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Dolja, V. V.

Publications and source records attributed to Dolja, V. V..

5 recordsLinked to original sources

Diversity and evolution of the ribovirian class Stelpaviricetes

Metatranscriptome mining has dramatically expanded the known diversity of ribovirians at all taxonomic levels. We explored in detail the class Stelpaviricetes in the phylum Pisuviricota that so far included 3 orders and 6 recognized virus families, order Stellavirales with family Astroviridae infecting vertebrates, Patatavirales with families Potyviridae, the largest known family of plant ribovirians, and Potyliviridae, and Hypofuvirales consisting of 3 families of viruses associated with phytopathogenic fungi. Using an order-specific collection of Hidden Markov Model profiles for the RNA-dependent RNA polymerase (RdRP), the hallmark protein of ribovirians, we identified 103 putative families within Stelpaviricetes, most of which share a uniform, astrovirus-like genome architecture, encoding three recognizable protein domains, the RdRP, a chymotrypsin-like protease and a single jelly roll capsid protein. The topology of the phylogenetic tree of the RdRP implies that the common ancestor of Stelpaviricetes had an astrovirus-like genome. The ancestor of the order Patatavirales acquired two additional domains, a papain-like protease and a superfamily 2 helicase, whereas the capsid protein was replaced with an unrelated one forming filamentous capsids. The ancestor of Hypofuvirales also encoded a superfamily 2 helicase and, possibly, a papain-like protease, but lost the capsid protein. Hypofuvirales might have derived from Patatavirales or evolved independently from an astro-like ancestor. For the vast majority of Stelpaviricetes identified in metatranscriptomes, host assignment remains elusive. Nevertheless, analysis of endogenous virus elements combined with information on isolated viruses provides some clues, in particular, suggesting that the common ancestor of Potyviridae and Potyliviridae had a fungal host whereas the common ancestor of Stelpaviricetes might have been a protist virus. IMPORTANCEThe enormous diversity of viruses on earth is only now coming to light through extensive metagenome and metatranscriptome mining. Using vast databases of ribovirus genomes, we performed phylogenomic analysis of the class Stelpaviricetes that includes the family of animal viruses Astroviridae and Potyviridae, the largest known family of plant viruses. We identified more than 100 family-level groups of viruses most of which have small, astrovirus-like genomes, likely, resembling the common ancestor of Stelpaviricetes. In contrast, the putative common ancestor of Potyviridae and its sister family Potyliviridae exhibits higher genome complexity that apparently emerged in viruses of fungi. The most plausible scenario for the origin of Potyviridae involves cross-kingdom horizontal virus transfer between plant-associated fungi and plants.

microbiology↗

The protein structurome of Orthornavirae and its dark matter

Metatranscriptomics is uncovering more and more diverse families of viruses with RNA genomes comprising the viral kingdom Orthornavirae in the realm Riboviria. Thorough protein annotation and comparison are essential to get insights into the functions of viral proteins and virus evolution. In addition to sequence- and hmm profile-based methods, protein structure comparison adds a powerful tool to uncover protein functions and relationships. We constructed an Orthornavirae structurome consisting of already annotated as well as unannotated ( dark matter) proteins and domains encoded in viral genomes. We used protein structure modeling and similarity searches to illuminate the remaining dark matter in hundreds of thousands of orthornavirus genomes. The vast majority of the dark matter domains showed either generic folds, such as single -helices, or no high confidence structure predictions. Nevertheless, a variety of lineage-specific globular domains that were new either to orthornaviruses in general or to particular virus families were identified within the proteomic dark matter of orthornaviruses, including several predicted nucleic acid-binding domains and nucleases. In addition, we identified a case of exaptation of a cellular nucleoside monophosphate kinase as an RNA-binding protein in several virus families. Notwithstanding the continuing discovery of numerous orthornaviruses, it appears that all the protein domains conserved in large groups of viruses have already been identified. The rest of the viral proteome seems to be dominated by poorly structured domains including intrinsically disordered ones that likely mediate specific virus-host interactions. IMPORTANCEAdvanced methods for protein structure prediction, such as AlphaFold2, greatly expand our capability to identify protein domains and infer their likely functions and evolutionary relationships. This is particularly pertinent for proteins encoded by viruses that are known evolve rapidly and as a result often cannot be adequately characterized by analysis of the protein sequences. We performed an exhaustive structure prediction and comparative analysis for uncharacterized proteins and domains ( dark matter) encoded by viruses with RNA genomes. The results show the dark matter of RNA virus proteome consists mostly of disordered and all -helical domains that cannot be readily assigned a specific function and that likely mediate various interactions between viral proteins and between viral and host proteins. The great majority of globular proteins and domains of RNA viruses are already known although we identified several unexpected domains represented in individual viral families.

