Abstract
Aflatoxins (AFs) as potent food contaminants are highly detrimental to human and animal health. The production of such biological toxins is influenced by environmental factors including pollutants, such as dioxins. Here, we report the biological feedback of an active AF-producer strain of A. flavus upon in vitro exposure to the most toxic congener of dioxins, the 2,3,7,8-tetrachlorinated dibenzo-p-dioxin (TCDD). The phenotype of TCDD-exposed A. flavus was typified by a severe limitation in vegetative growth, activation of conidia formation and a significant boost in AF production. Furthermore, the level of reactive oxygen species (ROS) in fungal protoplast was increased (3.1- to 3.8-fold) in response to TCDD exposure at 10 and 50 ng mL–1, respectively. In parallel, superoxide dismutase (SOD) and catalase (CAT) activities were, respectively, increased by a factor of 2 and 3. In contrast to controls, transcript, protein and enzymatic activity of caleosin/peroxygenase (AfPXG) was also significantly induced in TCDD-exposed fungi. Subsequently, fungal cells accumulated fivefold more lipid droplets (LDs) than controls. Moreover, the TCDD-exposed fungi exhibited twofold higher levels of AFB1. Interestingly, TCDD-induced hyperaflatoxicogenicity was drastically abolished in the AfPXG-silencing strain of A. flavus, suggesting a role for AfPXG in fungal response to TCDD. Finally, TCDD-exposed fungi showed an increased in vitro virulence in terms of sporulation and AF production. The data highlight the possible effects of dioxin on aflatoxicogenicity of A. flavus and suggest therefore that attention should be paid in particular to the potential consequences of climate change on global food safety.
Highlights
Aflatoxins (AFs) are fungal lipid-derived toxins that provoke both acute and chronic toxicity in humans and animals
Speaking, the amount of aflatoxin B1 (AFB1), measured by HPLC, was doubled in the tetrachlorinated dibenzo-p-dioxin (TCDD)-exposed fungi compared to control, where the highest concentration of AFB1 (24.8 μg mL−1) was detected when A. flavus was exposed to 50 ng L−1 on day 7 after inoculation (Figure 1E)
We recently reported that the caleosin/peroxygenase activity of caleosin/peroxygenase (AfPXG) of A. flavus modulates the biosynthesis of AF and its trafficking via the lipid droplets (LDs) (Hanano et al, 2018a)
Summary
Aflatoxins (AFs) are fungal lipid-derived toxins that provoke both acute and chronic toxicity in humans and animals These toxins are produced by certain ascomycete fungi, most notably Aspergillus flavus and Aspergillus parasiticus (Yu et al, 2004; Shephard, 2008; Yu, 2012) and contaminate a range of fresh and stored food/feed products, causing serious health, Dioxins Affect the Aflatoxicogenicity of A. flavus economic and ecological troubles. As a possible consequence of climate change, persistent environmental pollutants could dramatically increase because of the increased incidence of large-scale forest fires that has occurred over the last decade Such pollutants, namely polychlorinated dibenzo-p-dioxins (PCDDs) and polychlorinated dibenzofurans (PCDFs), are considered the most toxic group of Persistent Organic Pollutants (POPs) (WHO, 2016). Due to their physicochemical properties, dioxins can persist in the environment and bioaccumulate in the organisms of a given ecosystem, including bacteria, fungi, plants, animals, and humans (Field and Sierra-Alvarez, 2008; Ishida et al, 2010; Anasonye et al, 2014; Hanano et al, 2014b)
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