Impacts of thermal fluctuations on heat tolerance and its metabolomic basis in Arabidopsis thaliana, Drosophila melanogaster, and Orchesella cincta

Abstract

Temperature varies on a daily and seasonal scale and thermal fluctuations are predicted to become even more pronounced under future climate changes. Studies suggest that plastic responses are crucial for species’ ability to cope with thermal stress including variability in temperature, but most often laboratory studies on thermal adaptation in plant and ectotherm organisms are performed at constant temperatures and few species included. Recent studies using fluctuating thermal regimes find that thermal performance is affected by both temperature mean and fluctuations, and that plastic responses likely will differ between species according to life strategy and selective past. Here we investigate how acclimation to fluctuating or constant temperature regimes, but with the same mean temperature, impact on heat stress tolerance across a plant ( Arabidopsis thaliana ) and two arthropod species ( Orchesella cincta and Drosophila melanogaster ) inhabiting widely different thermal microhabitats and with varying capability for behavioral stress avoidance. Moreover, we investigate the underlying metabolic responses of acclimation using NMR metabolomics. We find increased heat tolerance for D . melanogaster and A . thaliana exposed to fluctuating acclimation temperatures, but not for O . cincta . The response was most pronounced for A . thaliana , which also showed a stronger metabolome response to thermal fluctuations than both arthropods. Generally, sugars were more abundant across A . thaliana and D . melanogaster when exposed to fluctuating compared to constant temperature, whereas amino acids were less abundant. This pattern was not evident for O . cincta , and generally we do not find much evidence for similar metabolomics responses to fluctuating temperature acclimation across species. Differences between the investigated species’ ecology and different ability to behaviorally thermoregulate may have shaped their physiological responses to thermal fluctuations.

Rapid Adjustments in Thermal Tolerance and the Metabolome to Daily Environmental Changes – A Field Study on the Arctic Seed Bug Nysius groenlandicus

“…Changes in polyols on the other hand have been associated with changes in heat tolerance ( Hendrix and Salvucci, 1998 ; Wolfe et al, 1998 ; Salvucci et al, 2000 ; Benoit et al, 2009 ). However, few have attempted to describe how these metabolites are affected by dynamic and fluctuating temperatures as encountered in nature (but see Kristensen et al, 2012 ; Noer et al, 2020 ; Sheldon et al, 2020 ).…”

The effect of thermal microenvironment in upper thermal tolerance plasticity in tropical tadpoles. Implications for vulnerability to climate warming

“…Also, Sørensen et al (2016) showed that the response to fluctuations is restricted to a much smaller set of genes in the transcriptomic response in contrast to mean constant temperatures, where a major part of the transcriptome is involved in the response, so it could be expected that CT max differed between both regimens. Also, Noer et al (2020) found stronger metabolome responses in thermally fluctuating conditions in Arabidopsis thaliana and Drosophila melanogaster that could be involved in heat resistance. Thus, the expression pattern of plastic responses may differ dramatically at constant and fluctuating temperatures (Podrabsky & Somero, 2004; Tomanek, 2010).…”

Additive effects of developmental acclimation and physiological syndromes on lifetime metabolic and water loss rates of a dry‐skinned ectotherm

“…At a given mean temperature, it has been suggested that a higher daily thermal fluctuation can lead to an increased tolerance to extreme temperature (Verheyen & Stoks, 2019). However, the effects of temporal variation of temperatures on acclimation responses of metabolism and other functional processes are often species dependent in ectotherms (Niehaus et al., 2011; Noer et al., 2020), and can also interact with changes in mean temperature (Bozinovic et al., 2011; Colinet et al., 2015). Further studies are required to elucidate whether acclimation responses of SMR and other functional traits in asp vipers are causally linked with changes in mean temperature, changes in the thermal variability or both.…”