evolutionary biology↗

A vast world of viroid-like circular RNAs revealed by mining metatranscriptomes

Viroids and viroid-like agents are unique, minimal RNA replicators that typically encode no proteins and hijack cellular enzymes for their genome replication. As the extent and diversity of viroid-like agents are poorly understood, we developed a computational pipeline to identify viroid-like covalently closed circular (ccc) RNAs and applied it to 5,131 global metatranscriptomes and 1,344 plant transcriptomes. The search resulted in 11,420 viroid-like, ribozyme-containing cccRNAs spanning 4,409 species-level clusters, which is a five-fold increase compared to the previously known set of viroids and viroid-like RNA agents. Within this diverse collection, we identified numerous putative novel viroids, satellite RNAs, retrozymes, and ribozylike viruses. We also found previously unknown ribozyme combinations and unusual ribozymes within the cccRNAs. Self-cleaving ribozymes were identified in both RNA strands of ambiviruses and some mito-like viruses as well as in capsid-encoding satellite virus-like cccRNAs. The broad presence of viroid-like cccRNAs in diverse transcriptomes and ecosystems implies that their host range is not limited to plants, and matches between viroid-like cccRNAs and CRISPR spacers suggest that some of them might replicate in prokaryotes.

microbiology↗

A five-fold expansion of the global RNA virome reveals multiple new clades of RNA bacteriophages

High-throughput RNA sequencing offers unprecedented opportunities to explore the Earth RNA virome. Mining 5,150 diverse metatranscriptomes uncovered >2.5 million RNA viral contigs. Via analysis of the 330k novel RNA-dependent RNA polymerases (RdRP), this expansion corresponds to a five-fold increase of RNA virus diversity. Extended RdRP phylogeny supports monophyly of the five established phyla, reveals two putative new bacteriophage phyla and numerous putative novel classes and orders. The dramatically expanded Lenarviricota phylum, consisting of bacterial and related eukaryotic viruses, now accounts for a third of the RNA virome diversity. Identification of CRISPR spacer matches and bacteriolytic proteins suggests that subsets of picobirnaviruses and partitiviruses, previously associated with eukaryotes, infect prokaryotic hosts. Gene content analysis revealed multiple domains previously not found in RNA viruses and implicated in virus-host interactions. This vast collection of new RNA virus genomes provides insights into RNA virus evolution and should become a major resource for RNA virology.

genomics↗

Origins and Evolution of the Global RNA Virome

Viruses with RNA genomes dominate the eukaryotic virome, reaching enormous diversity in animals and plants. The recent advances of metaviromics prompted us to perform a detailed phylogenomic reconstruction of the evolution of the dramatically expanded global RNA virome. The only universal gene among RNA viruses is the RNA-dependent RNA polymerase (RdRp). We developed an iterative computational procedure that alternates the RdRp phylogenetic tree construction with refinement of the underlying multiple sequence alignments. The resulting tree encompasses 4,617 RNA virus RdRps and consists of 5 major branches, 2 of which include positive-sense RNA viruses, 1 is a mix of positive-sense (+) RNA and double-stranded (ds) RNA viruses, and 2 consist of dsRNA and negative-sense (-) RNA viruses, respectively. This tree topology implies that dsRNA viruses evolved from +RNA viruses on at least two independent occasions, whereas -RNA viruses evolved from dsRNA viruses. Reconstruction of RNA virus evolution using the RdRp tree as the scaffold suggests that the last common ancestors of the major branches of +RNA viruses encoded only the RdRp and a single jelly-roll capsid protein. Subsequent evolution involved independent capture of additional genes, particularly, those encoding distinct RNA helicases, enabling replication of larger RNA genomes and facilitating virus genome expression and virus-host interactions. Phylogenomic analysis reveals extensive gene module exchange among diverse viruses and horizontal virus transfer between distantly related hosts. Although the network of evolutionary relationships within the RNA virome is bound to further expand, the present results call for a thorough reevaluation of the RNA virus taxonomy.\n\nIMPORTANCEThe majority of the diverse viruses infecting eukaryotes have RNA genomes, including numerous human, animal, and plant pathogens. Recent advances of metagenomics have led to the discovery of many new groups of RNA viruses in a wide range of hosts. These findings enable a far more complete reconstruction of the evolution of RNA viruses than what was attainable previously. This reconstruction reveals the relationships between different Baltimore Classes of viruses and indicates extensive transfer of viruses between distantly related hosts, such as plants and animals. These results call for a major revision of the existing taxonomy of RNA viruses.

microbiology↗