Revealing RNA virus diversity and evolution in unicellular algae transcriptomes

Remarkably little is known about the diversity and evolution of RNA viruses in unicellular eukaryotes. We screened a total of 570 transcriptomes from the Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP) project that encompasses a wide diversity of microbial eukaryotes, including most major photosynthetic lineages (i.e. the microalgae). From this, we identified 30 new and divergent RNA virus species, occupying a range of phylogenetic positions within the overall diversity of RNA viruses. Approximately one-third of the newly described viruses comprised single-stranded positive-sense RNA viruses from the order Lenarviricota associated with fungi, plants and protists, while another third were related to the order Ghabrivirales, including members of the protist and fungi-associated Totiviridae. Other viral species showed sequence similarity to positive-sense RNA viruses from the algae-associated Marnaviridae, the double-stranded RNA Partitiviridae, as well as a single negative-sense RNA virus related to the Qinviridae. Importantly, we were able to identify divergent RNA viruses from distant host taxa, revealing the ancestry of these viral families and greatly extending our knowledge of the RNA viromes of microalgal cultures. Both the limited number of viruses detected per sample and the low sequence identity to known RNA viruses imply that additional microalgal viruses exist that could not be detected at the current sequencing depth or were too divergent to be identified using sequence similarity. Together, these results highlight the need for further investigation of algal-associated RNA viruses as well as the development of new tools to identify RNA viruses that exhibit very high levels of sequence divergence.

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High-Resolution Metatranscriptomics Reveals the Ecological Dynamics of Mosquito-Associated RNA Viruses in Western Australia

Journal of Virology ◽

10.1128/jvi.00680-17 ◽

2017 ◽

Vol 91 (17) ◽

Cited By ~ 62

Author(s):

Mang Shi ◽

Peter Neville ◽

Jay Nicholson ◽

John-Sebastian Eden ◽

Allison Imrie ◽

...

Keyword(s):

Western Australia ◽

Rna Viruses ◽

Rna Virus ◽

Geographic Location ◽

Striking Difference ◽

Sampling Location ◽

Virus Species ◽

Diverse Range ◽

Content Type ◽

Virus Diversity

ABSTRACT Mosquitoes harbor a high diversity of RNA viruses, including many that impact human health. Despite a growing effort to describe the extent and nature of the mosquito virome, little is known about how these viruses persist, spread, and interact with both their hosts and other microbes. To address this issue we performed a metatranscriptomics analysis of 12 Western Australian mosquito populations structured by species and geographic location. Our results identified the complete genomes of 24 species of RNA viruses from a diverse range of viral families and orders, among which 19 are newly described. Comparisons of viromes revealed a striking difference between the two mosquito genera, with viromes of mosquitoes of the Aedes genus exhibiting substantially less diversity and lower abundances than those of mosquitoes of the Culex genus, within which the viral abundance reached 16.87% of the total non-rRNA. In addition, there was little overlap in viral diversity between the two genera, although the viromes were very similar among the three Culex species studied, suggesting that the host taxon plays a major role in structuring virus diversity. In contrast, we found no evidence that geographic location played a major role in shaping RNA virus diversity, and several viruses discovered here exhibited high similarity (95 to 98% nucleotide identity) to those from Indonesia and China. Finally, using abundance-level and phylogenetic relationships, we were able to distinguish potential mosquito viruses from those present in coinfecting bacteria, fungi, and protists. In sum, our metatranscriptomics approach provides important insights into the ecology of mosquito RNA viruses. IMPORTANCE Studies of virus ecology have generally focused on individual viral species. However, recent advances in bulk RNA sequencing make it possible to utilize metatranscriptomic approaches to reveal both complete virus diversity and the relative abundance of these viruses. We used such a metatranscriptomic approach to determine key aspects of the ecology of mosquito viruses in Western Australia. Our results show that RNA viruses are some of the most important components of the mosquito transcriptome, and we identified 19 new virus species from a diverse set of virus families. A key result was that host genetic background plays a more important role in shaping virus diversity than sampling location, with Culex species harboring more viruses at higher abundance than those from Aedes mosquitoes.

