Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying 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

doi:10.1016/j.funeco.2019.06.002

Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying 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. HodgeRichard A. Humber, Terry Gullion, Dylan P.G. Short, Teiya Kijimoto, Dan Mozgai, Nidia Arguedas, Matt T. Kasson^*

^*Corresponding author af dette arbejde

SOBI

11 Citationer (Scopus)

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Abstract

Entomopathogenic fungi routinely kill their hosts before releasing infectious spores, but a few species keep insects alive while sporulating, which enhances dispersal. Transcriptomics- and metabolomics-based studies of entomopathogens with post-mortem dissemination from their parasitized hosts have unraveled infection processes and host responses. However, the mechanisms underlying active spore transmission by Entomophthoralean fungi in living insects remain elusive. Here we report the discovery, through metabolomics, of the plant-associated amphetamine, cathinone, in four Massospora cicadina-infected periodical cicada populations, and the mushroom-associated tryptamine, psilocybin, in annual cicadas infected with Massospora platypediae or Massospora levispora, which likely represent a single fungal species. The absence of some fungal enzymes necessary for cathinone and psilocybin biosynthesis along with the inability to detect intermediate metabolites or gene orthologs are consistent with possibly novel biosynthesis pathways in Massospora. The neurogenic activities of these compounds suggest the extended phenotype of Massospora that modifies cicada behavior to maximize dissemination is chemically-induced.

Originalsprog	Engelsk
Tidsskrift	Fungal Ecology
Vol/bind	41
Sider (fra-til)	147-164
Antal sider	18
ISSN	1754-5048
DOI	https://doi.org/10.1016/j.funeco.2019.06.002
Status	Udgivet - 1 okt. 2019

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10.1016/j.funeco.2019.06.002Licens: CC BY-NC-ND

Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying cicada pathogensForlagets udgivne version, 2,56 MBLicens: CC BY-NC-ND

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Boyce, G. R., Gluck-Thaler, E., Slot, J. C., Stajich, J. E., Davis, W. J., James, T. Y., Cooley, J. R., Panaccione, D. G., Eilenberg, J., De Fine Licht, H. H., Macias, A. M., Berger, M. C., Wickert, K. L., Stauder, C. M., Spahr, E. J., Maust, M. D., Metheny, A. M., Simon, C., Kritsky, G., ... Kasson, M. T. (2019). Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying cicada pathogens. Fungal Ecology, 41, 147-164. https://doi.org/10.1016/j.funeco.2019.06.002

Boyce, GR, Gluck-Thaler, E, Slot, JC, Stajich, JE, Davis, WJ, James, TY, Cooley, JR, Panaccione, DG, Eilenberg, J , De Fine Licht, HH, Macias, AM, Berger, MC, Wickert, KL, Stauder, CM, Spahr, EJ, Maust, MD, Metheny, AM, Simon, C, Kritsky, G, Hodge, KT, Humber, RA, Gullion, T, Short, DPG, Kijimoto, T, Mozgai, D, Arguedas, N & Kasson, MT 2019, 'Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying cicada pathogens', Fungal Ecology, bind 41, s. 147-164. https://doi.org/10.1016/j.funeco.2019.06.002

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title = "Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying cicada pathogens",

abstract = "Entomopathogenic fungi routinely kill their hosts before releasing infectious spores, but a few species keep insects alive while sporulating, which enhances dispersal. Transcriptomics- and metabolomics-based studies of entomopathogens with post-mortem dissemination from their parasitized hosts have unraveled infection processes and host responses. However, the mechanisms underlying active spore transmission by Entomophthoralean fungi in living insects remain elusive. Here we report the discovery, through metabolomics, of the plant-associated amphetamine, cathinone, in four Massospora cicadina-infected periodical cicada populations, and the mushroom-associated tryptamine, psilocybin, in annual cicadas infected with Massospora platypediae or Massospora levispora, which likely represent a single fungal species. The absence of some fungal enzymes necessary for cathinone and psilocybin biosynthesis along with the inability to detect intermediate metabolites or gene orthologs are consistent with possibly novel biosynthesis pathways in Massospora. The neurogenic activities of these compounds suggest the extended phenotype of Massospora that modifies cicada behavior to maximize dissemination is chemically-induced.",

keywords = "Amphetamine, Cathinone, Entomopathogen, Entomophthorales, Invertebrate pathology, Magicicada, Massospora, Okanagana, Platypedia, Psilocin, Psilocybin, Tryptamine, Zoopagomycota",

