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Discovery of psychoactive plant and mushroom alkaloids in behavior-modifying fungal cicada pathogens

View ORCID ProfileGreg R. Boyce, Emile Gluck-Thaler, View ORCID ProfileJason C. Slot, View ORCID ProfileJason E. Stajich, William J. Davis, Tim Y. James, John R. Cooley, Daniel G. Panaccione, Jørgen Eilenberg, Henrik H. De Fine Licht, Angie M. Macias, Matthew C. Berger, Kristen L. Wickert, Cameron M. Stauder, Ellie J. Spahr, Matthew D. Maust, Amy M. Metheny, Chris Simon, Gene Kritsky, Kathie T. Hodge, Richard A. Humber, Terry Gullion, Dylan P. G. Short, Teiya Kijimoto, Dan Mozgai, Nidia Arguedas, View ORCID ProfileMatt T. Kasson
doi: https://doi.org/10.1101/375105
Greg R. Boyce
1Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia, 26506, USA
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Emile Gluck-Thaler
2Department of Plant Pathology, The Ohio State University, Columbus, Ohio 43210, USA
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Jason C. Slot
2Department of Plant Pathology, The Ohio State University, Columbus, Ohio 43210, USA
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Jason E. Stajich
3Department of Microbiology and Plant Pathology and Institute for Integrative Genome Biology, University of California, Riverside, California 92521, USA
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William J. Davis
4Department of Ecology and Evolution, University of Michigan, Ann Arbor, Michigan 48109, USA
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Tim Y. James
4Department of Ecology and Evolution, University of Michigan, Ann Arbor, Michigan 48109, USA
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John R. Cooley
5Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, Connecticut 06269, USA
6College of Integrative Sciences, Wesleyan University, Middletown Connecticut USA
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Daniel G. Panaccione
1Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia, 26506, USA
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Jørgen Eilenberg
7Department of Plant and Environmental Science, University of Copenhagen, Denmark
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Henrik H. De Fine Licht
7Department of Plant and Environmental Science, University of Copenhagen, Denmark
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Angie M. Macias
1Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia, 26506, USA
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Matthew C. Berger
1Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia, 26506, USA
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Kristen L. Wickert
1Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia, 26506, USA
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Cameron M. Stauder
1Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia, 26506, USA
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Ellie J. Spahr
1Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia, 26506, USA
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Matthew D. Maust
1Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia, 26506, USA
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Amy M. Metheny
1Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia, 26506, USA
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Chris Simon
5Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, Connecticut 06269, USA
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Gene Kritsky
8Department of Biology, Mount St. Joseph University, Cincinnati, Ohio 45233, USA
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Kathie T. Hodge
9Plant Pathology & Plant-Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853, USA
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Richard A. Humber
9Plant Pathology & Plant-Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853, USA
10USDA-ARS-NAA-BioIPM, Ithaca, New York 14853, USA
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Terry Gullion
11Department of Chemistry, West Virginia University, Morgantown, West Virginia, 26506, USA
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Dylan P. G. Short
12Amycel Spawnmate, Royal Oaks, California, 95067, USA
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Teiya Kijimoto
1Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia, 26506, USA
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Dan Mozgai
13Cicadamania.com, Sea Bright, New Jersey, 07760 USA
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Nidia Arguedas
14Cleveland Metroparks, Cleveland, Ohio, USA
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Matt T. Kasson
1Division of Plant and Soil Sciences, West Virginia University, Morgantown, West Virginia, 26506, USA
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  • ORCID record for Matt T. Kasson
  • For correspondence: mtkasson@mail.wvu.edu
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Abstract

Entomopathogenic fungi routinely kill their hosts before releasing infectious conidia, but select species keep their hosts alive while sporulating to enhance spore dispersal. Recent expression and metabolomics studies involving “host-killing” entomopathogens have helped unravel infection processes and host responses, yet the mechanisms underlying “active host transmission” in insects with Entomophthoralean fungal infections are completely unexplored. Here we report the discovery, through global and targeted metabolomics supported by metagenomics and proteomics, of the plant amphetamine, cathinone, in Massospora cicadina-infected periodical cicadas, and the mushroom tryptamine, psilocybin, in M. platypediae- and M. levispora-infected annual cicadas. The neurogenic activities of these alkaloids provide a hypothetical framework for a chemically induced extended phenotype of Massospora that alters cicada behavior by increasing endurance and suppressing feeding prior to death.

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Posted July 30, 2018.
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Discovery of psychoactive plant and mushroom alkaloids in behavior-modifying fungal cicada pathogens
Greg R. Boyce, Emile Gluck-Thaler, Jason C. Slot, Jason E. Stajich, William J. Davis, Tim Y. James, John R. Cooley, Daniel G. Panaccione, Jørgen Eilenberg, Henrik H. De Fine Licht, Angie M. Macias, Matthew C. Berger, Kristen L. Wickert, Cameron M. Stauder, Ellie J. Spahr, Matthew D. Maust, Amy M. Metheny, Chris Simon, Gene Kritsky, Kathie T. Hodge, Richard A. Humber, Terry Gullion, Dylan P. G. Short, Teiya Kijimoto, Dan Mozgai, Nidia Arguedas, Matt T. Kasson
bioRxiv 375105; doi: https://doi.org/10.1101/375105
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Discovery of psychoactive plant and mushroom alkaloids in behavior-modifying fungal cicada pathogens
Greg R. Boyce, Emile Gluck-Thaler, Jason C. Slot, Jason E. Stajich, William J. Davis, Tim Y. James, John R. Cooley, Daniel G. Panaccione, Jørgen Eilenberg, Henrik H. De Fine Licht, Angie M. Macias, Matthew C. Berger, Kristen L. Wickert, Cameron M. Stauder, Ellie J. Spahr, Matthew D. Maust, Amy M. Metheny, Chris Simon, Gene Kritsky, Kathie T. Hodge, Richard A. Humber, Terry Gullion, Dylan P. G. Short, Teiya Kijimoto, Dan Mozgai, Nidia Arguedas, Matt T. Kasson
bioRxiv 375105; doi: https://doi.org/10.1101/375105

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