Metabolic adaptations of starving purple sea urchins (Strongylocentrotus purpuratus) surviving in the barrens

Sea urchin grazing can drive kelp loss creating low productivity "barrens" with reduced biodiversity that may persist for decades. In these habitats, limited food driven by sea urchin herbivory reciprocally affects sea urchin physiology, yet the metabolic pathways enabling survival in the starvation conditions remain poorly understood. This study employed gas chromatography-mass spectrometry metabolomics to compare gonad metabolite profiles of purple sea urchins, Strongylocentrotus purpuratus, from barrens and adjacent kelp forest margins. Gonads from barren animals showed pronounced metabolic reallocations relative to kelp-margin animals, supporting energy production, redox balance, and membrane integrity. Carbohydrate metabolism was shifted towards increased glucose and gluconeogenesis with reduced alanine and glutamine as substrates for energy production. The pentose phosphate pathway fluxed towards energy production (supported by elevated sedoheptulose and mannoheptulose, and reduced glutamine and glutamate), rather than nucleotide synthesis and growth. Elevated amino acids (cysteine, cystine and lysine) reflected gonad protein catabolism, energy production and redox balance. Changes in lipid metabolism showed elevated monostearin from lipid breakdown, reduced heptanoic acid as energy substrate, and increased malonate supporting membrane integrity. This study reveals the specific metabolic adjustments purple sea urchins employ under food-limited conditions in barrens, diverting energy from reproduction to enhance long-term survival, potentially signaling challenges for kelp restoration.