Stony coral tissue loss disease induces transcriptional signatures of in situ degradation of dysfunctional Symbiodiniaceae.

Stony coral tissue loss disease (SCTLD), one of the most pervasive and virulent coral diseases on record, affects over 22 species of reef-building coral and is decimating reefs throughout the Caribbean. To understand how different coral species and their algal symbionts (family Symbiodiniaceae) respond to this disease, we examine the gene expression profiles of colonies of five species of coral from a SCTLD transmission experiment. The included species vary in their purported susceptibilities to SCTLD, and we use this to inform gene expression analyses of both the coral animal and their Symbiodiniaceae. We identify orthologous coral genes exhibiting lineage-specific differences in expression that correlate to disease susceptibility, as well as genes that are differentially expressed in all coral species in response to SCTLD infection. We find that SCTLD infection induces increased expression of rab7, an established marker of in situ degradation of dysfunctional Symbiodiniaceae, in all coral species accompanied by genus-level shifts in Symbiodiniaceae photosystem and metabolism gene expression. Overall, our results indicate that SCTLD infection induces symbiophagy across coral species and that the severity of disease is influenced by Symbiodiniaceae identity.

Analysis of Spatial Gene Expression at the Cellular Level in Stony Corals.

Scleractinians, or stony corals, are colonial animals that possess a high regenerative capacity and a highly diverse innate immune system. As such they present the opportunity to investigate the interconnection between regeneration and immunity in a colonial animal. Understanding the relationship between regeneration and immunity in stony corals is of further interest as it has major implications for coral reef health. One method for understanding the role of innate immunity in scleractinian regeneration is in situ hybridization using RNA probes. Here we describe a protocol for in situ hybridization in adult stony corals using a digoxigenin (DIG)-labeled RNA antisense probe which can be utilized to investigate the spatial expression of immune factors during regeneration.

Adaptive variation in homologue number within transcript families promotes expression divergence in reef-building coral.

Gene expression, especially in multispecies experiments, is used to gain insight into the genetic basis of how organisms adapt and respond to changing environments. However, evolutionary processes that can influence gene expression patterns between species such as the presence of paralogues which arise from gene duplication events are rarely accounted for. Paralogous transcripts can alter the transcriptional output of a gene, and thus exclusion of these transcripts can obscure important biological differences between species. To address this issue, we investigated how differences in transcript family size are associated with divergent gene expression patterns in five species of Caribbean reef-building corals. We demonstrate that transcript families that are rapidly evolving in terms of size have increased levels of expression divergence. Additionally, these rapidly evolving transcript families are enriched for multiple biological processes, with genes involved in the coral innate immune system demonstrating pronounced variation in homologue number between species. Overall, this investigation demonstrates the importance of incorporating paralogous transcripts when comparing gene expression across species by influencing both transcriptional output and the number of transcripts within biological processes. As this investigation was based on transcriptome assemblies, additional insights into the relationship between gene duplications and expression patterns will probably emergence once more genome assemblies are available for study.

Cnidarian Pattern Recognition Receptor Repertoires Reflect Both Phylogeny and Life History Traits.

Pattern recognition receptors (PRRs) are evolutionarily ancient and crucial components of innate immunity, recognizing danger-associated molecular patterns (DAMPs) and activating host defenses. Basal non-bilaterian animals such as cnidarians must rely solely on innate immunity to defend themselves from pathogens. By investigating cnidarian PRR repertoires we can gain insight into the evolution of innate immunity in these basal animals. Here we utilize the increasing amount of available genomic resources within Cnidaria to survey the PRR repertoires and downstream immune pathway completeness within 15 cnidarian species spanning two major cnidarian clades, Anthozoa and Medusozoa. Overall, we find that anthozoans possess prototypical PRRs, while medusozoans appear to lack these immune proteins. Additionally, anthozoans consistently had higher numbers of PRRs across all four classes relative to medusozoans, a trend largely driven by expansions in NOD-like receptors and C-type lectins. Symbiotic, sessile, and colonial cnidarians also have expanded PRR repertoires relative to their non-symbiotic, mobile, and solitary counterparts. Interestingly, cnidarians seem to lack key components of mammalian innate immune pathways, though similar to PRR numbers, anthozoans possess more complete immune pathways than medusozoans. Together, our data indicate that anthozoans have greater immune specificity than medusozoans, which we hypothesize to be due to life history traits common within Anthozoa. Overall, this investigation reveals important insights into the evolution of innate immune proteins within these basal animals.