can hinder their capability of infecting host plants such as corn and peanut. Drought stress has been shown to have significant effects on both fungal pathogenicity and on host resistance to infection with some degree of specificity. There also show the importance of metabolite accumulation in fungal environmental stress responses and in host pathogenicity for potential regulating host plant immunity. In this study, we performed a global, untargeted metabolomics analysis of two field isolates of Aspergillus flavus with different levels of aflatoxin production and their response to oxidative stress over time in order to better understand the relationship between drought-derived oxidative stress and exacerbated aflatoxin production in Aspergillus flavus. The goal was to identify the metabolic responses that explain fungal isolate variability in oxidative stress tolerance and for the probable use in improving host resistance through breeding selection or biotechnology like genome editing.

Technical Abstract: he primary and secondary metabolites of fungi are critical for adaptation to environmental stresses, host pathogenicity, competition with other microbes, and reproductive fitness. Under environmental stress from drought, both fungi and their hosts experience oxidative stresses which are countered either enzymatically or through reactions with antioxidant metabolites. Drought-derived reactive oxygen species (ROS) have been shown to stimulate aflatoxin production and regulate development in Aspergillus flavus, and may function in signaling with host plants. To better understand the role of aflatoxin production in oxidative stress responses and to explore isolate-specific oxidative stress responses over time, global, untargeted metabolomics was performed. Two field isolates of A. flavus, AF13 and NRRL3357, possessing high and moderate aflatoxin production, respectively, were cultured in medium with and without supplementation with 15mM H2O2, and mycelia were collected following 4 and 7 days in culture for global metabolomics. Overall, 389 compounds were described in the analysis which were examined for differential accumulation. Significant differences were observed in both isolates in response to oxidative stress and when comparing sampling time points. NRRL3357 showed extensive stimulation of antioxidant mechanisms and pathways including polyamines metabolism, glutathione metabolism, TCA cycle, and lipid metabolism while AF13 showed a less vigorous response to stress. Carbohydrate pathway levels also imply that carbohydrate repression and starvation may influence metabolite accumulation at the later timepoint. Higher conidial oxidative stress tolerance and antioxidant capacity in AF13 compared to NRRL3357, inferred from their metabolomic profiles and growth curves over time, may be connected to aflatoxin production capability and aflatoxin-related antioxidant accumulation. The coincidence of several of the detected metabolites in H2O2-stressed A. flavus and drought-stressed hosts also suggests their potential role in the interaction between these organisms and their use as markers/targets to enhance host resistance through biomarker selection or genetic engineering.