author = "Boyce, {Greg R.} and Emile Gluck-Thaler and Slot, {Jason C.} and Stajich, {Jason E.} and Davis, {William J.} and James, {Tim Y.} and Cooley, {John R.} and Panaccione, {Daniel G.} and J{\o}rgen Eilenberg and {De Fine Licht}, {Henrik H.} and Macias, {Angie M.} and Berger, {Matthew C.} and Wickert, {Kristen L.} and Stauder, {Cameron M.} and Spahr, {Ellie J.} and Maust, {Matthew D.} and Metheny, {Amy M.} and Chris Simon and Gene Kritsky and Hodge, {Kathie T.} and Humber, {Richard A.} and Terry Gullion and Short, {Dylan P.G.} and Teiya Kijimoto and Dan Mozgai and Nidia Arguedas and Kasson, {Matt T.}",

year = "2019",

month = oct,

day = "1",

doi = "10.1016/j.funeco.2019.06.002",

language = "English",

volume = "41",

pages = "147--164",

journal = "Fungal Ecology",

issn = "1754-5048",

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T1 - Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying cicada pathogens

AU - Boyce, Greg R.

AU - Gluck-Thaler, Emile

AU - Slot, Jason C.

AU - Stajich, Jason E.

AU - Davis, William J.

AU - James, Tim Y.

AU - Cooley, John R.

AU - Panaccione, Daniel G.

AU - Eilenberg, Jørgen

AU - De Fine Licht, Henrik H.

AU - Macias, Angie M.

AU - Berger, Matthew C.

AU - Wickert, Kristen L.

AU - Stauder, Cameron M.

AU - Spahr, Ellie J.

AU - Maust, Matthew D.

AU - Metheny, Amy M.

AU - Simon, Chris

AU - Kritsky, Gene

AU - Hodge, Kathie T.

AU - Humber, Richard A.

AU - Gullion, Terry

AU - Short, Dylan P.G.

AU - Kijimoto, Teiya

AU - Mozgai, Dan

AU - Arguedas, Nidia

AU - Kasson, Matt T.

PY - 2019/10/1

Y1 - 2019/10/1

N2 - Entomopathogenic fungi routinely kill their hosts before releasing infectious spores, but a few species keep insects alive while sporulating, which enhances dispersal. Transcriptomics- and metabolomics-based studies of entomopathogens with post-mortem dissemination from their parasitized hosts have unraveled infection processes and host responses. However, the mechanisms underlying active spore transmission by Entomophthoralean fungi in living insects remain elusive. Here we report the discovery, through metabolomics, of the plant-associated amphetamine, cathinone, in four Massospora cicadina-infected periodical cicada populations, and the mushroom-associated tryptamine, psilocybin, in annual cicadas infected with Massospora platypediae or Massospora levispora, which likely represent a single fungal species. The absence of some fungal enzymes necessary for cathinone and psilocybin biosynthesis along with the inability to detect intermediate metabolites or gene orthologs are consistent with possibly novel biosynthesis pathways in Massospora. The neurogenic activities of these compounds suggest the extended phenotype of Massospora that modifies cicada behavior to maximize dissemination is chemically-induced.

AB - Entomopathogenic fungi routinely kill their hosts before releasing infectious spores, but a few species keep insects alive while sporulating, which enhances dispersal. Transcriptomics- and metabolomics-based studies of entomopathogens with post-mortem dissemination from their parasitized hosts have unraveled infection processes and host responses. However, the mechanisms underlying active spore transmission by Entomophthoralean fungi in living insects remain elusive. Here we report the discovery, through metabolomics, of the plant-associated amphetamine, cathinone, in four Massospora cicadina-infected periodical cicada populations, and the mushroom-associated tryptamine, psilocybin, in annual cicadas infected with Massospora platypediae or Massospora levispora, which likely represent a single fungal species. The absence of some fungal enzymes necessary for cathinone and psilocybin biosynthesis along with the inability to detect intermediate metabolites or gene orthologs are consistent with possibly novel biosynthesis pathways in Massospora. The neurogenic activities of these compounds suggest the extended phenotype of Massospora that modifies cicada behavior to maximize dissemination is chemically-induced.

KW - Amphetamine

KW - Cathinone

KW - Entomopathogen

KW - Entomophthorales

KW - Invertebrate pathology

KW - Magicicada

KW - Massospora

KW - Okanagana

KW - Platypedia

KW - Psilocin

KW - Psilocybin

KW - Tryptamine

KW - Zoopagomycota

UR - http://www.scopus.com/inward/record.url?scp=85067621985&partnerID=8YFLogxK

U2 - 10.1016/j.funeco.2019.06.002

DO - 10.1016/j.funeco.2019.06.002

M3 - Journal article

C2 - 31768192

AN - SCOPUS:85067621985

SN - 1754-5048

VL - 41

SP - 147

EP - 164

JO - Fungal Ecology

JF - Fungal Ecology

ER -

Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying cicada pathogens

Abstract

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