Plasma metabolomic profiles reveal sex- and maturation-dependent metabolic strategies in sea lamprey (Petromyzon marinus)

Abstract

Introduction Adult sea lamprey (Petromyzon marinus) cease feeding and migrate to spawning streams where males build nests, undergo nal sexual maturation, and subsequently produce and release large quantities of bile acid pheromones that attract mature females. These animals are predicted to rearrange their metabolic pathways drastically to support their reproductive strategies, presenting advantageous opportunities to examine how sex and the maturation processes affect metabolism.Objectives The objective is to investigate the metabolic differences between sexes and maturation states in sea lamprey that support changes in physiological functions.Methods We compared plasma metabolomes of spawning and prespawning sea lamprey in both sexes using both non-targeted and targeted metabolomics approaches using UPLC/MS-MS with electrospray ionization in both positive and negative modes. The data were processed using Progenesis QI, Compound Discoverer and XCMS softwares for alignment, peak picking, and deconvolution of the peaks. Principle component analyses (PCA) and partial least squares discriminant analyses (PLS-DA) were performed using SIMCA and Metaboanalyst softwares to identify discriminating features, followed by fragmentation matching with extensive database search and pathway mapping. ResultsThe pheromonal bile acid biosynthesis was upregulated signi cantly in males compared to females. Spermiating males further upregulated bile acid biosynthesis by altering amino acid metabolisms, upregulating cofactors and nucleotide metabolisms, but downregulating carbohydrate and energy metabolisms.Conclusion Plasma metabolomes are sex-and maturation-dependent and re ect the special metabolic demands at each life stage and reproductive strategy.

LC-MS Based Metabolomic Profiling of Largehead Hairtail (Trichiurus japonicus) Ovary Reveals Metabolic Signatures of Ovarian Developmental Process (II–IV)

“…Protein has an important effect on the reproductive performance of aquatic animals, promoting the growth and maturation of ovarian cells, affecting precocious puberty, and benefiting the gonad index, fertility, and larval production (for details, see the review by Shi [48]). Several amino acids such as tryptophan (Try), phenylalanine (Phe), lysine (Lys), leucine (Leu), Valine (Val), alanine (Ala), serine (Ser), glutamic acid (Glu), Arginine (Arg), and aspartic acid (Asp) have been predicted to be important in the reproductive performance of fish [29,38,[49][50][51][52]. In the present study, a large number of different incomplete breakdown products of protein catabolism were found in the ovaries of T. japonicus, including oligopeptides, dipeptides, etc.…”

“…GnRH promotes the pituitary to release gonadotropin (GTH), which stimulates the synthesis and secretion of steroid hormones in the gonad, such as estradiol and progesterone, ultimately promoting the development of gonads [26]. Additionally, numerous signaling pathways and metabolites related to the metabolism of hormones, amino acids, lipids, and energy play important roles in this process [27][28][29].…”

“…To better understand gonadal development, metabolomics has been introduced to the reproduction research of aquatic animals [27][28][29]. Metabolomics is a powerful tool that can comprehensively analyze endogenous metabolites in biological systems, providing a better understanding of their metabolic functional states [30].…”

“…This approach is characterized by high sensitivity, high throughput, and rapidity [31]. Untargeted liquid chromatography (LC)-mass spectrometry (MS)-based metabolomics has successfully investigated the metabolic differences between sexes and maturation states of aquatic animals, including blunt snout bream (Megalobrama amblycephala) [27], Chinese sturgeon (Acipenser sinensis) [28], and sea lamprey (Petromyzon marinus) [29].…”