Pyruvate Accumulation Is the First Line of Cell Defense against Heat Stress in a Fungus

ABSTRACT Heat tolerance is well known to be key to fungal survival in many habitats, but our mechanistic understanding of how organisms adapt to heat stress is still incomplete. Using Metarhizium robertsii, an emerging model organism for assessing evolutionary processes, we report that pyruvate is i...

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Autores principales:	Xing Zhang, Raymond J. St. Leger, Weiguo Fang
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Metarhizium robertsii entomopathogenic fungi heat stress Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/55addc89701147c4aff2fffa01a927d1
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spelling	oai:doaj.org-article:55addc89701147c4aff2fffa01a927d12021-11-15T15:51:50ZPyruvate Accumulation Is the First Line of Cell Defense against Heat Stress in a Fungus10.1128/mBio.01284-172150-7511https://doaj.org/article/55addc89701147c4aff2fffa01a927d12017-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01284-17https://doaj.org/toc/2150-7511ABSTRACT Heat tolerance is well known to be key to fungal survival in many habitats, but our mechanistic understanding of how organisms adapt to heat stress is still incomplete. Using Metarhizium robertsii, an emerging model organism for assessing evolutionary processes, we report that pyruvate is in the vanguard of molecules that scavenge heat-induced reactive oxygen species (ROS). We show that, as well as inducing a rapid burst of ROS production, heat stress also downregulates genes for pyruvate consumption. The accumulating pyruvate is the fastest acting of several M. robertsii ROS scavengers, efficiently reducing protein carbonylation, stabilizing mitochondrial membrane potential, and promoting fungal growth. The acetate produced from pyruvate-ROS reactions itself causes acid stress, tolerance to which is regulated by Hog1 mitogen-activated protein kinase. Heat stress also induces pyruvate accumulation in several other fungi, suggesting that scavenging of heat-induced ROS by pyruvate is widespread. IMPORTANCE Heat is a dangerous challenge for most organisms, as it denatures proteins and induces the production of ROS that inactivate proteins, lipid membranes, and DNA. How organisms respond to this stress is not fully understood. Using the experimentally tractable insect pathogen Metarhizium robertsii as a model organism, we show for the first time that heat stress induces pyruvate production and that this functions as the first line of defense against heat-induced ROS. Heat stress also induces rapid pyruvate accumulation in other fungi, suggesting that pyruvate is a common but unappreciated defense against stress.Xing ZhangRaymond J. St. LegerWeiguo FangAmerican Society for MicrobiologyarticleMetarhizium robertsiientomopathogenic fungiheat stressMicrobiologyQR1-502ENmBio, Vol 8, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Metarhizium robertsii entomopathogenic fungi heat stress Microbiology QR1-502
spellingShingle	Metarhizium robertsii entomopathogenic fungi heat stress Microbiology QR1-502 Xing Zhang Raymond J. St. Leger Weiguo Fang Pyruvate Accumulation Is the First Line of Cell Defense against Heat Stress in a Fungus
description	ABSTRACT Heat tolerance is well known to be key to fungal survival in many habitats, but our mechanistic understanding of how organisms adapt to heat stress is still incomplete. Using Metarhizium robertsii, an emerging model organism for assessing evolutionary processes, we report that pyruvate is in the vanguard of molecules that scavenge heat-induced reactive oxygen species (ROS). We show that, as well as inducing a rapid burst of ROS production, heat stress also downregulates genes for pyruvate consumption. The accumulating pyruvate is the fastest acting of several M. robertsii ROS scavengers, efficiently reducing protein carbonylation, stabilizing mitochondrial membrane potential, and promoting fungal growth. The acetate produced from pyruvate-ROS reactions itself causes acid stress, tolerance to which is regulated by Hog1 mitogen-activated protein kinase. Heat stress also induces pyruvate accumulation in several other fungi, suggesting that scavenging of heat-induced ROS by pyruvate is widespread. IMPORTANCE Heat is a dangerous challenge for most organisms, as it denatures proteins and induces the production of ROS that inactivate proteins, lipid membranes, and DNA. How organisms respond to this stress is not fully understood. Using the experimentally tractable insect pathogen Metarhizium robertsii as a model organism, we show for the first time that heat stress induces pyruvate production and that this functions as the first line of defense against heat-induced ROS. Heat stress also induces rapid pyruvate accumulation in other fungi, suggesting that pyruvate is a common but unappreciated defense against stress.
format	article
author	Xing Zhang Raymond J. St. Leger Weiguo Fang
author_facet	Xing Zhang Raymond J. St. Leger Weiguo Fang
author_sort	Xing Zhang
title	Pyruvate Accumulation Is the First Line of Cell Defense against Heat Stress in a Fungus
title_short	Pyruvate Accumulation Is the First Line of Cell Defense against Heat Stress in a Fungus
title_full	Pyruvate Accumulation Is the First Line of Cell Defense against Heat Stress in a Fungus
title_fullStr	Pyruvate Accumulation Is the First Line of Cell Defense against Heat Stress in a Fungus
title_full_unstemmed	Pyruvate Accumulation Is the First Line of Cell Defense against Heat Stress in a Fungus
title_sort	pyruvate accumulation is the first line of cell defense against heat stress in a fungus
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/55addc89701147c4aff2fffa01a927d1
work_keys_str_mv	AT xingzhang pyruvateaccumulationisthefirstlineofcelldefenseagainstheatstressinafungus AT raymondjstleger pyruvateaccumulationisthefirstlineofcelldefenseagainstheatstressinafungus AT weiguofang pyruvateaccumulationisthefirstlineofcelldefenseagainstheatstressinafungus
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Pyruvate Accumulation Is the First Line of Cell Defense against Heat Stress in a Fungus

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