Ubiquity of Insect-Derived Nitrogen Transfer to Plants by Endophytic Insect-Pathogenic Fungi: an Additional Branch of the Soil Nitrogen Cycle

Abstract

ABSTRACTThe study of symbiotic nitrogen transfer in soil has largely focused on nitrogen-fixing bacteria. Vascular plants can lose a substantial amount of their nitrogen through insect herbivory. Previously, we showed that plants were able to reacquire nitrogen from insects through a partnership with the endophytic, insect-pathogenic fungusMetarhizium robertsii. That is, the endophytic capability and insect pathogenicity ofM. robertsiiare coupled so that the fungus acts as a conduit to provide insect-derived nitrogen to plant hosts. Here, we assess the ubiquity of this nitrogen transfer in fiveMetarhiziumspecies representing those with broad (M. robertsii,M. brunneum, andM. guizhouense) and narrower insect host ranges (M. acridumandM. flavoviride), as well as the insect-pathogenic fungiBeauveria bassianaandLecanicillium lecanii. Insects were injected with15N-labeled nitrogen, and we tracked the incorporation of15N into two dicots, haricot bean (Phaseolus vulgaris) and soybean (Glycine max), and two monocots, switchgrass (Panicum virgatum) and wheat (Triticum aestivum), in the presence of these fungi in soil microcosms. AllMetarhiziumspecies andB. bassianabut notL. lecaniishowed the capacity to transfer nitrogen to plants, although to various degrees. Endophytic association by these fungi increased overall plant productivity. We also showed that in the field, where microbial competition is potentially high,M. robertsiiwas able to transfer insect-derived nitrogen to plants.Metarhiziumspp. andB. bassianahave a worldwide distribution with high soil abundance and may play an important role in the ecological cycling of insect nitrogen back to plant communities.