Arginine accumulation suppresses heat production during fermentation of the biocontrol fungus Beauveria bassiana

ABSTRACT Beauveria bassiana ( Bb ) is one of the most widely used biocontrol agents, and its products constitute more than one-third of the global market share of fungal insecticides. Solid-state fermentation (SSF) is widely used in the production of Beauveria bassiana ( Bb ) because of its economic practicality and high production efficiency. However, the heat generated during fermentation can sharply reduce both the yield and quality of Bb , and current industrial methods to mitigate high temperatures during fermentation are inadequate, leading to increased production costs. Thus, exploring the underlying mechanism of how heat is produced by Bb is crucial for improving the SSF procedure and yield. This study employed multiomics data analysis of Bb during SSF to explore the relationships between fungal fermentation and environmental factors. We found that the heat production period for SSF was 12 hours to 48 hours post-inoculation. To further explore the underlying mechanism during this heating period, we identified 454 temperature-correlated metabolites (TCMs) and 1,994 temperature-correlated genes (TCGs). Annotations of the above TCMs and TCGs revealed significant enrichment in the arginine biosynthesis pathway; specifically, the expression level of glutamine synthetase, a TCG, decreased with fermentation time, whereas the expression levels of the TCGs L-arginine and L–glutamine increased with fermentation time, and glutamine synthetase and L-glutamine in the arginine biosynthesis pathway cycle produced the end product L-arginine. Furthermore, when the substrates of the SSF were treated with exogenous arginine, the temperature peak of the SSF significantly decreased with increasing concentration of exogenously added arginine. IMPORTANCE A large amount of experimental evidence from the field has shown that Bb is an irreplaceable mature product that protects the health of our agriculture and ecosystem. In addition to high efficiency and host extensiveness, low cost is a critical merit that makes Bb products frequently used in the field. However, the growing cost of power and labor in the Bb industry, especially the SSF procedure, has significantly increased the price of its products, thus restricting the use of Bb in the field. This study not only fills the theoretical knowledge gaps concerning the molecular basis of the interrelationship between Bb and the fermentation environment during SSF but also provides an economical and applicable strategy (the addition of arginine to the fermentation media) to further lower the cost and increase the yield of Bb during SSF at the industrial level.