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 for this work

Section for Organismal Biology

11 Citations (Scopus)

48 Downloads (Pure)

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.

Original language	English
Journal	Fungal Ecology
Volume	41
Pages (from-to)	147-164
Number of pages	18
ISSN	1754-5048
DOIs	https://doi.org/10.1016/j.funeco.2019.06.002
Publication status	Published - 1 Oct 2019

Keywords

Amphetamine
Cathinone
Entomopathogen
Entomophthorales
Invertebrate pathology
Magicicada
Massospora
Okanagana
Platypedia
Psilocin
Psilocybin
Tryptamine
Zoopagomycota

Access to Document

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

Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying cicada pathogensFinal published version, 2.56 MBLicence: CC BY-NC-ND

Cite this

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, vol. 41, pp. 147-164. https://doi.org/10.1016/j.funeco.2019.06.002

@article{f42ac7305c7b4a2394eb326920f9d5f9,

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",

publisher = "Elsevier",

}

TY - JOUR

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

Keywords

Access to Document

Other files and links

Fingerprint

Cite this