The multifunctional lifestyles of Metarhizium: evolution and applications

The genus Metarhizium is comprised of a diverse group of common soil fungi that exhibit multifunctional lifestyles with varying degrees of saprotrophic, endophytic, and insect pathogenic modes of nutrient acquisition. The transcriptome of these species is modulated to reflect immediate needs of the fungus and availability of resources—a form of transcriptional plasticity that allows for physiological adaptation to environments with diverse and dynamic exploitable nutrient sources. In this review, we discuss the endophytic, insect pathogenic lifestyles of Metarhizium spp., including their symbiotic interface, origins, and evolution, and agricultural applications. Isotope labeling experiments have demonstrated that a mutually beneficial exchange of limiting nutrients occurs between the fungus and its host plant, with nitrogen derived via insect pathogenesis being translocated from Metarhizium to host plants in exchange for fixed carbon in the form of photosynthate. Thus, the endophytic and entomopathogenic abilities of Metarhizium spp. are not exclusive of one another, but rather are interdependent and reciprocal in nature. Although endophytic, insect pathogenic fungi (EIPF) could certainly have evolved from insect pathogenic fungi, phylogenomic evidence indicates that this genus is more closely related to plant-associated fungi than animal pathogens, suggesting that Metarhizium evolved from a lineage of plant symbionts, which subsequently acquired genes for insect pathogenesis. Entomopathogenicity may have been an adaptive trait, allowing for procurement of insect-derived nitrogen that could be translocated to host plants and bartered for fixed carbon, thereby improving the stability of fungal-plant symbioses. Given their ability to simultaneously parasitize soil insects, including a number of pests of agriculturally important crops, as well as promote plant health, growth, and productivity, Metarhizium spp. are considered promising alternatives to the chemical pesticides and fertilizers that have wreaked havoc on the health and integrity of ecosystems. Key points • Metarhizium is a fungus that is an insect pathogen as well as a plant symbiont. • The genus Metarhizium has specialist and generalist insect pathogens. • Metarhizium is phylogenetically most closely related to plant endophytes.