Biochemical metabolomic profiling of the Crown-of-Thorns Starfish (Acanthaster): New insight into its biology for improved pest management

The Crown-of-Thorns Starfish (COTS), Acanthaster species, is a voracious coral predator that destroys coral reefs when in outbreak status. The baseline metabolite and lipid biomolecules of 10 COTS tissues, including eggs from gravid fe-males, were investigated in this study to provide insight into their biology and identify avenues for control. Targeted and untargeted metabolite-and lipidomics-based mass spectrometry approaches were used to obtain tissue-specific metabolite and lipid profiles. Across all COTS tissues, 410 metabolites and 367 lipids were identified. Most abundant were amino acids and peptides (18.7%) and wax esters (17%). There were 262 metabolites and 192 lipids identified in COTS eggs. Wax esters were more abundant in the eggs (30%) followed by triacylglycerols (TG), amino acids, and pep-tides. The diversity of asterosaponins in eggs (34) was higher than in tissues (2). Several asterosaponins known to mod-ulate sperm acrosome reaction were putatively identified, including glycoside B, asterosaponin-4 (Co-Aris III), and regularoside B (asterosaponin A). The saponins saponin A, thornasteroside A, hillaside B, and non-saponins dictyol J and axinellamine B which have been shown to possess defensive properties, were found in abundance in gonads, skin, and radial nerve tissues. Inosine and 2-hexyldecanoic acid are the most abundant metabolites in tissues and eggs. As a secondary metabolite of purine degradation, inosine plays an important role in purine biosynthesis, while 2-hexyldecanoic acid is known to suppress side-chain crystallization during the synthesis of amphiphilic macromole-cules (i.e., phospholipids). These significant spatial changes in metabolite, lipid, and asterosaponin profiles enabled unique insights into key biological tissue-specific processes that could be manipulated to better control COTS popula-tions. Our findings highlight COTS as a novel source of molecules with therapeutic and cosmetic properties (ceramides, sphingolipids, carnosine, and inosine). These outcomes will be highly relevant for the development of strategies for COTS management including chemotaxis-based biocontrol and exploitation of COTS carcasses for the extraction of commercial molecules.

Automated summary

This study investigated the metabolite and lipid profiles of Crown-of-Thorns Starfish (COTS) tissues, including eggs. A total of 410 metabolites and 367 lipids were identified, with amino acids and peptides being the most abundant. COTS eggs had more diverse asterosaponins compared to other tissues. Metabolite and lipid profiles provided insights into tissue-specific processes and potential control strategies of COTS populations. Additionally, COTS was found to be a novel source of molecules with therapeutic and cosmetic properties.