The Torpid State: Recent Advances in Metabolic Adaptations and Protective Mechanisms†.

Sylvain Giroud,Roberto F Nespolo,Samantha M Logan,Carlos Mejías,Caroline Habold,Kenneth B Storey,Jérémy Terrien,Robert H Henning

doi:10.3389/fphys.2020.623665

Abstract

Torpor and hibernation are powerful strategies enabling animals to survive periods of low resource availability. The state of torpor results from an active and drastic reduction of an individual’s metabolic rate (MR) associated with a relatively pronounced decrease in body temperature. To date, several forms of torpor have been described in all three mammalian subclasses, i.e., monotremes, marsupials, and placentals, as well as in a few avian orders. This review highlights some of the characteristics, from the whole organism down to cellular and molecular aspects, associated with the torpor phenotype. The first part of this review focuses on the specific metabolic adaptations of torpor, as it is used by many species from temperate zones. This notably includes the endocrine changes involved in fat- and food-storing hibernating species, explaining biomedical implications of MR depression. We further compare adaptive mechanisms occurring in opportunistic vs. seasonal heterotherms, such as tropical and sub-tropical species. Such comparisons bring new insights into the metabolic origins of hibernation among tropical species, including resistance mechanisms to oxidative stress. The second section of this review emphasizes the mechanisms enabling heterotherms to protect their key organs against potential threats, such as reactive oxygen species, associated with the torpid state. We notably address the mechanisms of cellular rehabilitation and protection during torpor and hibernation, with an emphasis on the brain, a central organ requiring protection during torpor and recovery. Also, a special focus is given to the role of an ubiquitous and readily-diffusing molecule, hydrogen sulfide (H2S), in protecting against ischemia-reperfusion damage in various organs over the torpor-arousal cycle and during the torpid state. We conclude that (i) the flexibility of torpor use as an adaptive strategy enables different heterothermic species to substantially suppress their energy needs during periods of severely reduced food availability, (ii) the torpor phenotype implies marked metabolic adaptations from the whole organism down to cellular and molecular levels, and (iii) the torpid state is associated with highly efficient rehabilitation and protective mechanisms ensuring the continuity of proper bodily functions. Comparison of mechanisms in monotremes and marsupials is warranted for understanding the origin and evolution of mammalian torpor.

Highlights

Torpor and hibernation represent powerful strategies that enable animals to survive periods of low resource availability in their environment
Torpor is employed by all three mammalian subclasses, i.e., monotremes, marsupial, and placentals, as well as several avian orders (Ruf and Geiser, 2015) whereas hibernation is documented in mammals from all three subclasses but is known for only one bird species
We notably address mechanisms of cellular rehabilitation and protection during torpor and hibernation, with (i) an emphasis on the brain, a central organ to be protected during torpor and recovery after, and (ii) the role of a ubiquitous and readilydiffusing molecule, H2S, in protecting the integrity of organs against damage occurring over the torpor-arousal cycle and during the torpid state

Summary

Introduction

Torpor and hibernation represent powerful strategies that enable animals to survive periods of low resource availability in their environment. Animals show average minimum torpid MR of ∼19% of basal rates and lower their Tb to usually between 12 and 25◦C during torpor; torpor lasts less than 24 h and is accompanied by continued foraging (Ruf and Geiser, 2015). On the other hand, during hibernation, individuals achieve a minimum torpid MR of 4% of basal rates, along with a variable reduction of their Tb ranging on average for most species between 0 and 10◦C (Ruf and Geiser, 2015). Torpor is diverse in both mammals and birds, and is typically not as seasonal as hibernation (Geiser, 2020). The use of torpor is often associated with species inhabiting cold and seasonal habitats, such as temperate and arctic zones, but torpor is used by many non-Holarctic species, i.e., the tropics and southern hemisphere (Nowack et al, 2020)

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