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Metatranscriptomic Identification of Diverse and Divergent RNA Viruses in Green and Chlorarachniophyte Algae Cultures

Viruses ◽

10.3390/v12101180 ◽

2020 ◽

Vol 12 (10) ◽

pp. 1180

Author(s):

Justine Charon ◽

Vanessa Rossetto Marcelino ◽

Richard Wetherbee ◽

Heroen Verbruggen ◽

Edward C. Holmes

Keyword(s):

Rna Viruses ◽

Rna Virus ◽

Sequence Similarity ◽

Land Plants ◽

Homology Detection ◽

Microbial Eukaryotes ◽

Virus Transfer ◽

History Of ◽

First Time ◽

Distant Homolog

Our knowledge of the diversity and evolution of the virosphere will likely increase dramatically with the study of microbial eukaryotes, including the microalgae within which few RNA viruses have been documented. By combining total RNA sequencing with sequence and structural-based homology detection, we identified 18 novel RNA viruses in cultured samples from two major groups of microbial algae: the chlorophytes and the chlorarachniophytes. Most of the RNA viruses identified in the green algae class Ulvophyceae were related to the Tombusviridae and Amalgaviridae viral families commonly associated with land plants. This suggests that the evolutionary history of these viruses extends to divergence events between algae and land plants. Seven Ostreobium sp-associated viruses exhibited sequence similarity to the mitoviruses most commonly found in fungi, compatible with horizontal virus transfer between algae and fungi. We also document, for the first time, RNA viruses associated with chlorarachniophytes, including the first negative-sense (bunya-like) RNA virus in microalgae, as well as a distant homolog of the plant virus Virgaviridae, potentially signifying viral inheritance from the secondary chloroplast endosymbiosis that marked the origin of the chlorarachniophytes. More broadly, these data suggest that the scarcity of RNA viruses in algae results from limited investigation rather than their absence.

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Structure Unveils Relationships between RNA Virus Polymerases

Viruses ◽

10.3390/v13020313 ◽

2021 ◽

Vol 13 (2) ◽

pp. 313

Author(s):

Heli A. M. Mönttinen ◽

Janne J. Ravantti ◽

Minna M. Poranen

Keyword(s):

Phylogenetic Tree ◽

Rna Viruses ◽

Rna Virus ◽

Sequence Similarity ◽

Protein Structures ◽

Structural Similarity ◽

Functional Differentiation ◽

Comparison Method ◽

Homologous Structure ◽

Biological Entities

RNA viruses are the fastest evolving known biological entities. Consequently, the sequence similarity between homologous viral proteins disappears quickly, limiting the usability of traditional sequence-based phylogenetic methods in the reconstruction of relationships and evolutionary history among RNA viruses. Protein structures, however, typically evolve more slowly than sequences, and structural similarity can still be evident, when no sequence similarity can be detected. Here, we used an automated structural comparison method, homologous structure finder, for comprehensive comparisons of viral RNA-dependent RNA polymerases (RdRps). We identified a common structural core of 231 residues for all the structurally characterized viral RdRps, covering segmented and non-segmented negative-sense, positive-sense, and double-stranded RNA viruses infecting both prokaryotic and eukaryotic hosts. The grouping and branching of the viral RdRps in the structure-based phylogenetic tree follow their functional differentiation. The RdRps using protein primer, RNA primer, or self-priming mechanisms have evolved independently of each other, and the RdRps cluster into two large branches based on the used transcription mechanism. The structure-based distance tree presented here follows the recently established RdRp-based RNA virus classification at genus, subfamily, family, order, class and subphylum ranks. However, the topology of our phylogenetic tree suggests an alternative phylum level organization.

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Origins and Evolution of the Global RNA Virome

mBio ◽

10.1128/mbio.02329-18 ◽

2018 ◽

Vol 9 (6) ◽

Cited By ~ 121

Author(s):

Yuri I. Wolf ◽

Darius Kazlauskas ◽

Jaime Iranzo ◽

Adriana Lucía-Sanz ◽

Jens H. Kuhn ◽

...

Keyword(s):

Plant Pathogens ◽

Rna Viruses ◽

Rna Virus ◽

Phylogenomic Analysis ◽

Rna Helicases ◽

Sequence Alignments ◽

Recent Advances ◽

Wide Range ◽

Positive Sense ◽

Dsrna Viruses

ABSTRACTViruses 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 gene encoding 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 the branches include positive-sense RNA viruses, 1 is a mix of positive-sense (+) RNA and double-stranded RNA (dsRNA) 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, in particular, 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.IMPORTANCEThe 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 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.

