Virome composition in marine fish revealed by meta-transcriptomics

Abstract

Revealing the determinants of virome composition is central to placing disease emergence in a broader evolutionary context. Fish are the most species-rich group of vertebrates and so provide an ideal model system to study the factors that shape virome compositions and their evolution. We characterised the viromes of 19 wild-caught species of marine fish using total RNA sequencing (meta-transcriptomics) combined with analyses of sequence and protein structural homology to identify divergent viruses that often evade characterisation. From this, we identified 25 new vertebrate-associated viruses and a further 22 viruses likely associated with fish diet or their microbiomes. The vertebrate-associated viruses identified here included the first fish virus in the Matonaviridae (single-strand, negative-sense RNA virus). Other viruses fell within the Astroviridae, Picornaviridae, Arenaviridae, Reoviridae, Hepadnaviridae, Paramyxoviridae, Rhabdoviridae, Hantaviridae, Filoviridae and Flaviviridae and were sometimes phylogenetically distinct from known fish viruses. We also show how key metrics of virome composition—viral richness, abundance and diversity—can be analysed along with host ecological and biological factors as a means to understand virus ecology. Accordingly, these data suggest that that the vertebrate-associated viromes of the fish sampled here are predominantly shaped by the phylogenetic history (i.e. taxonomic order) of their hosts, along with several biological factors including water temperature, habitat depth, community diversity and swimming behaviour. No such correlations were found for viruses associated with porifera, molluscs, arthropods, fungi and algae, that are unlikely to replicate in fish hosts. Overall, these data indicate that fish harbour particularly large and complex viromes and the vast majority of fish viromes are undescribed.

Metagenomic sequencing reveals a lack of virus exchange between native and invasive freshwater fish across the Murray–Darling Basin, Australia

“…A key observation of our study was the absence of Cyprinid herpesviruses, including CyHV-3 , as well as other Alloherpesviridae , in any of the thirty-six RNA libraries. Similarly, although members of the Hepadnaviridae are commonly detected in fish ( Dill et al 2016 ; Lauber et al 2017 ; Geoghegan et al 2018 ; Geoghegan et al 2021 ) they were notably absent in our samples. The only DNA virus detected in this study was a novel poxvirus ( Poxviridae ) identified in western carp-gudgeon.…”

“…Notably, we identified two novel arenaviruses that clustered with members of the newly formed Antennavirus genus that includes fish hosts ( Shi et al 2018 ; Abudurexiti et al 2019 ). Western carp-gudgeon arenavirus found at Narrabri creek shared 36.9 per cent amino acid sequence similarity with its closest relative, Wenling frogfish arenavirus 1 ( Shi et al 2018 ) and grouped with recently discovered arenaviruses from pygmy gobies ( Eviota zebrina ) sampled from an Australian coral reef ( Geoghegan et al 2021 ). Eastern mosquitofish arenavirus found in the Macquarie River shared 84.5 per cent amino acid sequence similarity with its closest available relative, Wenling frogfish arenavirus 1 .…”

“…Tissue specimens (liver and gills) were placed in RNALater and stored in a portable −80 °C freezer, then later in an −80 °C freezer in the laboratory at Macquarie University, Sydney. Tissue selection was based on previous studies ( Shi et al 2018 ; Geoghegan et al 2018 ; Geoghegan et al 2021 ), which show that liver and gill tissue serve as a rich source of viruses. To facilitate virus discovery, multiple individuals (one to ten) were pooled according to species and the location in which they were captured ( Supplementary Table S2 and Fig.…”

Beyond the Gastrointestinal Tract: The Emerging and Diverse Tissue Tropisms of Astroviruses

“…The International Committee on the Taxonomy of Viruses (ICTV) currently recognizes two genera of astroviruses, avastrovirus (avian astroviruses) and mamastroviruses (mammalian astroviruses; Figure 2 ) [ 4 ]. However, this naming convention will likely undergo further expansion as newer astrovirus genomes have now been identified from many other vertebrates including reptiles, amphibians, and fish, and from invertebrates ( Figure 2 ) [ 5 , 6 , 7 ]. In addition, some astrovirus-like viruses have been identified, including those that have evidence of recombination with hepatitis E [ 8 ].…”

A Novel Rubi-Like Virus in the Pacific Electric Ray (Tetronarce californica) Reveals the Complex Evolutionary History of the Matonaviridae

“…The first of these, Guangdong Chinese water snake rubivirus, was discovered via a large virological survey of vertebrates in China and is highly divergent from RuV, only sharing around 34% amino acid identity [10]. Similarly, Tiger flathead matonavirus was identified through a metatranscriptomic exploration of Australian marine fish [11], and, along with Guangdong Chinese water snake rubivirus, forms a sister clade to RuV. Even more recently, two novel rubella-like virus species were described: Rustrela virus, identified in several mammalian species in, and in close proximity to, a zoo in Germany, and Ruhugu virus from bats in Uganda [12].…”