Molecular Response of the Brain to Cross-Generational Warming in a Coral Reef Fish

Abstract

Ocean warming is a threat to marine biodiversity, as it can push marine species beyond their physiological limits. Detrimental effects can occur when marine poikilotherms are exposed to conditions beyond their thermal optima. However, acclamatory mechanisms, such as plasticity, may enable compensation of detrimental effects if warming is experienced during development or across generations. Studies evaluating the molecular responses of fishes to warming have mostly focused on liver, muscle, and gonads, and little is known about the effects on other vital organs, including the brain. This study evaluated the transcriptional program of the brain in the coral reef fish Acanthochromis polyacanthus, exposed to two different warming scenarios: +1.5°C and +3.0°C, across successive generations. Fish were exposed to these conditions in both developmental (F1 and F2) and transgenerational settings (F2 only), as well as a treatment with step-wise warming between generations. The largest differences in gene expression were between individuals of the first and second generation, a pattern that was corroborated by pairwise comparisons between Control F1 and Control F2 (7,500 DEGs) fish. This large difference could be associated with parental effects, as parents of the F1 generation were collected from the wild, whereas parents of the F2 generation were reared in captivity. A general response to warming was observed at both temperatures and in developmental and transgenerational treatments included protein folding, oxygen transport (i.e., myoglobin), apoptosis and cell death, modification of cellular structure, mitochondrial activity, immunity and changes in circadian regulation. Treatments at the highest temperature showed a reduction in synaptic activity and neurotransmission, which matches previous behavioral observations in coral reef fishes. The Transgenerational +3.0°C treatment showed significant activation of the gene pls3, which is known for the development of neuro-muscular junctions under heat-stress. F2 samples exposed to step-wise warming showed an intermediate response, with few differentially expressed genes compared to developmental and transgenerational groups (except for Transgenerational +1.5°C). In combination with previous studies on liver gene expression, this study indicates that warming produces a molecular signature of stress response in A. polyacanthus that is influenced both by the intensity of warming as well as the duration of exposure.

Transposable Element Tissue-Specific Response to Temperature Stress in the Stenothermal Fish Puntius tetrazona

“…This fish, living at 21-28 • C, tolerates small thermal fluctuations and experiences serious histopathological damages at low temperatures [38]. Overall, ambient temperature is an abiotic factor that acts on physiological and metabolic activities of poikilothermic teleosts, and in particular, on those of stenothermal fish [34][35][36][37]. Transcriptional analyses conducted by Liu and colleagues (2020) [38] on RNA-seq data obtained from P. tetrazona exposed at 27 • C (control) and 13 • C (test) have showed a high number of differentially expressed genes: in brain and liver the upregulated genes prevailed, differently from gill, in which the downregulated genes were the most represented.…”

“…In addition, analyzing RNA-seq data, we demonstrated for the first time an activation of TE transcriptional activity in response to salinity variations in the marbled eel Anguilla marmorata [11]. Since most teleosts are poikilotherms, environmental stimuli affect physiological and metabolic activities in these organisms [34][35][36][37]. In particular, ambient temperature might be a critical factor for stenothermal fish in which thermal fluctuations are less tolerated.…”

Application of transcriptome analysis to investigate the effects of long-term low temperature stress on liver function in the tiger puffer (Takifugu rubripes)

“…And the digestive rate of fish is also affected at non-adaptive temperature (Yufera et al, 2019;Xing et al, 2022). Similarly, change in temperature also affected the circadian rhythm in fish (Liu et al, 2020;Bernal et al, 2022). In the present study, most genes in the enriched pathways related to digestion, metabolism, and environmental adaptation were down-regulated at low temperature and only a few genes were up-regulated, suggesting that low temperature inhibited normal digestion and metabolism in tiger puffers, and changed their TABLE 3 The number of up-regulated and down-regulated genes in the top three significantly enriched pathways.…”

Placing human gene families into their evolutionary context

“…Similar observations have been reported in fish brains exposed to elevated temperatures, where activation of compensatory mechanisms can be similar to those observed in humans with cerebrovascular strokes or other neuro-motor ailments. For example, Drosophila flies and fish exposed to warm environments for multiple generations can exhibit compensation by improving neuro-motor connections by the activation of the gene plastin 3, which in humans and mice is a protective modifier for spinal muscular atrophy [ 25 , 26 ]. Similarly, warm water conditions can lead to the activation of genes associated with low oxygen conditions in the nervous system of aquatic animals, as a result of the increased oxygen demand, and similar pathways are known to be activated in humans with strokes and circulatory deficiencies ( e.g.…”

“…Similarly, warm water conditions can lead to the activation of genes associated with low oxygen conditions in the nervous system of aquatic animals, as a result of the increased oxygen demand, and similar pathways are known to be activated in humans with strokes and circulatory deficiencies ( e.g. , neuroglobins) [ 26 ]. Given climate forecasts for the next century, further investigation of how gene families evolve under changing abiotic conditions will be vital for identifying potential future risks to public health.…”