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Marine RNA Virus Quasispecies Are Distributed throughout the Oceans

mSphere ◽

10.1128/mspheredirect.00157-19 ◽

2019 ◽

Vol 4 (2) ◽

Cited By ~ 8

Author(s):

Marli Vlok ◽

Andrew S. Lang ◽

Curtis A. Suttle

Keyword(s):

Amino Acid ◽

Rna Viruses ◽

Rna Virus ◽

Purifying Selection ◽

Amino Acid Sequences ◽

Metagenomic Data ◽

Spatial And Temporal Patterns ◽

Data Set ◽

Virus Diversity ◽

Virus Genomes

ABSTRACTRNA viruses, particularly genetically diverse members of thePicornavirales, are widespread and abundant in the ocean. Gene surveys suggest that there are spatial and temporal patterns in the composition of RNA virus assemblages, but data on their diversity and genetic variability in different oceanographic settings are limited. Here, we show that specific RNA virus genomes have widespread geographic distributions and that the dominant genotypes are under purifying selection. Genomes from three previously unknown picorna-like viruses (BC-1, -2, and -3) assembled from a coastal site in British Columbia, Canada, as well as marine RNA viruses JP-A, JP-B, andHeterosigma akashiwoRNA virus exhibited different biogeographical patterns. Thus, biotic factors such as host specificity and viral life cycle, and not just abiotic processes such as dispersal, affect marine RNA virus distribution. Sequence differences relative to reference genomes imply that virus quasispecies are under purifying selection, with synonymous single-nucleotide variations dominating in genomes from geographically distinct regions resulting in conservation of amino acid sequences. Conversely, sequences from coastal South Africa that mapped to marine RNA virus JP-A exhibited more nonsynonymous mutations, probably representing amino acid changes that accumulated over a longer separation. This biogeographical analysis of marine RNA viruses demonstrates that purifying selection is occurring across oceanographic provinces. These data add to the spectrum of known marine RNA virus genomes, show the importance of dispersal and purifying selection for these viruses, and indicate that closely related RNA viruses are pathogens of eukaryotic microbes across oceans.IMPORTANCEVery little is known about aquatic RNA virus populations and genome evolution. This is the first study that analyzes marine environmental RNA viral assemblages in an evolutionary and broad geographical context. This study contributes the largest marine RNA virus metagenomic data set to date, substantially increasing the sequencing space for RNA viruses and also providing a baseline for comparisons of marine RNA virus diversity. The new viruses discovered in this study are representative of the most abundant family of marine RNA viruses, theMarnaviridae, and expand our view of the diversity of this important group. Overall, our data and analyses provide a foundation for interpreting marine RNA virus diversity and evolution.

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Evolutionary origins of epidemic potential among human RNA viruses

10.1101/771394 ◽

2019 ◽

Author(s):

Lu Lu ◽

Liam Brierley ◽

Gail Robertson ◽

Feifei Zhang ◽

Samantha Lycett ◽

...

Keyword(s):

Rna Viruses ◽

Rna Virus ◽

Virus Genome ◽

Human Populations ◽

Infective Virus ◽

Genome Sequences ◽

Evolutionary Origins ◽

Virus Diversity ◽

Human Viruses ◽

Do So

AbstractTo have epidemic potential, a pathogen must be able to spread in human populations, but of human-infective RNA viruses only a minority can do so. We investigated the evolution of human transmissibility through parallel analyses of 1755 virus genome sequences from 39 RNA virus genera. We identified 57 lineages containing human-transmissible species and estimated that at least 74% of these lineages have evolved directly from non-human viruses in other mammals or birds, a public health threat recently designated “Disease X”. Human-transmissible viruses rarely evolve from virus lineages that can infect but not transmit between humans. This result cautions against focussing surveillance and mitigation efforts narrowly on currently known human-infective virus lineages and supports calls for a better understanding of RNA virus diversity in non-human hosts.

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Viromes in Marine Ecosystems Reveal Remarkable Invertebrate RNA Virus Diversity

10.1101/2021.04.21.440720 ◽

2021 ◽

Author(s):

Yu-Yi Zhang ◽

Yicong Chen ◽

Xiaoman Wei ◽

Jie Cui

Keyword(s):

Rna Viruses ◽

Rna Virus ◽

Marine Invertebrate ◽

Ecological Factors ◽

Virus Evolution ◽

Marine Ecosystems ◽

Invertebrate Species ◽

Virus Diversity ◽

First Time ◽

Special Notice

AbstractOcean viromes remain poorly understood and little is known about the ecological factors driving aquatic RNA virus evolution. In this study, we used a meta-transcriptomic approach to characterize the viromes of 58 marine invertebrate species across three seas. This revealed the presence of 315 newly identified RNA viruses in nine viral families or orders (Durnavirales, Totiviridae, Bunyavirales, Hantaviridae, Picornavirales, Flaviviridae, Hepelivirales, Solemoviridae and Tombusviridae), with most of them are sufficiently divergent to the documented viruses. With special notice that we first time revealed an ocean virus rooting to mammalian hantaviruses. We also found evidence for possible host sharing and switch events during virus evolution. In sum, we demonstrated the hidden diversity of marine invertebrate RNA viruses.

