Ecological relevance of energy metabolism: transcriptional responses in energy sensing and expenditure to thermal and osmotic stresses in an intertidal limpet

Abstract

Summary For rocky intertidal species that experience changes in a number of potential stressors seasonally and during the tidal cycle, sensing cellular energy status and modulating it adaptively may be crucial for responding to stressor effects. However, the responses of energy metabolism of intertidal species to multiple sublethal stressors are still unclear. Here, we examined gene expression profiles of biomarkers related to sensing of cellular energy status and regulation of catabolism and energy expenditure in a mid‐intertidal limpet Cellana toreuma for elucidating the species’ cellular energy responses stresses from high temperature, desiccation and rainfall. Expression levels of genes encoding metabolic regulators [two subunits of AMP‐activated protein kinase, ampkα, ampkβ; Fu gene inhibition axis formation, axin; two sirtuins, NAD‐dependent deacetylase sirtuin‐1 (sirt1); NAD‐dependent deacetylase sirtuin‐5 (sirt5)], metabolic enzymes (hexokinase, hk; pyruvate kinase, pk; isocitrate dehydrogenase, idh) and heat shock protein 70 (hsp70) were quantified in specimens exposed to different temperatures and aerial/freshwater spray conditions. Based on the gene expression patterns, all individuals could be divided into three groups with divergent cellular energy status, indicating that the selected target genes are appropriate indicators of cellular metabolism. The divergent gene expression patterns indicated a sequence in which individuals from group 1, group 2 and group 3 were faced with increasing energy stress. The frequency distributions of individuals in the three groups were different among different time points and treatments, indicating that high temperature, desiccation, and rainfall, singly or in combination, could cause energy stress. Compared to the high percentage (100%) of individuals placed in the highest‐stress group (group 3), after 2 h of freshwater spray at 18 °C, the lower percentage (77·8%) of individuals in group 3 after 2 h of freshwater spray at 30 °C indicated the existence of interactive effects of high temperature and rain; high temperature resulted in a lower response of cellular energy metabolism to rainfall. Sublethal environmental stresses from single stressors such as temperature or osmotic challenges can lead to cellular energy stress. Interactions among stressors may lead to a complex overall effect on cellular energy status in intertidal species.