Iron acquisition in the weevil-farming fungus Penicillium herquei: Implications of mineral elements in insect-fungus mutualistic association

Abstract

Mutualistic interactions between insects and fungi are pivotal in ecosystem dynamics, yet the underlying molecular mechanisms remain largely unexplored. This study investigates iron acquisition strategies of the weevil-farming Penicillium herquei, revealing the involvement of mineral elements in insect-fungus symbiosis. Comparative transcriptomics of weevil-farming strain (WFS) and soil free-living strain (SFS) revealed distinct transcriptional profiles, with 4,357 up-regulated genes in WFS. Enrichment analyses highlighted a significant up-regulation of genes linked to oxidoreductase activity, iron and heme binding, with a notable prevalence of Cytochrome P450 (CYP450). qRT-PCR confirmed differential expression of CYP450 and siderophore-related genes, indicating enhanced iron absorption in WFS. Comparative analysis of iron content further demonstrated significantly higher iron levels in WFS than in SFS and weevil host plant leaves, suggesting a nutritional adaptation for symbiotic lifestyle. These findings provide novel insights into the role of iron metabolism in insect-fungus mutualism, highlighting potential evolutionary mechanisms that bolster symbiotic fitness. IMPORTANCEUnraveling the complex interplay between insects and fungi is crucial for deciphering the intricate dynamics of ecosystems. In this study a notable up-regulation of genes associated with iron and heme binding, as well as a significant increase in iron content within WFS, suggesting a specialized adaptation for enhanced iron acquisition, potentially enabling the fungus to efficiently provide essential nutrients, including bioavailable iron, to weevil host. This research not only advances our understanding of the molecular mechanisms governing insect-fungus mutualism but also highlights the potential evolutionary mechanisms that bolster symbiotic fitness and contribute to the co-evolution of these interacting species.