Lipid stores reveal the state of the coral-algae symbiosis at the single-cell level

Abstract

Coral reefs worldwide are threatened by environmental stress. The observable decline in coral cover, is principally due to the intensifying breakdown of the coral symbiosis, a process known as ‘bleaching’. Overproduction of reactive oxygen species (ROS) is considered a key driver of coral bleaching, where environmental stress leads to increased ROS expression. To explore the link between ROS damage and symbiont status, we measured lipid peroxidation (LPO), a ubiquitous form of ROS damage, in the lipid stores of individual endo- and ex-symbiotic algal cells of three coral species, using confocal microscopy and a lipid hydroperoxide sensitive fluorescent dye. We found LPO was higher in endosymbionts, while lipid volume was greater in ex-symbiotic cells. Cluster analysis revealed three metabolic profiles differentiating endosymbiotic (#1: high LPO, low lipid) and ex-symbiotic cells (#3: low LPO, high lipid), with the intermediate group (#2) containing both cell types. Heat stress caused endosymbionts of Pocillopora acuta to shift away from cluster #1, suggesting this cluster represents cells in healthy/stable symbiosis. Our study delivers a new means to assess the coral symbiosis, demonstrating that symbiont LPO ratio combined with lipid store volume is a robust metabolic marker for the state of the symbiosis at the cellular level.

Diversity of lipid profiles of Symbiodiniaceae under temperature and nutrient stress

“…OxPI and other oxidized phospholipids have not been well explored in algae but could indicate increases in ROS and oxidative stress due to temperature increase. ROS have been shown to leak from Symbiodiniaceae cells, implying that when in hospite would transfer to the coral host (Nielsen and Petrou, 2023), and corals are known to bleach under increased oxidative stress (Lesser, 1997). Therefore, it is possible that increases in relative abundances of OxPI as a result of temperature stress could potentially disrupt signaling between Symbiodiniaceae and coral host when in hospite and contribute to the breakdown of the symbiosis.…”

“…For example, nutrient limitation, alterations to the N:P ratio, and temperature extremes are known to disrupt the stability of some coral-Symbiodiniaceae symbioses, ultimately increasing susceptibility to coral bleaching and mortality (Ezzat et al, 2016;Rosset et al, 2017;Blanckaert et al, 2023). As nutrient concentrations and temperature can affect microalgae lipid composition (Holm et al, 2022;Gao et al, 2023), the plasticity of Symbiodiniaceae lipid composition, and thus what is translocated to the coral hosts, could determine the susceptibility of coral-Symbiodiniaceae associations to climate change and potential for the poleward range shifts of corals (Nielsen and Petrou, 2023).…”

Lipid Droplets in Endosymbiotic Symbiodiniaceae spp. Associated with Corals

“…Over a decade, lipid droplets in Symbiodiniaceae species have been observed that received wide attention from marine biologists [41]. It was reported that the lipid droplets were initially identified through ultramicroscopy, which demonstrated that the lipid droplets are mostly distributed within the cells of endosymbiotic Symbiodiniaceae species [35].…”

Genomic insights into photosymbiotic evolution inTridacna squamosa

“…In agreement with this, three members of SLC5 (solute carrier family 5) subfamily transporting glucose 38 and three members of SCL16 subfamily transporting lactate/pyruvate 39 were found to be predominantly expressed in the symbiotic mantle. Lipids could be further produced in the symbiont through utilization of inorganic carbon and carbohydrates in photosynthesis, which have recently been proven to be another main carrier of carbon translocation in the dynamic symbiotic relationship 40,41 . In this study, genomic and transcriptomic analyses revealed an active APOD-dependent LDLR lipid transport pathway in the symbiotic mantle (Figure 3A), implicating lipids as a key molecular class in carbon translocation supporting the giant clam-dinoflagellate association.…”