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In 2014, Stony Coral Tissue Loss Disease (SCTLD) was first detected off the coast of Miami, FL, United States, and continues to persist and spread along the Florida Reef Tractr (FRT) and into the Caribbean. SCTLD can have up to a 61% prevalence in reefs and has affected at least 23 species of scleractinian corals. This has contributed to the regional near-extinction of at least one coral species, Dendrogyra cylindrus. Initial studies of SCTLD indicate microbial community shifts and cessation of lesion progression in response to antibiotics on some colonies. However, the etiology and abiotic sources of SCTLD transmission are unknown. To characterize SCTLD microbial signatures, we collected tissue samples from four affected coral species: Stephanocoenia intersepta, Diploria labyrinthiformis, Dichocoenia stokesii, and Meandrina meandrites. Tissue samples were from apparently healthy (AH) corals, and unaffected tissue (DU) and lesion tissue (DL) on diseased corals. Samples were collected in June 2018 from three zones: (1) vulnerable (ahead of the SCTLD disease boundary in the Lower Florida Keys), (2) endemic (post-outbreak in the Upper Florida Keys), and (3) epidemic (SCTLD was active and prevalent in the Middle Florida Keys). From each zone, sediment and water samples were also collected to identify whether they may serve as potential sources of transmission for SCTLD-associated microbes. We used 16S rRNA gene amplicon high-throughput sequencing methods to characterize the microbiomes of the coral, water, and sediment samples. We identified a relatively higher abundance of the bacteria orders Rhodobacterales and Rhizobiales in DL tissue compared to AH and DU tissue. Also, our results showed relatively higher abundances of Rhodobacterales in water from the endemic and epidemic zones compared to the vulnerable zone. Rhodobacterales and Rhizobiales identified at higher relative abundances in DL samples were also detected in sediment samples, but not in water samples. Our data indicate that Rhodobacterales and Rhizobiales may play a role in SCTLD and that sediment may be a source of transmission for Rhodobacterales and Rhizobiales associated with SCTLD lesions.

ABSTRACT Panulirus argus virus 1 (PaV1) is the only known virus infecting the Caribbean spiny lobster (Panulirus argus) from the Caribbean Sea. Recently, related viruses, Dikerogammarus haemobaphes virus 1 (DhV1) and Carcinus maenas virus 1 (CmV1), have been detected in the demon shrimp (Dikerogammarus haemobaphes) and the European shore crab (Carcinus maenas), respectively, from sites in the United Kingdom. The virion morphology of these crustacean viruses is similar to that of iridoviruses. However, unlike iridoviruses and other nucleocytoplasmic large DNA viruses (NCLDVs), these viruses complete their morphogenesis in the host cell nucleus rather than in the cytoplasm. To date, these crustacean viruses have remained unclassified due to a lack of genomic data. Using an Illumina MiSeq sequencer, we sequenced the complete genomes of PaV1, CmV1, and DhV1. Comparative genome analysis shows that these crustacean virus genomes encode the 10 hallmark proteins previously described for the NCLDVs of eukaryotes, strongly suggesting that they are members of this group. With a size range of 70 to 74 kb, these are the smallest NCLDV genomes identified to date. Extensive gene loss, divergence of gene sequences, and the accumulation of low-complexity sequences reflect the extreme degradation of the genomes of these “minimal” NCLDVs rather than any direct relationship with the NCLDV ancestor. Phylogenomic analysis supports the classification of these crustacean viruses as a distinct family, “Mininucleoviridae,” within the pitho-irido-Marseille branch of the NCLDVs. IMPORTANCE Recent genomic and metagenomic studies have led to a dramatic expansion of the known diversity of nucleocytoplasmic large DNA viruses (NCLDVs) of eukaryotes, which include giant viruses of protists and important pathogens of vertebrates, such as poxviruses. However, the characterization of viruses from nonmodel hosts still lags behind. We sequenced the complete genomes of three viruses infecting crustaceans, the Caribbean spiny lobster, demon shrimp, and European shore crab. These viruses have the smallest genomes among the known NCLDVs, with losses of many core genes, some of which are shared with iridoviruses. The deterioration of the transcription apparatus is compatible with microscopic and ultrastructural observations indicating that these viruses replicate in the nucleus of infected cells rather than in the cytoplasm. Phylogenomic analysis indicates that these viruses are sufficiently distinct from all other NCLDVs to justify the creation of a separate family, for which we propose the name “Mininucleoviridae” (i.e., small viruses reproducing in the cell nucleus).