Building consensus around the assessment and interpretation of Symbiodiniaceae diversity

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.journal articl

Building consensus around the assessment and interpretation of Symbiodiniaceae diversity

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships

Investigating the roles of transforming growth factor-beta in immune response of Orbicella faveolata, a scleractinian coral

Symbiotic relationships range from parasitic to mutualistic, yet all endosymbionts face similar challenges, including evasion of host immunity. Many symbiotic organisms have evolved similar mechanisms to face these challenges, including manipulation of the host's transforming growth factor-beta (TGFβ) pathway. Here we investigate the TGFβ pathway in scelaractinian corals which are dependent on symbioses with dinoflagellates from the family Symbiodiniaceae. Using the Caribbean coral, Orbicella faveolata, we explore the effects of enhancement and inhibition of the TGFβ pathway on host gene expression. Following transcriptomic analyses, we demonstrated limited effects of pathway manipulation in absence of immune stimulation. However, manipulation of the TGFβ pathway significantly affects the subsequent ability of host corals to mount an immune response. Enhancement of the TGFβ pathway eliminates transcriptomic signatures of host coral immune response, while inhibition of the pathway maintains the response. This is, to our knowledge, the first evidence of an immunomodulatory role for TGFβ in a scelaractinian coral. These findings suggest variation in TGFβ signaling may have implications in the face of increasing disease prevelance. Our results suggest that the TGFβ pathway can modulate tradeoffs between symbiosis and immunity. Further study of links between symbiosis, TGFβ, and immunity is needed to better understand the ecological implications of these findings

Associations between transcriptional changes and protein phenotypes provide insights into immune regulation in corals

Disease outbreaks in marine ecosystems have driven worldwide declines of numerous taxa, including corals. Some corals, such as Orbicella faveolata, are particularly susceptible to disease. To explore the mechanisms contributing to susceptibility, colonies of O. faveolata were exposed to immune challenge with lipopolysaccharides. RNA sequencing and protein activity assays were used to characterize the response of corals to immune challenge. Differential expression analyses identified 17 immune-related transcripts that varied in expression post-immune challenge. Network analyses revealed several groups of transcripts correlated to immune protein activity. Several transcripts, which were annotated as positive regulators of immunity were included in these groups, and some were downregulated following immune challenge. Correlations between expression of these transcripts and protein activity results further supported the role of these transcripts in positive regulation of immunity. The observed pattern of gene expression and protein activity may elucidate the processes contributing to the disease susceptibility of species like O. faveolata

Variation in symbiont density is linked to changes in constitutive immunity in the facultatively symbiotic coral, Astrangia poculata

Scleractinian corals are essential ecosystem engineers, forming the basis of coral reef ecosystems. However, these organisms are in decline globally, in part due to rising disease prevalence. Most corals are dependent on symbiotic interactions with single-celled algae from the family Symbiodiniaceae to meet their nutritional needs, however, suppression of host immunity may be essential to this relationship. To explore immunological consequences of algal symbioses in scleractinian corals, we investigated constitutive immune activity in the facultatively symbiotic coral, Astrangia poculata. We compared immune metrics (melanin synthesis, antioxidant production and antibacterial activity) between coral colonies of varying symbiont density. Symbiont density was positively correlated to both antioxidant activity and melanin concentration, likely as a result of the dual roles of these pathways in immunity and symbiosis regulation. Our results confirm the complex nature of relationships between algal symbiosis and host immunity and highlight the need for nuanced approaches when considering these relationships

Step2_GoMWU

This zip folder contains the gene_ids and the module membership scores for the identified O. faveolata UPRmt genes, as well as the GO terms for those genes

Increased Algal Symbiont Density Reduces Host Immunity in a Threatened Caribbean Coral Species, Orbicella faveolata

Scleractinian corals are the principal builders of coral reefs. These megadiverse ecosystems are declining due to coral mortality from a variety of stressors, including disease. Corals are dependent upon symbiotic dinoflagellates in the family Symbiodiniaceae for phototrophic contributions to their energy budgets. However, suppression of host immunity may be necessary to maintain these intracellular symbioses. To explore the consequences of symbiosis on host immunity, we manipulated symbiont density by increasing nitrogen availability. Replicate cores from four colonies of the Caribbean coral, Orbicella faveolata, were reared in seawater treated with ammonium for 1 month to increase symbiont density. Corals were then immune-stimulated using lipopolysaccharide and poly I:C. Gene expression was analyzed using RNAseq and symbiont density was quantified (as symbiont:host cell ratio) using quantitative PCR (qPCR). Ammonium treatment had limited positive effects on host immunity. In contrast, increases in symbiont density had large negative effects on host expression of immune-related transcripts. These results suggest links between nutrient enrichment and coral disease may be the result of the effect of increased symbiont density on host immunity, rather than the direct effect of the nutrients. Further study of the trade-offs between symbiont density and immunity may help understand how decreasing water quality and increasing disease will shape future reef communities

Supplementary Figure 1 from Transcriptional analyses provide new insight into the late-stage immune response of a diseased Caribbean coral

Results of principle component analysis of patterns of differential expression in all six samples conducted in the R package CummeRbund

Supplementary File 1 from Transcriptional analyses provide new insight into the late-stage immune response of a diseased Caribbean coral

Summary of all differentially expressed contigs and list of differentially expressed contigs identified as part of the immune response

Supplementary File 2 from Transcriptional analyses provide new insight into the late-stage immune response of a diseased Caribbean coral

Results of the WGCNA coexpression analysis listing each contig's annotation, module classification, and module membership