Abstract
Fungal entomopathogens rely on cellular heterogeneity during the different stages of insect host infection. Their pathogenicity is exhibited through the secretion of secondary metabolites, which implies that the infection life history of this group of environmentally important fungi can be revealed using metabolomics. Here metabolomic analysis in combination with ex vivo insect tissue culturing shows that two generalist isolates of the genus Metarhizium and Beauveria, commonly used as biological pesticides, employ significantly different arrays of secondary metabolites during infectious and saprophytic growth. It also reveals that both fungi exhibit tissue specific strategies by a distinguishable metabolite secretion on the insect tissues tested in this study. In addition to showing the important heterogeneous nature of these two entomopathogens, this study also resulted in the discovery of several novel destruxins and beauverolides that have not been described before, most likely because previous surveys did not use insect tissues as a culturing system. While Beauveria secreted these cyclic depsipeptides when encountering live insect tissues, Metarhizium employed them primarily on dead tissue. This implies that, while these fungi employ comparable strategies when it comes to entomopathogenesis, there are most certainly significant differences at the molecular level that deserve to be studied.
Highlights
Isogenic cell populations of both prokaryotic and eukaryotic organisms can exhibit a highly dynamic transcriptome, proteome and metabolome
Using this novel culturing approach, we discovered additional cyclic depsipeptides for both species that have not yet been described. These compounds have been reported to have roles in cellular paralysis and cytotoxic effects, which have been shown to have an antitumor, antibiotic, antifungal, immunosuppressant and anti-inflammatory effect [20,21,22,23,24]. We discovered that these insecticidal compounds are heterogeneously secreted depending on the type of tissue: the Beauveria isolate secretes its beauverolides mainly on live tissues, while the Metarhizium isolate adopts a strategy of releasing destruxins predominantly on dead tissue
Carpenter ants of the species C. pennsylvanicus are considered a pest in the United States since they preferably nest in dead wood and cause structural damage to many houses every year [25]
Summary
Isogenic cell populations of both prokaryotic and eukaryotic organisms can exhibit a highly dynamic transcriptome, proteome and metabolome. The genera Beauveria and Metarhizium are both comprised of anamorph entomopathogenic fungi that infect a wide range of arthropod hosts Fungal strains for both these genera are frequently isolated from soil and have been the most widely employed as mycoinsecticides for the biological control of insect pests worldwide. Liquid chromatography coupled with quadrupole time-of-flight mass spectrometry on the medium after prolonged contact between fungus and ant tissue shows that these two fungal isolates secrete a very different array of metabolites (hereafter referred to as their secretome) on both live and dead ant material. They each exhibit a significantly different secretome when encountering different insect tissues. We discovered that these insecticidal compounds are heterogeneously secreted depending on the type of tissue: the Beauveria isolate secretes its beauverolides mainly on live tissues, while the Metarhizium isolate adopts a strategy of releasing destruxins predominantly on dead tissue
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