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Nidoviruses comprise the most complex grouping among other viruses with respect to their multiplicity, phylogeny, systematics, species identification, genetic relationships within a taxon, progressive variability. Like other single-stranded RNA viruses, nidoviruses have a relatively high ability to mutate and recombine, which allows them to quickly adapt to new hosts and new ecological niches. Although most of the known representatives of nidoviruses are associated with terrestrial hosts, more and more data has recently appeared on nidoviruses recovered from aquatic organisms. This review is the analysis of current data on the representatives of the order Nidovirales associated with aquatic animals. They are all included in the eight families based on the current classification of viruses. The most studied among them are members of the families Coronaviridae, Tobaniviridae and Roniviridae. Representatives of the other families of aquatic animal nidoviruses were identified using metagenomic deep sequencing (metagenomics), but their effect on the host organism has not yet been adequately studied. Data on the distribution of nidoviruses among aquatic animals in different global aquatic systems are presented, clinical signs of the disease are described, a brief description of nidoviruses and their genomes is given. Nidoviruses of aquatic animals as the earliest members of the animal kingdom are supposed to have played a possible role in the evolution of terrestrial animal nidoviruses. Therefore, aquatic animal nidoviruses could play a significant role in the formation of new natural reservoirs unknown to science, as well as in their interspecies transfer between marine, freshwater and terrestrial hosts.

This review focuses on the monophyletic group of animal RNA viruses united in the order Nidovirales. The order includes the distantly related coronaviruses, toroviruses, and roniviruses, which possess the largest known RNA genomes (from 26 to 32 kb) and will therefore be called ‘large’ nidoviruses in this review. They are compared with their arterivirus cousins, which also belong to the Nidovirales despite having a much smaller genome (13–16 kb). Common and unique features that have been identified for either large or all nidoviruses are outlined. These include the nidovirus genetic plan and genome diversity, the composition of the replicase machinery and virus particles, virus-specific accessory genes, the mechanisms of RNA and protein synthesis, and the origin and evolution of nidoviruses with small and large genomes. Nidoviruses employ single-stranded, polycistronic RNA genomes of positive polarity that direct the synthesis of the subunits of the replicative complex, including the RNA-dependent RNA polymerase and helicase. Replicase gene expression is under the principal control of a ribosomal frameshifting signal and a chymotrypsin-like protease, which is assisted by one or more papain-like proteases. A nested set of subgenomic RNAs is synthesized to express the 3′-proximal ORFs that encode most conserved structural proteins and, in some large nidoviruses, also diverse accessory proteins that may promote virus adaptation to specific hosts. The replicase machinery includes a set of RNA-processing enzymes some of which are unique for either all or large nidoviruses. The acquisition of these enzymes may have improved the low fidelity of RNA replication to allow genome expansion and give rise to the ancestors of small and, subsequently, large nidoviruses.