Environmental acidification drives inter-organ energy mobilization to enhance reproductive performance in medaka (Oryzias latipes)

Abstract

Anthropogenically environmental acidification impacts aquatic organisms, including teleosts, the largest group of vertebrates. Despite its significance, how teleosts allocate nutrient and energy among their organs to cope with acidic stress remains unclear. Our integrated analysis of physiological, metabolic, and gene expression data reveals that Japanese medaka (Oryzias latipes) mobilize energy resources among organs in response to acidic conditions. We found that the muscles lost carbohydrates and proteins and the liver accumulates all macronutrients in both sexes. Notably, female-specific energy mobilization between the liver and ovary were triggered by estrogen signaling, resulting in improved oocyte maturation and ovulation. Female produced more offspring under acidic stress. Furthermore, the offspring embryos exhibited smaller diameters and earlier hatching but demonstrated growth rates and acid tolerance. These metabolic changes suggest a trade-off in energy allocation by suppressing basal maintenance (33 % decrease in oxygen consumption) and growth (25 % decrease in muscle mass) but enhancing energy storage (159 % increase in liver mass in males and 127 % in females) and reproduction (165 % increase in ovary mass). This reallocation may improve medaka fitness and population sustainability in acidic environments. Further investigation into more species is needed to project the survival of aquatic animals in an acidified future.