Lipidomic profiling reveals biosynthetic relationships between phospholipids and diacylglycerol ethers in the deep-sea soft coral Paragorgia arborea

Abstract

The cold-water gorgonian coral Paragorgia arborea is considered as a foundation species of deep-sea ecosystems in the northern Atlantic and Pacific oceans. To advance lipidomic studies of deep-sea corals, molecular species compositions of diacylglycerol ethers (DAGE), which are specific storage lipids of corals, and structural glycerophospholipids (GPL) including ethanolamine, choline, inositol and serine GPL (PE, PC, PI, and PS, respectively) were analyzed in P. arborea by HPLC and tandem mass spectrometry. In DAGE molecules, alkyl groups (16:0, 14:0, and 18:1), polyunsaturated fatty acids (PUFA), and monounsaturated FA are mainly substituted the glycerol moiety at position sn-1, sn-2, and sn-3, respectively. The ether form (1-O-alkyl-2-acyl) predominates in PE and PC, while PI is comprised of the 1,2-diacyl form. Both ether and diacyl forms were observed in PS. At position sn-2, C20 PUFA are mainly attached to PC, but C24 PUFA, soft coral chemotaxonomic markers, concentrate in PS, PI, and PE. A comparison of non-polar parts of molecules has shown that DAGE, ether PE, and ether PC can originate from one set of 1-O-alkyl-2-acyl-sn-glycerols. Ether PE may be converted to ether PS by the base-exchange reaction. A diacylglycerol unit generated from phosphatidic acid can be a precursor for diacyl PS, PC, and PI. Thus, a lipidomic approach has confirmed the difference in biosynthetic origins between ether and diacyl lipids of deep-sea gorgonians.

Applications of lipidomics in marine organisms: progress, challenges and future perspectives

“…The use of lipidomics to understand the associations between organisms of different phyla has been the focus of several studies. Imbs et al have mapped the lipidome of soft corals, hydrocorals (cnidaria phylum) and nudibranch (mollusc phyla) to trace lipid dynamics in coral symbiotic associations (i.e., host coral and symbiotic dinoflagellates) and trophic relationships in predator-prey systems, such as nudibranch molluscs preying on soft corals (e.g., [123][124][125][126] ). Soft coral chemotaxonomic markers (e.g., tetracosapolyenoic acids (TPA), 24:5 n-6 and 24:6 n-3) have been used to trace nudibranch trophic relationships by analysing the structural composition of nudibranch lipid molecular species.…”

“…This study revealed the relationship between DAGE and ether PL, suggesting that DAGE, ether PE and ether PC originate from one set of 1-O-alkyl-2-acyl-snglycerols in this deep-sea gorgonian. 125 Marine invertebrates are relevant ingredients in several gastronomic traditions around the world, such as Mediterranean, This journal is © The Royal Society of Chemistry 2022 Atlantic, Korean, Chinese or Japanese diets. The edible parts of marine invertebrates are recognized as healthy and functional food ingredients, contributing to deliver essential lipids when introduced into human diet.…”

“…142 The analysis of marine invertebrate lipidome has demonstrated that these organisms are source of unique lipids with relevance for biological applications. The phosphonolipid CAEP has been identified in the deep-sea soft coral P. arborea, 125 the soft coral Sinularia siaesensis, 126 cold-water nudibranchs Dendronotus robustus and Dendronotus sp., 127 Millepora hydrocorals, 123 the Japanese edible jellyfish R. esculentum, 134 and the Galician mussel M. galloprovincialis, 141 among others (see ESI † Table S2). CAEP contains a P-C bond in their structure, which prevents the hydrolytic effect of phospholipase and phosphatase enzymes, keeping their unsaturated FA groups stable under oxidative conditions.…”

“…CAEP contains a P-C bond in their structure, which prevents the hydrolytic effect of phospholipase and phosphatase enzymes, keeping their unsaturated FA groups stable under oxidative conditions. 143 Ether PL [plasmanyl and plasmenyl (i.e., plasmalogens)] are abundant in marine invertebrates such as clams, 136 mussels, 141 soft corals, 125 hydrocorals, 128 nudibranchs 127 or sacoglossan sea slugs, 130 among other organisms. Plasmalogens have been recognized by their antioxidant properties, protecting PUFA or other vulnerable membrane lipids against oxidation.…”

Serine ether glycerophospholipids: Decrements in the frontal cortex associated with mild cognitive impairment and Alzheimer’s disease

“…Serine ether GPL (PSe; i.e., alkyl-acyl serine GPL; Figure 1 ) and serine plasmalogens (PSp; i.e., alkenyl-acyl serine GPL), have been reported from studies of human retina and optic nerve ( Nagy et al, 2012 ), human lens ( Deeley et al, 2008 , 2009 ; Ellis et al, 2010 ), rat prostate ( Pulido et al, 1986 ), the mouse macrophage cell line RAW 264.7 ( Ivanova et al, 2010 ), gills of bivalves ( Kraffe et al, 2004 ), the fungus pneumocystis carinii ( Kaneshiro et al, 1998 ), a number of bacteria ( van Golde et al, 1973 ; Oe et al, 2008 ; Rezanka et al, 2011 ), murine mamillary tumors ( Sekar et al, 2022 ), and coral ( Imbs and Velansky, 2021 ).…”