Abstract
BackgroundAflatoxins (AFs) are highly carcinogenic compounds produced by Aspergillus species in seeds with high lipid and protein contents. It has been known for over 30 years that peptone is not conducive for AF productions, although reasons for this remain unknown.ResultsIn this study, we showed that when Aspergillus flavus was grown in peptone-containing media, higher initial spore densities inhibited AF biosynthesis, but promoted mycelial growth; while in glucose-containing media, more AFs were produced when initial spore densities were increased. This phenomenon was also observed in other AF-producing strains including A. parasiticus and A. nomius. Higher peptone concentrations led to inhibited AF production, even in culture with a low spore density. High peptone concentrations did however promote mycelial growth. Spent medium experiments showed that the inhibited AF production in peptone media was regulated in a cell-autonomous manner. mRNA expression analyses showed that both regulatory and AF biosynthesis genes were repressed in mycelia cultured with high initial spore densities. Metabolomic studies revealed that, in addition to inhibited AF biosynthesis, mycelia grown in peptone media with a high initial spore density showed suppressed fatty acid biosynthesis, reduced tricarboxylic acid (TCA) cycle intermediates, and increased pentose phosphate pathway products. Additions of TCA cycle intermediates had no effect on AF biosynthesis, suggesting the inhibited AF biosynthesis was not caused by depleted TCA cycle intermediates.ConclusionsWe here demonstrate that Aspergillus species grown in media with peptone as the sole carbon source are able to sense their own population densities and peptone concentrations to switch between rapid growth and AF production. This switching ability may offer Aspergillus species a competition advantage in natural ecosystems, producing AFs only when self-population is low and food is scarce.
Highlights
Aflatoxins (AFs) are highly carcinogenic compounds produced by Aspergillus species in seeds with high lipid and protein contents
Spore density-dependent AF production in peptone mineral salts (PMS) media PMS has long been considered to be a non-conducive medium for AF production in both A. flavus and A. parasiticus [23,24,25]
We examined the mycelial growth in media with 5%, 10% and 15% peptone, and observed increased mycelium dry weights when the peptone concentrations were increased (Figure 3B), suggesting that high concentrations of peptone promoted mycelial growth and at the same time inhibited AF biosynthesis
Summary
Aflatoxins (AFs) are highly carcinogenic compounds produced by Aspergillus species in seeds with high lipid and protein contents. Extensive studies carried out in A. flavus and A. parasiticus lead to the identification of a 70 kb DNA cluster consisting two specific transcriptional regulators (aflR and aflS), Various nutritional and environmental factors including carbon sources [11], nitrate [12], light [13], temperature [14,15], pH [14,16], and oxygen availability [17,18,19] affect AF productions and expressions of AF biosynthesisrelated genes [9,20,21] It has been known for a long time that sugars and related carbohydrates support both fungal growth and AF production. Recent studies have revealed cell density-dependent sclerotium formation and AF production in media with glucose and sorbitol as the carbohydrate sources, which is regulated through non-cell autonomous factors [28,29]
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