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 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...

Full description

Bibliographic Details
Main Authors: Mohamed A. Farag, Heba A. El‐Kammar, Sabrin Abdelghany, Radwa H. El‐Akad
Format: Article
Language:English
Published: Wiley 2024-03-01
Series:Food Frontiers
Subjects:
Online Access:https://doi.org/10.1002/fft2.332
_version_ 1797257847638065152
author Mohamed A. Farag
Heba A. El‐Kammar
Sabrin Abdelghany
Radwa H. El‐Akad
author_facet Mohamed A. Farag
Heba A. El‐Kammar
Sabrin Abdelghany
Radwa H. El‐Akad
author_sort Mohamed A. Farag
collection DOAJ
description 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.
first_indexed 2024-04-24T22:44:09Z
format Article
id doaj.art-eaae695e36124d8c8dee7894e59bd931
institution Directory Open Access Journal
issn 2643-8429
language English
last_indexed 2024-04-24T22:44:09Z
publishDate 2024-03-01
publisher Wiley
record_format Article
series Food Frontiers
spelling doaj.art-eaae695e36124d8c8dee7894e59bd9312024-03-18T16:46:15ZengWileyFood Frontiers2643-84292024-03-015258460610.1002/fft2.332Seasonal 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 chemometricsMohamed A. Farag0Heba A. El‐Kammar1Sabrin Abdelghany2Radwa H. El‐Akad3Pharmacognosy Department College of PharmacyCairo UniversityCairoEgyptPharmacognosy Department College of PharmacyCairo UniversityCairoEgyptLeibniz Centre for Tropical Marine Research (ZMT)Bremen GermanyPharmacognosy Department Pharmaceutical and Drug Industries Research Institute, National Research Centre Cairo EgyptAbstract 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.https://doi.org/10.1002/fft2.332Actinopyga crassacytotoxicityHolothuria atrametabolite characterizationsea cucumberseasonal biomarkers
spellingShingle Mohamed A. Farag
Heba A. El‐Kammar
Sabrin Abdelghany
Radwa H. El‐Akad
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
Food Frontiers
Actinopyga crassa
cytotoxicity
Holothuria atra
metabolite characterization
sea cucumber
seasonal biomarkers
title 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
title_full 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
title_fullStr 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
title_full_unstemmed 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
title_short 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
title_sort 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
topic Actinopyga crassa
cytotoxicity
Holothuria atra
metabolite characterization
sea cucumber
seasonal biomarkers
url https://doi.org/10.1002/fft2.332
work_keys_str_mv AT mohamedafarag seasonalandtaxaimpactonedibleseacucumbersmetabolomeandinrelationtoitscytotoxicityasanalyzedviauhplchrmsmsbasedmolecularnetworkingandchemometrics
AT hebaaelkammar seasonalandtaxaimpactonedibleseacucumbersmetabolomeandinrelationtoitscytotoxicityasanalyzedviauhplchrmsmsbasedmolecularnetworkingandchemometrics
AT sabrinabdelghany seasonalandtaxaimpactonedibleseacucumbersmetabolomeandinrelationtoitscytotoxicityasanalyzedviauhplchrmsmsbasedmolecularnetworkingandchemometrics
AT radwahelakad seasonalandtaxaimpactonedibleseacucumbersmetabolomeandinrelationtoitscytotoxicityasanalyzedviauhplchrmsmsbasedmolecularnetworkingandchemometrics