Heat stress drives rapid viral and antiviral innate immunity activation in Hexacorallia

Abstract

The cnidarian class Hexacorallia, encompassing stony corals and sea anemones, plays a critical role in marine ecosystems. Coral bleaching, the disruption of the symbiosis between stony corals and zooxanthellate algae, is driven by climate change-induced seawater warming and further exacerbated by pathogenic microbes. However, how pathogens, especially viruses, contribute to accelerated bleaching remains poorly understood. The present study utilizes the model sea anemone Nematostella vectensis to explore these dynamics by creating a transgenic line with a reporter gene regulated by sequences from two RIG-I-like receptor (RLR) genes involved in antiviral responses. Under heat stress, the reporter gene showed significant upregulation, indicating that these regulatory sequences are indeed responsive to thermal stress. Analyses of transcriptome data of N. vectensis, Exaiptasia diaphana (another sea anemone), and the stony coral Stylophora pistillata revealed stress-induced activation of a set of bona fide immune-related genes conserved between the three species. Population-specific differences in stress-induced transcriptional responses of immune-related genes were evident in both Nematostella and Stylophora, depending on geographic origin. In Exaiptasia, the presence or absence of zooxanthellae also influenced stress-induced immune gene expression. To test whether the viruses themselves may contribute to this immune response under stress, we subjected Nematostella polyps to variable periods of heat stress and measured the transcript levels of resident viruses as well as selected antiviral genes. While the antiviral genes responded within 1-3 hours of heat stress, viral gene expression was already upregulated within 30 minutes, suggesting that their increase might be contributing to the elevated immune response under stress, and consequentially, the further demise of organismal homeostasis. These findings highlight the complex interplay between environmental stress, viruses, immune responses, and symbiotic states in Hexacorallia. Better understanding of these mechanisms could provide insights into the role of immune pathways in coral resilience and bleaching in a changing climate.