An algal symbiont (Breviolum psygmophilum) responds more strongly to chronic high temperatures than its facultatively symbiotic coral host (Astrangia poculata)

Abstract

Scleractinian corals form the foundation of coral reefs by secreting skeletons of calcium carbonate. Their intracellular algal symbionts (Symbiodiniaceae) translocate a large proportion of photosynthate to the coral host, which is required to maintain high rates of calcification. Global warming is causing dissociation of coral host and algal symbiont, visibly presented as coral bleaching. Despite decades of study, the precise mechanisms of coral bleaching remain unknown. Separating the thermal stress response of the coral from the algal symbiont is key to understanding bleaching in tropical corals. The facultatively symbiotic northern star coral, Astrangia poculata, naturally occurs as both symbiotic and aposymbiotic (lacking algal symbionts) polyps - sometimes on the same coral colony. Thus, it is possible to separate the heat stress response of the coral host alone from the coral in symbiosis with its symbiont Breviolum psygmophilum. Using replicate symbiotic and aposymbiotic ramets of A. poculata, we conducted a chronic heat stress experiment to increase our understanding of the cellular mechanisms resulting in coral bleaching. Sustained high temperature stress resulted in photosynthetic dysfunction in B. psygmophilum, including a decline in maximum photosynthesis rate, maximum photochemical efficiency, and the absorbance peak of chlorophyll a. Interestingly, the metabolic rates of symbiotic and aposymbiotic corals were differentially impacted. RNAseq analysis revealed more differentially expressed genes between heat-stressed and control aposymbiotic colonies than heat-stressed and control symbiotic colonies. Notably, aposymbiotic colonies increased the expression of inflammation-associated genes such as nitric oxide synthases. Unexpectedly, the largest transcriptional response was observed between heat-stressed and control B. psygmophilum, including genes involved in photosynthesis, response to oxidative stress, and meiosis. Thus, it appears that the algal symbiont suppresses the immune response of the host, potentially increasing the vulnerability of the host to pathogens. The A. poculata-B. psygmophilum symbiosis provides a tractable model system for investigating thermal stress and immune challenge in scleractinian corals.

Algal symbioses with fire corals demonstrate host genotype specificity and niche adaptation at subspecies resolution

“…The strong host genotype fidelity observed is consistent with previous reports showing that host identity largely determines the physiological response of the symbiont, as well as the stability and functionality of the symbiosis to changing environmental conditions 35,49 . Notably, variations in the physiological response to increased temperature within a single Symbiodiniaceae species or clonal host-symbiont combinations have been previously described in temperate corals 16 and Aiptasia 49 , but are rare for tropical corals 50 .…”

“…Algal identity is an important factor contributing to variability of stress tolerance in corals [9][10][11][12] . This variability is likely in part due to the considerable genetic and phenotypic diversity found within each of the most common coral-associating algal genera (Symbiodinium, Breviolum, Cladocopium, and Durusdinium 13 ) characterized by their own physiological and ecological traits 2, [14][15][16] . Such phenotypic diversity means that certain assemblages are better suited for specific prevailing environments than others, as evidenced by the observed environmental structuring of coral-algal associations [17][18][19][20] .…”

Genomic comparison of the temperate coralAstrangia poculatawith tropical corals yields insights into winter quiescence, innate immunity, and sexual reproduction

“…Astrangia poculata has increasingly been used as a model coral system due to its temperature tolerance and flexibility in symbiont state (Aichelman et al, 2019; Burmester et al 2017; Burmester et al 2018; Chan et al, 2021; Dimond & Carrington, 2007; Jacques et al, 1983; Peters, 1988; Sharp et al, 2017; DiRoberts et al 2021; Wuitchik et al, 2021). Because A. poculata is facultatively symbiotic, the host and the algal symbiont response to manipulation can be distinguished—a study design that is often impossible in adult tropical corals, many of whom do not occur naturally in an aposymbiotic state.…”

“…RNA sequencing data from Chan et al (2021) were used to construct a de novo transcriptome. First, to limit the potential for symbiont contamination, only reads for aposymbiotic individuals were used for the host transcriptome assembly.…”

“…Burmester et al (2017) found that symbiotic colonies significantly outperformed aposymbiotic colonies at 9, 18, and 24°C with respect to wound healing, while Wuitchik et al (2021) found that aposymbiotic colonies responded more strongly transcriptionally to a cold exposure than to a heat exposure treatment. In a separate thermal stress experiment, the algal endosymbiont Breviolum psygmophilum responded more strongly than the A. poculata host to chronic heat stress (Chan et al, 2021). Further, season, rather than symbiont state, was shown to drive the structure of the microbiome in A. poculata (Sharp, Pratte, Kerwin, Rotjan, & Stewart, 2017).…”