Targeted metabolomics revealed the seasonal plasticity of skin color and pigment metabolites in ornamental koi carp

The koi carp is an ornamental fish that was obtained through artificial selection from the common carp (Cyprinus carpio L.). The most economically important traits of koi are their beautiful skin patterns in bright colors. As seasonality is an important factor in the biology and ecology of fish, we thus assumed that seasonal changes are involved in regulating the formation of skin color and patterns of koi carp. The white, red, cyan, and black skin colors from four varieties of scaleless koi carp (Doitsu Shiromuji (W), Doitsu Kohaku (WR), Doitsu Showa Sanke (WRI), and Kumonryu (WI)) were evaluated using the CIELab color space (lightness, redness, and yellowness) in different seasons. Compared to winter, the yellowness of the white color in all koi varieties decreased in summer and autumn. The black skin color areas in WRI and WI koi increased in summer and autumn compared to winter. The yellowness of the red color decreased only in WRI koi, while no changes were observed in WR koi. Targeted metabolomics analysis revealed that the levels of the structural pigment guanine of all koi varieties showed significant seasonal variation. Of seven detected carotenoids, the zeaxanthin and tunaxanthin contents in W, WI, and WRI koi changed with the seasons, while none of the carotenoids in WR koi were altered. Of the seven potential regulatory metabolites, epinephrine, melatonin, and cyclic adenosine monophosphate (cAMP) in all four koi varieties showed the highest levels in winter. A correlation analysis suggested that the seasonal changes in white skin color occurred through the epinephrine-cAMP pathway; melanin-dependent and carotenoid-dependent skin color changes occurred through melatonin in koi carp. This study demonstrated the seasonal plasticity of skin color in koi carp regulated by melatonin and epinephrine, associating with variety and color specificity.