Remarkable virus diversity and organized community in filter-feeding oysters varied from those of the ocean virome

Abstract

Background:Viruses play critical roles in the marine environment because of their interactions with an extremely broad range of potential hosts. Many studies of viruses in seawater have been published, but viruses that inhabit marine animals have been largely neglected. Oysters are keystone species in coastal ecosystems, but as filter-feeding bivalves with very large roosting numbers and species co-habitation, it is not clear what role they play in marine virus transmission and coastal microbiome regulation.Results:Here we report a Dataset of Oyster Virome (DOV) that contains 728,784 nonredundant viral operational taxonomic unit (vOTU) (≥800 bp) contigs and 3,473 high-quality viral genomes, enabling the first comprehensive overview of both DNA and RNA viral communities in oysters (Crassostrea hongkongensis). We discovered tremendous diversity among novel viruses that inhabit oysters using multiple approaches, including reads recruitment, vOTUs, and high-quality virus genomes. Our results show that these viruses are very different from viruses in the oceans or other habitats. In particular, the high diversity of novel circoviruses that we found in oysters indicates that oysters may be potential hotspots for circoviruses. Notably, the viruses that were enriched in oysters are not random but are well organized communities that can respond to changes in the health state of the host and the external environment at both compositional and functional levels.Conclusions:In this study, we generated a first knowledge landscape of the oyster virome, which has increased the number of known oyster-related viruses by tens of thousands of times. Our results suggest that oysters provide a unique habitat that is different from that of seawater, and highlight the importance of filter-feeding bivalves for marine virus exploration as well as their essential but still invisible roles in regulating marine ecosystems.

Novel RNA viruses in oysters revealed by virome

“…We used 18 RNA virus sequences from the DOV obtained previously [ 14 ] for deep analysis. Because the 18 RNA virus sequences were very different they could not be reliably aligned, and therefore could not be used to construct a unified and reliable phylogenetic tree.…”

“…Furthermore, we found two virus types, Sobelivirales (sobemo‐like) and Leviviridae (levi‐like), that had not been identified previously in oysters. In our previous mining of DOV data, we found that there were a large number of unclassified circoviruses in oysters [ 14 ].…”

“…Although many studies have shown that the microbiota in oysters is mainly disturbed and influenced by the external environment [ 30 , 31 ], it is significantly different from the environment. It indicates that the internal environment of oysters has a selective effect on their inner microbial community [ 14 , 32 ]. All these data indicate that oysters have rich, diverse, and unique viral groups that are very different from the viruses found in marine invertebrates so far.…”

“…The Data set of Oyster Virome (DOV) was reported by Jiang et al [ 14 ]. DOV, which contains 728,784 contigs (≥800 bp) of nonredundant virus operation taxa (vOTU) and 3473 high‐quality viral genomes, provided the first comprehensive description of oyster viral community structure.…”

“…DOV, which contains 728,784 contigs (≥800 bp) of nonredundant virus operation taxa (vOTU) and 3473 high‐quality viral genomes, provided the first comprehensive description of oyster viral community structure. Among them, 4958 RNA virus‐related vOTUs were found to be particularly noteworthy [ 14 ]. This study used bioinformatics tools to analyze the genomes of 18 oyster‐associated RNA viruses among the RNA virus‐related vOTUs in DOV.…”