Baseline dynamics of Symbiodiniaceae genera and photochemical efficiency in corals from reefs with different thermal histories.

Ocean warming and marine heatwaves induced by climate change are impacting coral reefs globally, leading to coral bleaching and mortality. Yet, coral resistance and resilience to warming are not uniform across reef sites and corals can show inter- and intraspecific variability. To understand changes in coral health and to elucidate mechanisms of coral thermal tolerance, baseline data on the dynamics of coral holobiont performance under non-stressed conditions are needed. We monitored the seasonal dynamics of algal symbionts (family Symbiodiniaceae) hosted by corals from a chronically warmed and thermally variable reef compared to a thermally stable reef in southern Taiwan over 15 months. We assessed the genera and photochemical efficiency of Symbiodiniaceae in three coral species: Acropora nana, Pocillopora acuta, and Porites lutea. Both Durusdinium and Cladocopium were present in all coral species at both reef sites across all seasons, but general trends in their detection (based on qPCR cycle) varied between sites and among species. Photochemical efficiency (i.e., maximum quantum yield; Fv/Fm) was relatively similar between reef sites but differed consistently among species; no clear evidence of seasonal trends in Fv/Fm was found. Quantifying natural Symbiodiniaceae dynamics can help facilitate a more comprehensive interpretation of thermal tolerance response as well as plasticity potential of the coral holobiont.

The diversity and ecology of Symbiodiniaceae: A traits-based review.

Among the most successful microeukaryotes to form mutualisms with animals are dinoflagellates in the family Symbiodiniaceae. These photosynthetic symbioses drive significant primary production and are responsible for the formation of coral reef ecosystems but are particularly sensitive when environmental conditions become extreme. Annual episodes of widespread coral bleaching (disassociation of the mutualistic partnership) and mortality are forecasted from the year 2060 under current trends of ocean warming. However, host cnidarians and dinoflagellate symbionts display exceptional genetic and functional diversity, and meaningful predictions of the future that embrace this biological complexity are difficult to make. A recent move to trait-based biology (and an understanding of how traits are shaped by the environment) has been adopted to move past this problem. The aim of this review is to: (1) provide an overview of the major cnidarian lineages that are symbiotic with Symbiodiniaceae; (2) summarise the symbiodiniacean genera associated with cnidarians with reference to recent changes in taxonomy and systematics; (3) examine the knowledge gaps in Symbiodiniaceae life history from a trait-based perspective; (4) review Symbiodiniaceae trait variation along three abiotic gradients (light, nutrients, and temperature); and (5) provide recommendations for future research of Symbiodiniaceae traits. We anticipate that a detailed understanding of traits will further reveal basic knowledge of the evolution and functional diversity of these mutualisms, as well as enhance future efforts to model stability and change in ecosystems dependent on cnidarian-dinoflagellate organisms.

Genomic conservation and putative downstream functionality of the phosphatidylinositol signalling pathway in the cnidarian-dinoflagellate symbiosis.

The mutualistic cnidarian-dinoflagellate symbiosis underpins the evolutionary success of stony corals and the persistence of coral reefs. However, a molecular understanding of the signalling events that lead to the successful establishment and maintenance of this symbiosis remains unresolved. For example, the phosphatidylinositol (PI) signalling pathway has been implicated during the establishment of multiple mutualistic and parasitic interactions across the kingdoms of life, yet its role within the cnidarian-dinoflagellate symbiosis remains unexplored. Here, we aimed to confirm the presence and assess the specific enzymatic composition of the PI signalling pathway across cnidaria and dinoflagellates by compiling 21 symbiotic anthozoan (corals and sea anemones) and 28 symbiotic dinoflagellate (Symbiodiniaceae) transcriptomic and genomic datasets and querying genes related to this pathway. Presence or absence of PI-kinase and PI-phosphatase orthologs were also compared between a broad sampling of taxonomically related symbiotic and non-symbiotic species. Across the symbiotic anthozoans analysed, there was a complete and highly conserved PI pathway, analogous to the pathway found in model eukaryotes. The Symbiodiniaceae pathway showed similarities to its sister taxon, the Apicomplexa, with the absence of PI 4-phosphatases. However, conversely to Apicomplexa, there was also an expansion of homologs present in the PI5-phosphatase and PI5-kinase groups, with unique Symbiodiniaceae proteins identified that are unknown from non-symbiotic unicellular organisms. Additionally, we aimed to unravel the putative functionalities of the PI signalling pathway in this symbiosis by analysing phosphoinositide (PIP)-binding proteins. Analysis of phosphoinositide (PIP)-binding proteins showed that, on average, 2.23 and 1.29% of the total assemblies of anthozoan and Symbiodiniaceae, respectively, have the potential to bind to PIPs. Enrichment of Gene Ontology (GO) terms associated with predicted PIP-binding proteins within each taxon revealed a broad range of functions, including compelling links to processes putatively involved in symbiosis regulation. This analysis establishes a baseline for current understanding of the PI pathway across anthozoans and Symbiodiniaceae, and thus a framework to target future research.

The characteristics of host lipid body biogenesis during coral-dinoflagellate endosymbiosis.

Intracellular lipid body (LB) biogenesis depends on the symbiosis between coral hosts and their Symbiodinaceae. Therefore, understanding the mechanism(s) behind LB biosynthesis in corals can portentially elucide the drivers of cellular regulation during endosymbiosis. This study assessed LB formation in the gastrodermal tissue layer of the hermatypic coral Euphyllia glabrescens. Diel rhythmicity in LB size and distribution was observed; solar irradiation onset at sunrise initiated an increase in LB formation, which continued throughout the day and peaked after sunset at 18:00. The LBs migrated from the area near the mesoglea to the gastrodermal cell border near the coelenteron. Micro-LB biogenesis occurred in the endoplasmic reticulum (ER) of the host gastrodermal cells. A transcriptomic analysis of genes related to lipogenesis indicated that binding immunoglobulin protein (BiP) plays a key role in metabolic signaling pathways. The diel rhythmicity of LB biogenesis was correlated with ER-localized BiP expression. BiP expression peaked during the period with the largest increase in LB formation, thereby indicating that the chaperoning reaction of abnormal protein folding inside the host ER is likely involved in LB biosynthesis. These findings suggest that the host ER, central to LB formation, potentially facilitates the regulation of endosymbiosis between coral hosts and Symbiodiniaceae.

The Molecular Language of the Cnidarian-Dinoflagellate Symbiosis.

The cnidarian-dinoflagellate symbiosis is of huge importance as it underpins the success of coral reefs, yet we know very little about how the host cnidarian and its dinoflagellate endosymbionts communicate with each other to form a functionally integrated unit. Here, we review the current knowledge of interpartner molecular signaling in this symbiosis, with an emphasis on lipids, glycans, reactive species, biogenic volatiles, and noncoding RNA. We draw upon evidence of these compounds from recent omics-based studies of cnidarian-dinoflagellate symbiosis and discuss the signaling roles that they play in other, better-studied symbioses. We then consider how improved knowledge of interpartner signaling might be used to develop solutions to the coral reef crisis by, for example, engineering more thermally resistant corals.