Seasonally related metabolic changes and energy allocation associated with growth and reproductive phases in the liver of male goldfish (Carassius auratus)

Reproduction and growth follow a seasonal pattern in many fish species involving changes in gonadal development, growth, and metabolism. Significant metabolic energy is needed during gametogenesis in both female and male to produce hundreds of eggs and billions of sperms. Seasonal variations are controlled by the hormones of brain-pituitary-peripheral axis and are accompanied by significant metabolic changes. There is evidence that GnRH and GnIH are among the key neurohormones that regulate the reciprocal control of growth and reproduction. The objective of this study was to investigate changes in metabolic profile and energy allocation patterns at different stages of reproduction, using goldfish as a model organism and LC-MS as analytical platform for metabolic analysis. Goldfish undergoes a clear seasonal cycle of growth and reproduction. In vivo experiments were conducted at three different time point of the annual cycle: regressed gonadal phase (peak growth phase), mid gametogenesis and late gametogenesis. Emphasis is placed on changes in liver metabolic pathways to energetically sustain the physiological processes related to growth and reproduction. Moreover, we tested the hypothesis that GnRH and GnIH may play a role in the regulation of metabolism by investigating acute effects of these peptides at different stages of reproductive cycle. Significance: The findings in this paper provide novel information on the seasonal changes in basal metabolism during different stages of reproductive cycle, and evidence for differential allocation of energy during reciprocal control of reproduction and growth in goldfish. Chemometrics combined with pathway-driven bioinformatics elucidated a shift in the metabolic profile, indicating distinct patterns of energy allocation in the reproductive and growth seasons. Furthermore, to our knowledge this is the first study to provide evidence for a possible regulatory role of GnRH and GnIH in liver metabolism and energy allocation patterns associated with growth and reproductive processes. Together our findings present a framework for better understanding of the hormonally induced changes in metabolism to energetically sustain growth and reproduction in fish and other oviparous species undergoing seasonal cycle.

Automated summary

This study investigated metabolic profile and energy allocation patterns at different stages of reproduction in goldfish, revealing seasonal changes in basal metabolism and differential energy allocation in growth and reproductive cycles. The findings also suggest a possible regulatory role of GnRH and GnIH in liver metabolism and energy allocation patterns associated with growth and reproduction, providing insights into hormonally induced changes in metabolism in fish undergoing seasonal cycles.