Integration of microscopy and multi-omics data reveals pathology of a coral disease outbreak

Background Marine disease outbreaks are increasing in frequency and severity, threatening coral reef function and persistence. Coral diseases are often difficult to distinguish due to similar gross pathology and frequently unresolved etiologies. Integrating diverse data types (e.g., morphology, molecular, and microbial) may clarify disease etiology, yet few marine studies have integrated them. In August 2022, a multi-species coral disease outbreak with pathology consistent with white syndromes (stony coral tissue loss disease and white plague) occurred at the Flower Garden Banks (northwest Gulf of Mexico). To characterize this disease, we combined microscopy (histopathology and transmission electron microscopy) with multi-omics approaches (comparative metatranscriptomics; 16S rRNA gene sequencing, and Symbiodiniaceae ITS-2 sequencing) to 15 apparently healthy and diseased Pseudodiploria strigosa corals collected during the initial outbreak. Results Analysis revealed signatures of pathology, including coral-Symbiodiniaceae dysbiosis characterized by shrunken Symbiodiniaceae cells and vacuoles, coral and Symbiodiniaceae gene expression indicative of immune stress, and the presence of putative viral structures. Integrating these data types provided a more comprehensive view of disease dynamics within the coral holobiont by linking histopathological changes with molecular signatures of immune response, nutrient deficiency, coral-Symbiodiniaceae dysbiosis, and enrichment of a viral operational taxonomic unit (Order Orthopolintovirales). Conclusions Combined evidence from morphology, reef monitoring, pathology, and comparison with stony coral tissue loss disease identified the outbreak as white plague. We present the first descriptions of white plague in P. strigosa across multiple data types. This study provides an integrative framework for characterizing marine diseases across cellular, sub-cellular, microbial, viral, and transcriptomic scales.