Metabolic breadth links insect pathogenicity and plant association in Metarhizium robertsii

Fungi frequently transition between pathogenic, endophytic, and saprophytic lifestyles, yet the functional traits enabling these ecological shifts remain unclear. Comparative analyses of early and recently diverged lineages of Metarhizium robertsii reveal contrasting life-history strategies. Early diverged strains exhibit limited plant root association, slower insect lethality, extensive within-host proliferation, and high sporulation, whereas recently diverged strains display rapid germination on insect cuticle and plant roots, accelerated host killing, and hyphal growth from cadavers to plant roots; most also exhibit destruxin activity. Carbon utilization profiling across 95 substrates demonstrates that expanded metabolic breadth strongly predicts cuticle and plant-responsive germination, virulence across multiple insect hosts, and root colonization efficiency, linking cross-kingdom performance to nutritional breadth. Host immune activation further modulates strain-specific virulence but does not obscure the central role of metabolic flexibility. Collectively, these findings identify metabolic capacity as a functional axis coupling nutrient acquisition to ecological diversification, providing a mechanistic framework for understanding ecological plasticity in host-associated fungi.