Abstract
ABSTRACTHeat 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.
Highlights
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
This results in a reduction of protein carbonylation, stabilization of the Δ⌿m, and promotion of fungal growth
A very notable feature of pyruvate accumulation in M. robertsii hyphae is the rapidity of its induction, coincident with reactive oxygen species (ROS) production, and its speed of action as a scavenger
Summary
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). The endophytic insect-pathogenic fungus Metarhizium robertsii (formerly Metarhizium anisopliae) is an emerging model for the assessment of fungal evolution in natural communities It has a worldwide distribution from the arctic to the tropics [7, 8] and must have the necessary molecular machinery to adapt to heat and cold. Addition of pyruvate to cell suspensions of two microaerophilic protozoa (Giardia intestinalis and Hexamita inflata) facilitates their tolerance to oxidative stress by eliminating ROS [11] To our knowledge, this is the first study to document in any organism that heat treatment induces pyruvate accumulation. As heat induces pyruvate accumulation in five other fungi, pyruvate scavenging of heatinduced ROS could be widespread
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