Skeletal muscle and cardiac transcriptomics of a regionally endothermic fish, the Pacific bluefin tuna, Thunnus orientalis

Adam Ciezarek,Luke Gardner,Vincent Savolainen,Barbara Block

doi:10.1186/s12864-020-07058-z

Abstract

BackgroundThe Pacific bluefin tuna (Thunnus orientalis) is a regionally endothermic fish that maintains temperatures in their swimming musculature, eyes, brain and viscera above that of the ambient water. Within their skeletal muscle, a thermal gradient exists, with deep muscles, close to the backbone, operating at elevated temperatures compared to superficial muscles near the skin. Their heart, by contrast, operates at ambient temperature, which in bluefin tunas can range widely. Cardiac function in tunas reduces in cold waters, yet the heart must continue to supply blood for metabolically demanding endothermic tissues. Physiological studies indicate Pacific bluefin tuna have an elevated cardiac capacity and increased cold-tolerance compared to warm-water tuna species, primarily enabled by increased capacity for sarcoplasmic reticulum calcium cycling within the cardiac muscles.ResultsHere, we compare tissue-specific gene-expression profiles of different cardiac and skeletal muscle tissues in Pacific bluefin tuna. There was little difference in the overall expression of calcium-cycling and cardiac contraction pathways between atrium and ventricle. However, expression of a key sarcoplasmic reticulum calcium-cycling gene, SERCA2b, which plays a key role maintaining intracellular calcium stores, was higher in atrium than ventricle. Expression of genes involved in aerobic metabolism and cardiac contraction were higher in the ventricle than atrium. The two morphologically distinct tissues that derive the ventricle, spongy and compact myocardium, had near-identical levels of gene expression. More genes had higher expression in the cool, superficial muscle than in the warm, deep muscle in both the aerobic red muscle (slow-twitch) and anaerobic white muscle (fast-twitch), suggesting thermal compensation.ConclusionsWe find evidence of widespread transcriptomic differences between the Pacific tuna ventricle and atrium, with potentially higher rates of calcium cycling in the atrium associated with the higher expression of SERCA2b compared to the ventricle. We find no evidence that genes associated with thermogenesis are upregulated in the deep, warm muscle compared to superficial, cool muscle. Heat generation may be enabled by by the high aerobic capacity of bluefin tuna red muscle.

Highlights

The Pacific bluefin tuna (Thunnus orientalis) is a regionally endothermic fish that maintains temperatures in their swimming musculature, eyes, brain and viscera above that of the ambient water
There is no upregulation of calcium cycling pathways overall, we find upregulation of a key Ca2+ cycling gene, SERCA2b, in the atrium compared to the ventricle
Between 20 and 27 million paired-end reads were retained after trimming for adapter sequences and low-quality bases for each sample, of which 90.5–98.3% pseudo-aligned to the reference Pacific bluefin tuna transcriptome (Table 1) [56]

Summary

Introduction

The Pacific bluefin tuna (Thunnus orientalis) is a regionally endothermic fish that maintains temperatures in their swimming musculature, eyes, brain and viscera above that of the ambient water Within their skeletal muscle, a thermal gradient exists, with deep muscles, close to the backbone, operating at elevated temperatures compared to superficial muscles near the skin. Thunnus orientalis, migrate across the entire Pacific ocean as juveniles and sub-adults, and have an extensive thermal tolerance range when foraging in seas ranging around 5–29 °C [1, 2] This tolerance of cooler waters is partly enabled by regional endothermy, as counter-current heat exchangers allow three species of bluefin tunas to retain metabolic heat, resulting in elevated temperatures of the viscera, brain, eye and locomotory muscle [3, 4]. Pacific bluefin tuna experience bradycardia in the cold, the heart maintains a regular cardiac rhythm at lower temperatures compared to less cold-tolerant Thunnus species [11, 13]

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