The transcriptomic and proteomic responses of Daphnia pulex to changes in temperature and food supply comprise environment-specific and clone-specific elements

Abstract

BackgroundRegulatory adjustments to acute and chronic temperature changes are highly important for aquatic ectotherms because temperature affects their metabolic rate as well as the already low oxygen concentration in water, which can upset their energy balance. This also applies to severe changes in food supply. Thus, we studied on a molecular level (transcriptomics and/or proteomics) the immediate responses to heat stress and starvation and the acclimation to different temperatures in two clonal isolates of the model microcrustacean Daphnia pulex from more or less stressful environments, which showed a higher (clone M) or lower (clone G) tolerance to heat and starvation.ResultsThe transcriptomic responses of clone G to acute heat stress (from 20 °C to 30 °C) and temperature acclimation (10 °C, 20 °C, and 24 °C) and the proteomic responses of both clones to acute heat, starvation, and heat-and-starvation stress comprised environment-specific and clone-specific elements. Acute stress (in particular heat stress) led to an early upregulation of stress genes and proteins (e.g., molecular chaperones) and a downregulation of metabolic genes and proteins (e.g., hydrolases). The transcriptomic responses to temperature acclimation differed clearly. They also varied depending on the temperature level. Acclimation to higher temperatures comprised an upregulation of metabolic genes and, in case of 24 °C acclimation, a downregulation of genes for translational processes and collagens. The proteomic responses of the clones M and G differed at any type of stress. Clone M showed markedly stronger and less stress-specific proteomic responses than clone G, which included the consistent expression of a specific heat shock protein (HSP60) and vitellogenin (VTG-SOD).ConclusionsThe expression changes under acute stress can be interpreted as a switch from standard products of gene expression to stress-specific products. The expression changes under temperature acclimation probably served for an increase in energy intake (via digestion) and, if necessary, a decrease in energy expenditures (e.g, for translational processes). The stronger and less stress-specific proteomic responses of clone M indicate a lower degree of cell damage and an active preservation of the energy balance, which allowed adequate proteomic responses under stress, including the initiation of resting egg production (VTG-SOD expression) as an emergency reaction.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4742-6) contains supplementary material, which is available to authorized users.

Breaking Free from Thermodynamic Constraints: Thermal Acclimation and Metabolic Compensation in a freshwater zooplankton species

“…This includes correlated heat-tolerance response caused by exposure to mild hypoxia (Zeis et al, 2013;Coggins et al, 2017). Secondly, gene expression studies (Yampolsky et al, 2014b;Becker et al, 2018) indicate that acclimation to higher temperatures is accompanied by downregulation of a broad spectrum of gene expression-related proteins, consistent with the idea of adjustments aiming to decrease metabolic energy expenditures. These observations lead us to the hypothesis that acclimation to high temperature in Daphnia may be accomplished by means of metabolic compensation.…”

Environmentally-induced DNA methylation is inherited across generations in an aquatic keystone species (Daphnia magna)

“…Three of these studies used microcystin as stressor [35][36][37], two used zinc [38,39], and one used temperature [40]. Between 6% and 15% of the key genes differentially expressed in response to microcystin, zinc, or temperature as stressor are highly functionally similar to genes identified as differentially methylated in our data, though gene identity was not identical (Tables S13 and S14).…”

Heat shock protein gene expression is higher and more variable with thermal stress and mutation accumulation inDaphnia

“…Daphnia (Cladocera) have served as an ecological, evolutionary, and ecotoxicological model for well over a century (Schaack, 2008, Shaw et al, 2008, Yampolsky et al, 2014, and genomic resources are now available as well (e.g., Colbourne et al, 2011, Orsini et al, 2016, and Lee et al, 2019. Previously, the Daphnia system has been used to demonstrate differences in gene expression, protein production, and evidence for microevolutionary change at HSP genes in the lab in response to environmental change (Pauwels et al 2007, Mikulski et al, 2009, Becker et al, 2018. We predict both heat shock and mutation accumulation will increase HSP expression for both genes if they both act as mutational capacitors, but also that the interaction of the two stressors might have a synergistic effect on expression levels, compared to one stress alone.…”