College of Ocean and Earth Sciences, Xiamen University
cological relevance of energy metabolism: transcriptional responses in energy sensing and expenditure to thermal and osmotic stresses in an intertidal limpet
MEL MEL 2015/12/21 284

Dr. Yunwei Dong has published a research article in Functional Ecology on December 15, 2015.

Citation: Yunwei Dong*, Shu Zhang, 2015. Ecological relevance of energy metabolism: transcriptional responses in energy sensing and expenditure to thermal and osmotic stresses in an intertidal limpet. Functional Ecology, DOI:10.1111/1365-2435.12625.


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, sirt1 and 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 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 (100.0%) of individuals placed in the highest-stress group (group 3), after 2 h freshwater spray at 18°C, the lower percentage (77.8%) of individuals in group 3 after 2 h 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 like 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.

Figure 1 Scheme showing the action of metabolic sensors, enzymes involving glycolysis and the tricarboxylic acid cycle (TCA cycle), and heat shock proteins. In low cellular energy status (high AMP/ATP ratio), AMP can induce the upregulation of AXIN, AMP-activated Kinase (AMPK) and Sirtuins (SIRT). AXIN plays an essential role for AMPK activation by orchestrating AMPK and Serine-threonine liver kinase B1 (LKB1) (Zhang et al. 2013). AMPK and SIRT can activate each other. The impact of AMPK and SIRT1 on peroxisome proliferator-activated receptor-γ coactivator 1α (PGC-1α), estrogen related receptor α (ERRα), forkhead box O (FOXO) and other transcriptional regulators will then affect carbohydrate and lipid metabolism to produce ATP for stress responses (Cantó et al. 2009).

Figure 2 Gene expression of limpets in different treatments and time points. Limpets were acclimated at 18°C and 30°C. After acclimation, limpets were aerially exposed or freshwater sprayed for 2 h for three consecutive days. On each day, three limpets (n = 3) in each treatments were randomly sampled at 16:00 (before aerial exposure/freshwater spray, 0 h), 18:00 (2h after aerial exposure/freshwater spray) and next 08:00 (14 h recovery from aerial exposure/freshwater spray) for measuring gene expressions. The color scale bar indicates log-transformed data, with green indicating downregulation, red indicating upregulation and black indicating no change compared to the median of the control samples.

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