Coral Lipidome: Molecular Species of Phospholipids, Glycolipids, Betaine Lipids, and Sphingophosphonolipids

Abstract

Coral reefs are the most biodiversity-rich ecosystems in the world's oceans. Coral establishes complex interactions with various microorganisms that constitute an important part of the coral holobiont. The best-known coral endosymbionts are Symbiodiniaceae dinoflagellates. Each member of the coral microbiome contributes to its total lipidome, which integrates many molecular species. The present study summarizes available information on the molecular species of the plasma membrane lipids of the coral host and its dinoflagellates (phosphatidylcholine (PC), phosphatidylethanolamine (PE), phosphatidylserine (PS), phosphatidylinositol (PI), ceramideaminoethylphosphonate, and diacylglyceryl-3-O-carboxyhydroxymethylcholine), and the thylakoid membrane lipids of dinoflagellates (phosphatidylglycerol (PG) and glycolipids). Alkyl chains of PC and PE molecular species differ between tropical and cold-water coral species, and features of their acyl chains depend on the coral's taxonomic position. PS and PI structural features are associated with the presence of an exoskeleton in the corals. The dinoflagellate thermosensitivity affects the profiles of PG and glycolipid molecular species, which can be modified by the coral host. Coral microbiome members, such as bacteria and fungi, can also be the source of the alkyl and acyl chains of coral membrane lipids. The lipidomics approach, providing broader and more detailed information about coral lipid composition, opens up new opportunities in the study of biochemistry and ecology of corals.

Keywords: Cnidaria; Hexacorallia; Millepora; Octocorallia; ceramideaminoethylphosphonate; gorgonian corals; lipidomics; plasma membrane.

Figure 1

Taxon tree of the phylum Cnidaria [8].

Figure 2

Lipidome features of corals. (a) A principal component analysis (PCA) of phosphatidylcholine (PC) molecular species composition with different fatty acids (FAs): saturated FAs (SFAs), monounsaturated FAs (MUFAs), C₁₆ polyunsaturated FAs (PUFAs), C₁₈ PUFAs, C₂₀ PUFAs, C₂₂ PUFAs, and C₂₄ PUFAs; (b) clustering of these FAs. (c) PCA of PC molecular species with different alkyl chains: 14:0alk, 14:1alk, 16:0alk, 16:1alk, 18:0alk, 18:1alk, 20:0alk, and 20:1alk; (d) their clustering. (e) PCA of phosphatidylethanolamine (PE) molecular species with different saturation degree of alkyl chains: saturated (Sat_alk), monounsaturated (Mono_alk), and polyunsaturated; (f) their clustering. (g) PCA of PE molecular species with different FAs: C16 PUFAs, C18 PUFAs, 16:1 FA, hydroxylated FAs (OH-FAs), 20:4 and 20:5 FAs, 20:3, 22:2, and 24:3 FAs, 22:4, 22:5, and 22:6 FAs, 24:5 and 24:6 FAs; (h) their clustering. The preliminary data were arcsine-transformed prior to the PCA (eigenvalues of all components > 1) and cluster analysis (tree clustering, wards method, and Euclidean distances) [59]. The acronyms of coral species are as follows: SH—Sinularia heterospiculata; SS—S. siaesensis; SM—S. macropodia; CS—Capnella sp.; JF—Junceella fragilis; DS—Dichotella sp.; MS—Menella sp.; AR—Astrogorgia rubra; AC—Acropora cerealis; PT—Palythoa tuberculosa; SC—Seriatopora caliendrum; AS—Allopora stejnegeri; GR—Gersemia rubiformis; MP—Millepora platyphylla; MD—M. dichotoma.

Figure 3

Lipidome features of corals. (a) Three-dimensional scatter plot of contents of total alkylacyl forms of phosphatidylserine (PS), all PS forms with saturated and monounsaturated alkyl and acyl chains. The dotted line outlines the following clusters: red, by content of total alkylacyl forms of PS; green, by saturation of PS. (b) A principal component analysis of PS molecular species composition with different fatty acids (FAs): monounsaturated FAs (MUFAs), C₂₀ polyunsaturated FAs (PUFAs), C₂₂ PUFAs, and C₂₄ PUFAs. (c) Three-dimensional scatter plot of contents of total alkylacyl forms of phosphatidylinositol (PI), PI molecular species with saturated and monounsaturated alkyl and acyl chains. (d) Three-dimensional scatter plot of PI molecular species with different FAs: C₂₀ PUFAs, C₂₂ PUFAs, and C₂₄ PUFAs, and their clustering. The dotted line outlines clusters. The preliminary data were arcsine-transformed prior to the PCA (eigenvalues of all components > 1) and cluster analysis (tree clustering, wards method, and Euclidean distances) [59]. The acronyms of coral species are as follows: SH—Sinularia heterospiculata; SS—S. siaesensis; SM—S. macropodia; CS—Capnella sp.; JF—Junceella fragilis; DS—Dichotella sp.; MS—Menella sp.; AR—Astrogorgia rubra; AC—Acropora cerealis; PT—Palythoa tuberculosa; XS—Xenia sp.; AS—Allopora stejnegeri; GR—Gersemia rubiformis; MP—Millepora platyphylla; MD—M. dichotoma.

Figure 4

Lipidome features of corals. A heat map of glycolipid molecular species (sulfoquinovosyldiacylglycerol (SQDG), mono- and digalactosyldiacylglycerol (MGDG and DGDG)) grouped on the basis of acyl chain length (C_28–31, C_30–34, C_32–34, C_35–40, C_36–38, C_39–42, and C_40–42) and fatty acid residues with different unsaturation degrees (saturated fatty acids (SFA), monounsaturated fatty acids (MUFA), polyunsaturated fatty acids (PUFA), FAs with 0–5 double bonds (d.b.), 6–8 d.b., and 9–11 d.b.); with clustering analyses (tree clustering, wards method, and Euclidean distances). The scale bar under the heat map(s) represents the arcsine-transformed relative abundance of lipid content in the samples [59]. The acronyms of coral or symbiont species are as follows: SH—Sinularia heterospiculata; SS—S. siaesensis; C(S)—Cladocopium C1/C3 from S. heterospiculata; D(S)—Durusdinium trenchii from S. heterospiculata; JF—Junceella fragilis; C(A)—Cladocopium C1 from Acropora valida; D(A)—D. trenchii (D1) from A. valida; D(P)—D. trenchii (D1) and Cladocopium C1/C3 from Palythoa tuberculosa; AC—A. cerealis; PT—P. tuberculosa; MP—Millepora platyphylla; MD—M. dichotoma.