Integrative analysis uncovers the mechanism underlying the environmental adaptation of an indigenous crucian carp (Carassius auratus gibelio) in Dong's Rice Fish Duck System

Abstract

The golden-back crucian carp (Carassius auratus gibelio), an indigenous fish with significant ecological, economic and cultural value, is found in Dong's Rice Fish Duck System, one of the Globally Important Agricultural Heritage Systems in the world. Its pigment cells undergo a complicated series of physiological and biochemical changes, which is mainly related to the specific local altitudinal, temperature and aquaculture methods. To obtain new insights into the underlying molecular mechanisms, a parallel analysis of morphological, physiological, biochemical, transcriptomic and proteomic of C. gibelio scales and skins with various colors were conducted. The greenish grey scales (Ggsc) and skins (Ggsk) were dominated by dendritic melanocytes, the golden scales (Gsc) and skins (Gsk) were dominated by xanthophores, and no iridophores were found. The activities of SOD and MDA were significantly high in Ggsc, while tyrosinase activity and melanin content were highest in Ggsk. Only two carotenoid components, xanthophyll and β-carotene were detected, and both abundant in Gsc and Gsk. These findings may be related to the irregular distribution of pigment cells. Furthermore, 1308 transcripts and 801 proteins were recognized with significant differential abundances in pairwise comparisons. Using KEGG pathway and protein-protein interaction network analysis, key candidate genes (e.g., tyr, tyrp1, dct, etc.) and proteins (e.g., ASP1, GOT1, HSPB1, etc.) involved in pigment cell differentiation and pigmentation in the melanogenesis, tyrosine metabolism, MAPK and wnt signaling pathway were identified. Noteworthily, we discovered that genes and proteins corresponding to the cardio adrenergic signaling system and cellular dynamics, such as plcb2, mctp2, MYH2 and TPM1, might influence formation and mobility of melanin granules and be the primary causes of golden skin. Finally, qRT-PCR validation indicated that sequencing results were reliable. With this exploratory multi-omics dataset, our results provide theoretical support to explain the relationship between metabolic regulation and phenotype formation in C. gibelio under special aquaculture conditions.