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Seagrasses are marine angiosperms that form highly productive and diverse ecosystems. These ecosystems, however, are declining worldwide. Plant-associated microbes affect critical functions like nutrient uptake and pathogen resistance, which has led to an interest in the seagrass microbiome. However, despite their significant role in plant ecology, viruses have only recently garnered attention in seagrass species. In this study, we produced original data and mined publicly available transcriptomes to advance our understanding of RNA viral diversity inZostera marina,Zostera muelleri,Zostera japonica, andCymodocea nodosa. InZ.marina, we present evidence for additional Zostera marina amalgavirus 1 and 2 genotypes, and a complete genome for an alphaendornavirus previously evidenced by an RNA-dependent RNA polymerase gene fragment. InZ.muelleri, we present evidence for a second complete alphaendornavirus and near complete furovirus. Both are novel, and, to the best of our knowledge, this marks the first report of a furovirus infection naturally occurring outside of cereal grasses. InZ.japonica, we discovered genome fragments that belong to a novel strain of cucumber mosaic virus, a prolific pathogen that depends largely on aphid vectoring for host-to-host transmission. Lastly, inC.nodosa, we discovered two contigs that belong to a novel virus in the familyBetaflexiviridae. These findings expand our knowledge of viral diversity in seagrasses and provide insight into seagrass viral ecology. 

Marine invertebrate mass mortality events (MMEs) threaten biodiversity and have the potential to catastrophically alter ecosystem structure. A proximal question around acute MMEs is their etiologies and/or environmental drivers. Establishing a robust cause of mortality is challenging in marine habitats due to the complexity of the interactions among species and the free dispersal of microorganisms from surrounding waters to metazoan microbiomes. The 2013–2014 sea star wasting disease (SSWD) MME in the northeast Pacific Ocean highlights the difficulty in establishing responsible agents. In less than a year of scientific investigation, investigators identified a candidate agent and provided at the time convincing data of pathogenic and transmissible disease. However, later investigation failed to support the initial results, and critical retrospective analyses of experimental procedures and reinterpretation of early findings disbanded any candidate agent. Despite the circuitous path that the investigation and understanding of SSWD have taken, lessons learned from the initial investigation—improving on approaches that led to misinterpretation—have been successfully applied to the 2022Diadema antillaruminvestigation. In this review, we outline the history of the initial SSWD investigation, examine how early exploration led to spurious interpretations, summarize the lessons learned, provide recommendations for future work in other systems, and examine potential links between the SSWD event and theDiadema antillarumMME. 

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. 

Sea star wasting disease (SSWD) refers to a suite of gross pathological signs observed in Asteroidea species. It presents to varying degrees as abnormal posture, epidermal ulceration, arm autotomy and eversion of viscera. We report observations of SSWD in the sunstar Crossaster papposus, the first observations of its kind in Europe. While the exact cause of SSWD remains unknown, studies have proposed pathogenic and environmental-stress pathways for disease outbreaks. Although the present observations do not support a precise aetiology, the presence of SSWD in a keystone predator may have wide reaching ecological and management implications. 

Echinoderms are a phylum of marine invertebrates that include model organisms, keystone species, and animals commercially harvested for seafood. Despite their scientific, ecological, and economic importance, there is little known about the diversity of RNA viruses that infect echinoderms compared to other invertebrates. We screened over 900 transcriptomes and viral metagenomes to characterize the RNA virome of 38 echinoderm species from all five classes (Crinoidea, Holothuroidea, Asteroidea, Ophiuroidea and Echinoidea). We identified 347 viral genome fragments that were classified to genera and families within nine viral orders - Picornavirales, Durnavirales, Martellivirales, Nodamuvirales, Reovirales, Amarillovirales, Ghabrivirales, Mononegavirales, and Hepelivirales . We compared the relative viral representation across three life stages (embryo, larvae, adult) and characterized the gene content of contigs which encoded complete or near-complete genomes. The proportion of viral reads in a given transcriptome was not found to significantly differ between life stages though the majority of viral contigs were discovered from transcriptomes of adult tissue. This study illuminates the biodiversity of RNA viruses from echinoderms, revealing the occurrence of viral groups in natural populations. 

Sea star wasting disease (SSWD) is a condition that has affected asteroids for over 120 years, yet mechanistic understanding of this wasting etiology remains elusive. We investigated temporal virome variation in two Pisaster ochraceus specimens that wasted in the absence of external stimuli and two specimens that did not experience SSWD for the duration of our study, and compared viromes of wasting lesion margin tissues to both artificial scar margins and grossly normal tissues over time. Global assembly of all SSWD-affected tissue libraries resulted in 24 viral genome fragments represented in >1 library. Genome fragments mostly matched densoviruses and picornaviruses with fewer matching nodaviruses, and a sobemovirus. Picornavirus-like and densovirus-like genome fragments were most similar to viral genomes recovered in metagenomic study of other marine invertebrates. Read recruitment revealed only two picornavirus-like genome fragments that recruited from only SSWD-affected specimens, but neither was unique to wasting lesions. Wasting lesion margin reads recruited to a greater number of viral genotypes (i.e., richness) than did either scar tissue and grossly normal tissue reads. Taken together, these data suggest that no single viral genome fragment was associated with SSWD. Rather, wasting lesion margins may generally support viral proliferation.