Oxidative stress and carbon metabolism influence Aspergillus flavus transcriptome composition and secondary metabolite production

Abstract

Contamination of crops with aflatoxin is a serious global threat to food safety. Aflatoxin production by Aspergillus flavus is exacerbated by drought stress in the field and by oxidative stress in vitro. We examined transcriptomes of three toxigenic and three atoxigenic isolates of A. flavus in aflatoxin conducive and non-conducive media with varying levels of H2O2 to investigate the relationship of secondary metabolite production, carbon source, and oxidative stress. We found that toxigenic and atoxigenic isolates employ distinct mechanisms to remediate oxidative damage, and that carbon source affected the isolates’ expression profiles. Iron metabolism, monooxygenases, and secondary metabolism appeared to participate in isolate oxidative responses. The results suggest that aflatoxin and aflatrem biosynthesis may remediate oxidative stress by consuming excess oxygen and that kojic acid production may limit iron-mediated, non-enzymatic generation of reactive oxygen species. Together, secondary metabolite production may enhance A. flavus stress tolerance, and may be reduced by enhancing host plant tissue antioxidant capacity though genetic improvement by breeding selection.

Responses of Aspergillus flavus to Oxidative Stress Are Related to Fungal Development Regulator, Antioxidant Enzyme, and Secondary Metabolite Biosynthetic Gene Expression

“…a Aflatoxin production capability (+++, high; +, moderately high) and maximum H 2 O 2 tolerance observed in Fountain et al (2015) .b Numbers of DEGs described in Fountain et al (2016) .…”

“…Together these results indicate, as has been previously suggested in the literature, that aflatoxin production may contribute to oxidative stress tolerance in Aspergillus spp. (Narasaiah et al, 2006; Roze et al, 2013, 2015; Fountain et al, 2014, 2016). …”

“…The methodologies presented here are adapted from Fountain et al (2016) and describe the data generation and analysis procedures for the toxigenic isolates examined in this study.…”

“…in addition to antioxidant enzymes, altered carbon metabolism, and the production of other secondary metabolites (Narasaiah et al, 2006; Roze et al, 2013; Fountain et al, 2014, 2016). The tolerance of A. flavus and A. parasiticus isolates to oxidative stress has been shown to be correlated with their levels of aflatoxin production.…”

“…However, the observed stress tolerance of the toxigenic isolates cultured in aflatoxin non-conducive medium was reduced yet comparable indicating that factors in addition to aflatoxin production also contributed to the observed differences. In order to better understand the differences in isolate-specific responses to oxidative stress, and to further explore the potential role of aflatoxin production in stress alleviation in A. flavus , we examined the global transcriptional responses of several isolates of A. flavus to increasing oxidative stress, which has been summarized in an overview-type publication (Fountain et al, 2016). Here, we present a detailed analysis of changes in the transcriptomes of different toxigenic A. flavus isolates with distinguished aflatoxin production capabilities to increasing oxidative stress in an aflatoxin conducive culture medium.…”