Seasonal and taxa impact on edible sea cucumber's metabolome and in relation to its cytotoxicity as analyzed via UHPLC/HR‐MS/MS‐based molecular networking and chemometrics

Abstract

Abstract Sea cucumbers, belonging to class Holothuroidea, are marine invertebrates with substantial bioactive compounds. This study provides the first comparative metabolome profiling of Holothuria atra and Actinopyga crassa sea cucumbers in relation to their season of collection to dissect between winter and summer samples, providing several first‐time reported metabolites as well as the effect of metabolome variation on their cytotoxic activity against colon and prostate cancer cell lines. Ultrahigh‐performance liquid chromatography coupled with high‐resolution mass spectrometry and global natural products social molecular networking followed by multivariate data analysis were employed for metabolite profiling and seasonal biomarker assignment for each species. The cytotoxic activity was evaluated using in vitro assays against prostate and colon cancer cell lines. A total of 113 metabolites were annotated in both species, including 4 organic acids, 21 sulfoquinovosyl glycerol (sulfolipids), 5 alkyl sulfates, 13 sulfated/saponins, 8 sulfated/triterpene mono/di‐glycosides, 10 triterpenes, 13 sulfated/sterols, 32 phospholipids, 4 sphingolipids, and 3 glycerolipids, several of which are new or first‐time reported. Multivariate data analyses revealed lipid accumulation in summer samples versus triterpene and saponin enrichment in winter‐collected samples, particularly in H. atra, rationalizing its potent cytotoxic activity (IC50 6–12 µg/mL) as revealed using a regression model. However, winter‐collected samples of A. crassa are relatively the least abundant in antinutrient saponins, thus considered to have higher food value.

Keywords

• Actinopyga crassa
• cytotoxicity
• Holothuria atra
• metabolite characterization
• sea cucumber
• seasonal biomarkers