Genome-wide identification of BCS1 domain-containing proteins reveals the mitochondrial bcs1 essential for growth, stress response, and virulence of the filamentous entomopathogenic fungus Beauveria bassiana

In yeasts, bcs1 is a mitochondrial AAA protein (ATPase associated with diverse cellular activities) and required for biogenesis of the complex III in mitochondrial electron transfer chain. However, the presence and biological roles of bcs1 remain largely unknown in the filamentous fungi. In present study, genome-wide identification revealed that there were six BCS1-domain containing proteins (Bbbcs1a through f) in the filamentous insect pathogenic fungus Beauveria bassiana, five of which (except for Bbbcs1f) were functionally analyzed. Phenotypic evaluation revealed that only Bbbcs1b and Bbbcs1c contributed to fungal physiologies, and they localized to nuclei and mitochondria, respectively. Hence, Bbbcs1c is considered as the ortholog of yeast bcs1 in B. bassiana. Ablation of Bbbcs1c did not affect biogenesis of mitochondria, but its loss significantly attenuated mitochondrial functionality (e.g., ATP synthesis and mitochondrial targeting of proteins) significantly. ΔBbbcs1c mutant displayed the impaired phenotypes in vegetative growth, stress response, development, and virulence. Notably, ΔBbbcs1c mutant displayed the increased sensitivity to linoleic acid (LA) stress and lost the intracellular fatty acid homeostasis. The Bbbcs1c loss compromised the mitochondrial membrane potential, and LA stress exacerbated this damage. These findings indicate that Bbbcs1c is a functional homolog of yeast bcs1 in B. bassiana and links mitochondrial functionality to unique lifestyle in the entomopathogenic fungi.