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

Abstract

Increasing global temperatures due to climate change have resulted in respective increases in the severity and frequency of epizootics around the globe. Corals in particular have faced rapid declines due to disease outbreaks. Understanding immune responses and associated potential life-history trade-offs is therefore a priority. In the autumn of 2011, a novel disease of octocorals of the genus Eunicea was first documented in the Florida Keys. Termed Eunicea Black Disease (EBD), the disease is easily identified by the dark appearance of affected tissue, caused by a strong melanization response on the part of the host. In order to better understand the response of corals to EBD, we conducted full transcriptome analysis of 3 healthy and 3 diseased specimens of Eunicea calyculata collected from offshore southeast Florida. Differential expression and protein analyses revealed a strong, diverse immune response to EBD characterized by phagocytosis, adhesion and melanization on the part of the host. Furthermore, coexpression network analyses suggested this might come at the cost of reduced cell cycle progression and growth. This is in accordance with past histological studies of naturally infected hard corals, suggesting that potential trade-offs during infection may affect post-outbreak recovery of reef ecosystems by reducing both organismal growth and fecundity. Our findings highlight the importance of considering factors beyond mortality when estimating effects of disease outbreaks on ecosystems.

Differential gene expression analysis of symbiotic and aposymbiotic Exaiptasia anemones under immune challenge with Vibrio coralliilyticus

“…Initial characterizations of cnidarian immune genes indicated that they possess key components of the major innate immune pathways including Toll/TLR pathway, complement C3, membrane attack complex/perforin domains, and other components of innate immunity once thought to have evolved much later (Miller et al, ; Nyholm & Graf, ; Putnam et al, ; Shinzato et al, ); yet, it was not known whether cnidarians used these immune pathways to mount a response against pathogens. A number of groups have since used RNA‐Seq data to produce some of the first profiles of anthozoan innate immunity (Anderson, Walz, Weil, Tonellato, & Smith, ; Burg, Prentis, Surm, & Pavasovic, ; Fuess, Mann, Jinks, Brinkhuis, & Mydlarz, ; Fuess, Pinzón, Weil, Grinshpon, & Mydlarz, ; Libro, Kaluziak, & Vollmer, ; Libro & Vollmer, ; Pinzón et al, ; Poole & Weis, ; Vidal‐Dupiol et al, ; Weiss et al, ). To date, at least nine studies have profiled the immune response of corals and their anthozoan relatives, and the data suggest that the immune response varies across anthozoans and/or immune exposures.…”

Caspases from Scleractinian Coral Show Unique Regulatory Features

“…Where O. faveolata is sensitive to disease and activates apoptotic responses to stress, P. astreoides is resistant to disease and activates autophagic responses to stress. Thus, the two stony coral represent intriguing systems to characterize the biochemical responses to stress (18).…”

“…Coral possess a rudimentary immune system that consists of innate immune pathways but no adaptive immune system (16). The invertebrate innate immune system is similar to that of vertebrates in utilizing physical and chemical barriers, cellular defenses, and humoral responses to pathogens (17), but in the relatively new field of ecological immunity, major knowledge gaps remain regarding the cellular defenses to disease (18). Although general response types have been outlined regarding receptor recognition, signaling pathways, and effector responses, such as metabolic changes, very few functional studies have been performed on the responses of coral to disease stressors (19).…”

“…Caspase-3-like activity was detected in the stony coral Pocillopora damicornis when exposed to heat-stress and high levels of ammonium (25), and caspase inhibitors have been shown to prevent the death of bleached coral (9). Recently, Fuess and colleagues showed an increase in expression of apoptosis-related genes, among others, in Caribbean coral with Eunicea Black Disease, which results in a heavily melanized appearance of gorgonian corals (18), but the response has not been elucidated in functional or biochemical studies. Collectively, the data show the potential for complex apoptotic signaling pathways in coral, but data on activation and control mechanisms, and how they compare to those in vertebrates, are lacking due to a dearth of biochemical characterization.…”

Innate immune gene expression inAcropora palmatais consistent despite variance in yearly disease events

“…Cell adhesion is important to maintaining the integrity of the tissue layer and within corals, evidence has been presented that factors, including heat stress and disease, can cause upregulation of genes involved in cell adhesion pathways [20,60–63]. Interestingly, in previous coral disease studies, cell adhesion enrichment was present in corals that were showing signs of disease pathology and hypothesized to be due to the importance of apoptotic processes and phagocytosis of melanized particles and pathogens [20, 21]. Our findings show that cell adhesion is also important in corals not exhibiting visual signs of disease.…”