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BackgroundEchinoderms play crucial roles in coral reef ecosystems, where they are significant detritivores and herbivores. The phylum is widely known for its boom and bust cycles, driven by food availability, predation pressure and mass mortalities. Hence, surveillance of potential pathogens and associates of grossly normal specimens is important to understanding their roles in ecology and mass mortality. MethodsWe performed viral surveillance in two common coral reef echinoderms,Diadema antillarumandHolothuria floridana, using metagenomics. Urchin specimens were obtained during the 2022Diadema antillarumscuticociliatosis mass mortality event from the Caribbean and grossly normalH. floridanaspecimens from a reef in Florida. Viral metagenomes were assembled and aligned against viral genomes and protein encoding regions. Metagenomic reads and previously sequenced transcriptomes were further investigated for putative viral elements by Kraken2. ResultsD. antillarumwas devoid of viruses typically seen in echinoderms, butH. floridanayielded viral taxa similar to those found in other sea cucumbers, includingPisoniviricetes(Picornaviruses),Ellioviricetes(Bunyaviruses), andMagsaviricetes(Nodaviruses). The lack of viruses detected inD. antillarummay be due to the large amount of host DNA in viral metagenomes, or because viruses are less abundant inD. antillarumtissues when compared toH. floridanatissues. Our results also suggest that RNA amplification approach may influence viral representation in viral metagenomes. While our survey was successful in describing viruses associated with both echinoderms, our results indicate that viruses are less pronounced inD. antillarumthan in other echinoderms. These results are important in context of wider investigation on the association between viruses andD. antillarummass mortalities, since the conventional method used in this study was unsuccessful. 

Abstract Mass mortality of the dominant coral reef herbivore Diadema antillarum in the Caribbean in the early 1980s contributed to a persistent phase shift from coral- to algal-dominated reefs. In 2022, a scuticociliate most closely related to Philaster apodigitiformis caused further mass mortality of D. antillarum across the Caribbean, leading to >95% mortality at affected sites. Mortality was also reported in the related species Diadema setosum in the Mediterranean in 2022, though the causative agent of the Mediterranean outbreak has not yet been determined. In April 2023, mass mortality of Diadema setosum occurred along the Sultanate of Oman's coastline. Urchins displayed signs compatible with scuticociliatosis including abnormal behavior, drooping and loss of spines, followed by tissue necrosis and death. Here we report the detection of an 18S rRNA gene sequence in abnormal urchins from Muscat, Oman, that is identical to the Philaster strain responsible for D. antillarum mass mortality in the Caribbean. We also show that scuticociliatosis signs can be elicited in Diadema setosum by experimental challenge with the cultivated Philaster strain associated with Caribbean scuticociliatosis. These results demonstrate the Philaster sp. associated with D. antillarum mass mortality has rapidly spread to geographically distant coral reefs, compelling global-scale awareness and monitoring for this devastating condition through field surveys, microscopy, and molecular microbiological approaches, and prompting investigation of long-range transmission mechanisms. 

Flaviviruses cause some of the most detrimental vertebrate diseases, yet little is known of their impacts on invertebrates. Microbial activities at the animal-water interface are hypothesized to influence viral replication and possibly contribute to pathology of echinoderm wasting diseases due to hypoxic stress. We assessed the impacts of enhanced microbial production and suboxic stress onApostichopus californicusassociated flavivirus (PcaFV) load in a mesocosm experiment. Organic matter amendment and suboxic stress resulted in lower PcaFV load, which also correlated negatively with animal mass loss and microbial activity at the animal-water interface. These data suggest that PcaFV replication and persistence was best supported in healthier specimens. Our results do not support the hypothesis that suboxic stress or microbial activity promote PcaFV replication, but rather that PcaFV appears to be a neutral or beneficial symbiont ofApostichopus californicus. 

A scuticociliate ( Philaster sp.) causes mass mortality of the long-spined sea urchin Diadema antillarum .