Several Metarhizium species produce ergot alkaloids in a conditionally specific manner

Authors: LEADMON, CAROLINE - West Virginia University; SAMPSON, JESSI - West Virginia University; MAUST, MATTHEW - West Virginia University; MACIAS, ANGIE - West Virginia University; Rehner, Stephen; KASSON, MATTHEW - West Virginia University; PANACCIONE, DANIEL - West Virginia University

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/8/2020
Publication Date: 7/1/2020
Citation: Leadmon, C.E., Sampson, J.K., Maust, M.D., Macias, A.M., Rehner, S.A., Kasson, M.T., Panaccione, D.G. 2020. Several Metarhizium species produce ergot alkaloids in a conditionally specific manner. Applied and Environmental Microbiology. 86(14):1-13. https://doi.org/10.1128/AEM.00373-20.
DOI: https://doi.org/10.1128/AEM.00373-20

Interpretive Summary: Ergot alkaloids are chemicals that can cause health issues for both humans and animals. Insect biocontrol fungi in the genus Metarhizium have genes that can produce these chemicals. This study investigated if and under what conditions Metarhizium species produce and accumulate ergot alkaloids. Ergot alkaloids were found to be absent in spores, which are used in mycoinsecticide formulations, validating their safe use. Several species excrete ergot alkaloids when grown in specific liquid media, although others do not. This indicates that regulation of ergot alkaloid production varies among species. Significantly, M. brunneum and related species produce ergot alkaloids only when inoculated into living insects. Results of this study are significant because they demonstrate the safety of Metarhizium as a biocontrol agent and the likely importance of ergot alkaloids in contributing to insect disease. Information from this study will be used by insect pathologists and mycologists investigating fungal diseases of insects in support of pest management programs for field crop and forest pests.

Technical Abstract: Genomic sequence data indicate certain fungi in the genus Metarhizium have the capacity to produce lysergic acid-derived ergot alkaloids, but accumulation of ergot alkaloids in these fungi has not been demonstrated previously. We assayed several Metarhizium species grown under different conditions for accumulation of ergot alkaloids. Isolates of M. brunneum and M. anisopliae accumulated the lysergic acid amides lysergic acid a-hydroxyethyl amide, ergine, and ergonovine on sucrose-yeast extract agar but not on two other tested media. Isolates of six other Metarhizium species did not accumulate ergot alkaloids on sucrose-yeast extract agar. Conidia of M. brunneum lacked detectable ergot alkaloids, and mycelia of this fungus secreted over 80% of their ergot alkaloid yield into the culture medium. Isolates of M. brunneum, M. flavoviride, M. robertsii, M. acridum, and M. anisopliae produced high concentrations of ergot alkaloids in infected larvae of the model insect Galleria mellonella, but larvae infected with M. pingshaense, M. album, M. majus, and M. guizhouense lacked detectable ergot alkaloids. Alkaloid concentrations were significantly higher when insects were alive (as opposed to killed by freezing or gas) at the time of inoculation with M. brunneum. Roots of corn and beans were inoculated with M. brunneum or M. flavoviride, and global metabolomic analyses indicated that the inoculated roots were colonized though no ergot alkaloids were detected. The data demonstrate that several Metarhizium species produce ergot alkaloids of the lysergic acid amide class and that production of ergot alkaloids is tightly regulated and associated with insect colonization.