Osmolytes vs. Anabolic Reserves: Contrasting Gonadal Metabolomes in Two Sympatric Mediterranean Sea Urchins

The Mediterranean sea urchins Paracentrotus lividus and Arbacia lixula are ecologically coexisting grazers that exert strong control on benthic algal communities but display strikingly different physiological and ecological traits. To explore the biochemical basis of these differences, we applied high-resolution magic angle spinning nuclear magnetic resonance (HR-MAS NMR) spectroscopy combined with multivariate chemometric analysis to characterize the gonadal metabolomes of both species. Distinct species-specific metabolic fingerprints were observed. A. lixula exhibited an osmolyte- and redox-oriented profile dominated by betaine, taurine, sarcosine, TMA, TMAO, carnitine, and creatine, reflecting enhanced homeostatic regulation, antioxidant protection, and mitochondrial flexibility. In contrast, P. lividus showed an amino-acid- and lipid-enriched anabolic metabolism characterized by high levels of lysine, glycine, glutamine, and proline, consistent with a reproductive strategy focused on energy storage and protein biosynthesis. Additional metabolites—including malonate, methylmalonate, uridine, xanthine, formaldehyde, methanol, and 3-carboxypropyl-trimethyl-ammonium—highlighted microbial mediation of methylated substrates and host–microbiota metabolic interactions. These results reveal two complementary adaptive strategies: a resilience-oriented osmolyte metabolism in A. lixula and an efficiency-oriented anabolic metabolism in P. lividus. The findings demonstrate that metabolomic divergence, coupled with distinct microbial associations, underpins the ecological and physiological differentiation of these sympatric echinoids. HR-MAS NMR metabolomics thus provides a powerful tool for elucidating adaptive biochemical pathways in marine invertebrate holobionts.