Coral Holobionts Possess Distinct Lipid Profiles That May Be Shaped by Symbiodiniaceae Taxonomy

Abstract

Symbiotic relationships are very important for corals. Abiotic stressors cause the acclimatization of cell membranes in symbionts, which possess different membrane acclimatization strategies. Membrane stability is determined by a unique lipid composition and, thus, the profile of thylakoid lipids can depend on coral symbiont species. We have analyzed and compared thylakoid lipidomes (mono- and digalactosyldiacylglycerols (MGDG and DGDG), sulfoquinovosyldiacylglycerols (SQDG), and phosphatidylglycerols (PG)) of crude extracts from symbiotic reef-building coral Acropora sp., the hydrocoral Millepora platyphylla, and the octocoral Sinularia flexibilis. S. flexibilis crude extracts were characterized by a very high SQDG/PG ratio, a DGDG/MGDG ratio < 1, a lower degree of galactolipid unsaturation, a higher content of SQDG with polyunsaturated fatty acids, and a thinner thylakoid membrane which may be explained by the presence of thermosensitive dinoflagellates Cladocopium C3. In contrast, crude extracts of M. platyphylla and Acropora sp. exhibited the lipidome features of thermotolerant Symbiodiniaceae. M. platyphylla and Acropora sp. colonies contained Cladocopium C3u and Cladocopium C71/C71a symbionts, respectively, and their lipidome profiles showed features that indicate thermotolerance. We suggest that an association with symbionts that exhibit the thermotolerant thylakoid lipidome features, combined with a high Symbiodiniaceae diversity, may facilitate further acclimatization/adaptation of M. platyphylla and Acropora sp. holobionts in the South China Sea.

Keywords: Symbiodiniaceae; corals; genetic analysis; lipidome; mass-spectrometry; thylakoid.

Figure 1

The lipidome features of the coral colonies Acropora sp. (A1–A5), Sinularia flexibilis (S1–S5), and Millepora platyphylla (M1–M5). (a) A ratio of total sulfoquinovosyldiacylglycerol (SQDG) to total phosphatidylglycerol (PG). (b) A heat map of SQDG molecular species grouped on the basis of chain length (C_28–32 and C_33–34) and fatty acids with different unsaturation degree (saturated fatty acids (SFA), monounsaturated fatty acids (MUFA), and polyunsaturated fatty acids (PUFA)) with a clustering (tree clustering, wards method, and Euclidean distances). The scale bar above the heatmap(s) represents the arcsine-transformed relative abundance of lipid content in the samples. Symbiodiniaceae community in corals was determined based on the internal transcribed spacer-2 (ITS2) region. Symbiodiniaceae type: “A1a”—Symbiodinium; “B1”—Breviolum; “C3”, “C3sg”, “C3u”, “C50bn”, “C66”, “C71/C71a”—Cladocopium; “D1”—Durusdinium. The green algae Ostreobium sp. (Bryopsidales, Ulvophyceae) in corals was determined based on the 23S rRNA gene sequences.

Figure 2

The lipidome features of the coral colonies Acropora sp. (A1–A5), Sinularia flexibilis (S1–S5), and Millepora platyphylla (M1–M5). (a) A ratio of total digalactosyldiacylglycerol (DGDG) to total monogalactosyldiacylglycerol (MGDG). (b) A heat map of galactolipid molecular species grouped on the basis of chain length (C_30–34, C_36–38, and C_40–42) with a clustering (tree clustering, wards method, and Euclidean distances). The scale bar above the heatmap(s) represents the arcsine-transformed relative abundance of lipid content in the samples. (c) A principal component analysis of the composition of galactolipid molecular species with different unsaturation degrees (with 0–5 double bonds (MGDG 0–5 d.b. and DGDG 0–5 d.b.), 6–8 double bonds (MGDG 6–8 d.b. and DGDG 6–8 d.b.), and 9–11 double bonds (MGDG 9–11 d.b. and DGDG 9–11 d.b.)). The dotted line outlines clusters (tree clustering, wards method, and Euclidean distances). Symbiodiniaceae community in corals was determined based on the internal transcribed spacer-2 (ITS2) region. Symbiodiniaceae type: A1a”—Symbiodinium; “B1”—Breviolum; “C3”, “C3sg”, “C3u”, “C50bn”, “C66”, “C71/C71a”—Cladocopium; “D1”—Durusdinium. The green algae Ostreobium sp. (Bryopsidales, Ulvophyceae) in corals was determined based on the 23S rRNA gene sequences.