Origins and metabolic evolution of multifunctionality in Metarhizium robertsii: linking phenotypic diversity to ecological niche plasticity

Abstract

This study investigates the evolution of fungi with complex multifunctional ecological roles using early and recently diverged lineages of Metarhizium robertsii as a model. The early diverged strains are characterized by slower insect killing, extensive pre-mortem fungal proliferation within hosts, and prolific sporulation, whereas recently diverged strains show rapid growth, a "kill and consume" strategy linked to destruxin toxin production, and enhanced plant root colonization. Metabolic assays demonstrated that recently diverged strains utilize a broader range of carbon sources, supporting their ecological versatility as pathogens, endophytes, and saprophytes. Germination rates on insect cuticles and plant roots strongly correlate with each other, and with virulence to Drosophila and beetles (Tenebrio molitor, Popillia japonica), highlighting nutritional flexibility as a key driver of ecological adaptation. Immune response assays in Drosophila revealed that virulence differences among strains are also partly mediated by host immune activation. These findings suggest that nutritional mode shifts underpin the evolutionary trajectory from specialist insect pathogen to plant associations and enhanced insect virulence within M. robertsii, providing a valuable model for studying fungal ecological plasticity and informing the development of fungal biofertilizers and biopesticides.