Thermal plasticity of coral reef symbionts is linked to major alterations in their lipidome composition

Abstract

Coral bleaching caused by ocean warming is leading to worldwide coral decline. The physiological processes underlying this ecological event are still incompletely understood, although previous research has suggested oxidative stress as major player in the impairment of symbiont thylakoid membranes and in symbiosis breakdown. Lipids are interesting targets of investigation, given their susceptibility to thermal and oxidative stresses. Here, an untargeted lipidomic approach was employed to examine changes in lipidome and pigments of three coral reef symbionts (Symbiodiniaceae) after a heat shock in in vitro experiments. The acute thermal stress induced species-specific changes in lipidome and pigments compositions of both heat sensitive and tolerant symbionts. Heat sensitivity was characterized by a steep and steady decline in cell densities over time (4 and 240 h after heat shock). At the membrane level, heat sensitive symbiont displayed a quantitative decrease in glycolipids linked to polyunsaturated fatty acids, followed by enrichment in oxidized lipids and sphingolipids. Despite showing distinct adaptations, the two heat tolerant symbionts were characterized by the preservation of membrane lipids after heat shock, particularly glycolipids. This finding suggests the action of powerful antioxidant systems, preventing the escalation of oxidized lipids concentration in thylakoid membranes under thermal stress. Although limited by the examination of free-living symbionts, our study provides a solid baseline for the investigation of lipidome and pigments alterations of Symbiodiniaceae in response to heat stress. Novel potential lipid biomarkers linked to thermal stress are suggested. In particular, oxidized lipids-which are implicated in coral symbiosis establishment and breakdown-appear as attractive targets for further research.

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

“…However, PC 22:6/22:6 was detected only in the symbiotic corals S. caliendrum, M. platyphylla , and M. dichotoma . Earlier, this PC was found in cultured symbiotic dinoflagellates [ 56 ]. Thus, the source of PC 22:6/22:6 is coral dinoflagellates.…”

“…Nevertheless, the influence of the coral host can be significant, as evidenced by the cluster analysis in the present study. In addition, the PG and SQDG of some coral species contain odd-numbered FAs [ 49 , 52 , 56 ]. PG is one of the major structural lipids of the bacterial plasma membrane, SQDG is also found in bacteria [ 99 ], and, therefore, these odd-numbered molecular species of PG and SQDG in the lipid extracts of corals can belong to bacteria.…”

“…and M. platyphylla [ 52 ]. In addition, this PG is detected in the lipids of various cultured symbiotic dinoflagellates [ 56 ]. This confirms that the source of the molecular species in the coral is definitely symbiotic dinoflagellates.…”

“…Dinoflagellates from S. flexibilis were characterized by a higher content of PG 16:2/20:2; dinoflagellates from Acropora sp., by higher contents of PG 16:2/20:2, 16:1/19:2, and 16:0/20:1; and dinoflagellates from M. platyphylla , by higher contents of PG 16:1/19:2, 16:1/18:2, 16:0/18:2, and 16:0/18:1. Earlier, the molecular species PG 16:1/19:2 and 16:2/20:2 were detected in the cultured symbiotic dinoflagellate species Symbiodinium microadriaticum (A1) and C. goreaui (C1) [ 56 ].…”

Betaine lipids of Symbiodiniaceae hosted by Indo‐Pacific corals

“…Probably, DGCC 18:0/28:8 and 18:0/28:7 are a separate DGCC pool that performs a special function in coral's symbionts. Previously, the molecular species DGCC 18:0/28:7 has been detected in lipids of A. cerealis (Ermolenko & Sikorskaya 2021), in in hospite endosymbionts of hexacoral Palythoa tuberculosa (Sikorskaya et al 2021) and in cultured coral symbionts Symbiodinium microadriaticum (Botana et al 2022).…”