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Label-free Quantitative Proteomics Combined With Transcriptomics Revealed the Importance of Cardiac Development in Producing the High Metabolic Capacity of Yellowfin Tuna (Thunnus Albacares)


 Tuna are commercially important fish throughout the world, and they are renowned for their endothermy, which allows them to maintain elevated temperatures in the oxidative locomotor muscles, viscera, brain, and eyes while occupying cold, productive, high-latitude waters. The endothermic mechanism is supported by a high heart rate and cardiac output, but the genes and proteins that participate in this cardiac function are poorly known. In this study, we combined label-free quantitative proteomics and transcriptomics to investigate the changes in the heart of yellowfin tuna (Thunnus albacares) before and after they developed endothermy. We identified 515,428 transcripts and 3355 protein groups in the hearts of two development stages of yellowfin tuna. Twenty-eight differentially expressed proteins were correlated with differentially expressed genes. The proteins that accelerate energy production were more highly expressed in the hearts of the large yellowfin tuna compared with the small specimens. Moreover, the proteins in the Z-disk, which protect against mechanical damage, were only detected in the hearts of large fish. These results indicate that as yellowfin tuna grow, the heart develops a self-protection strategy to cope with high metabolic rates and high mechanical forces. The differentially expressed proteins related to cardiac function, which are closely associated with striated muscle differentiation, glycosylation, and cardiac myocytes motility, were highly expressed in the larger (endothermic) tuna than that in the smaller (poikilothermic) tuna. Therefore, we suggest that the heart function of yellowfin tuna changes and improves during the transition from poikilothermic tuna (small size, 126 mm < fork length (FL) < 152 mm, 30 g < body weight < 46 g) to endothermic tuna (large size, 207 mm < FL < 235 mm, 170 g < body weight < 200 g). This is the first report of how gene and protein expression levels explain the strong heart function of yellowfin tuna.