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Tissue Tropism and Transmission Ecology Predict Virulence of Human RNA Viruses

10.1101/581512 ◽

2019 ◽

Cited By ~ 1

Author(s):

Liam Brierley ◽

Amy B. Pedersen ◽

Mark E. J. Woolhouse

Keyword(s):

Public Health ◽

Machine Learning ◽

Risk Factors ◽

Random Forest ◽

Infectious Diseases ◽

Rna Viruses ◽

Rna Virus ◽

Tissue Tropism ◽

Virus Species ◽

Ecological Traits

AbstractNovel infectious diseases continue to emerge within human populations. Predictive studies have begun to identify pathogen traits associated with emergence. However, emerging pathogens vary widely in virulence, a key determinant of their ultimate risk to public health. Here, we use structured literature searches to review the virulence of each of the 214 known human-infective RNA virus species. We then use a machine learning framework to determine whether viral virulence can be predicted by ecological traits including human-to-human transmissibility, transmission routes, tissue tropisms and host range. Using severity of clinical disease as a measurement of virulence, we identified potential risk factors using predictive classification tree and random forest ensemble models. The random forest model predicted literature-assigned disease severity of test data with 90.3% accuracy, compared to a null accuracy of 74.2%. In addition to viral taxonomy, the ability to cause systemic infection, having renal and/or neural tropism, direct contact or respiratory transmission, and limited (0 < R0 ≤ 1) human-to-human transmissibility were the strongest predictors of severe disease. We present a novel, comparative perspective on the virulence of all currently known human RNA virus species. The risk factors identified may provide novel perspectives in understanding the evolution of virulence and elucidating molecular virulence mechanisms. These risk factors could also improve planning and preparedness in public health strategies as part of a predictive framework for novel human infections.Author SummaryNewly emerging infectious diseases present potentially serious threats to global health. Although studies have begun to identify pathogen traits associated with the emergence of new human diseases, these do not address why emerging infections vary in the severity of disease they cause, often termed ‘virulence’. We test whether ecological traits of human viruses can act as predictors of virulence, as suggested by theoretical studies. We conduct the first systematic review of virulence across all currently known human RNA virus species. We adopt a machine learning approach by constructing a random forest, a model that aims to optimally predict an outcome using a specific structure of predictors. Predictions matched literature-assigned ratings for 28 of 31 test set viruses. Our predictive model suggests that higher virulence is associated with infection of multiple organ systems, nervous systems or the renal systems. Higher virulence was also associated with contact-based or airborne transmission, and limited capability to transmit between humans. These risk factors may provide novel starting points for questioning why virulence should evolve and identifying causative mechanisms of virulence. In addition, our work could suggest priority targets for infectious disease surveillance and future public health risk strategies.BlurbComparative analysis using machine learning shows specificity of tissue tropism and transmission biology can act as predictive risk factors for virulence of human RNA viruses.

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RNA Viruses in Aquatic Unicellular Eukaryotes

Viruses ◽

10.3390/v13030362 ◽

2021 ◽

Vol 13 (3) ◽

pp. 362

Author(s):

Mohammadreza Sadeghi ◽

Yuji Tomaru ◽

Tero Ahola

Keyword(s):

Host Species ◽

Rna Viruses ◽

Rna Virus ◽

Sequence Information ◽

Virus Species ◽

Ecological Role ◽

Major Fraction ◽

Marine Virus ◽

Unicellular Eukaryotes

Increasing sequence information indicates that RNA viruses constitute a major fraction of marine virus assemblages. However, only 12 RNA virus species have been described, infecting known host species of marine single-celled eukaryotes. Eight of these use diatoms as hosts, while four are resident in dinoflagellate, raphidophyte, thraustochytrid, or prasinophyte species. Most of these belong to the order Picornavirales, while two are divergent and fall into the families Alvernaviridae and Reoviridae. However, a very recent study has suggested that there is extraordinary diversity in aquatic RNA viromes, describing thousands of viruses, many of which likely use protist hosts. Thus, RNA viruses are expected to play a major ecological role for marine unicellular eukaryotic hosts. In this review, we describe in detail what has to date been discovered concerning viruses with RNA genomes that infect aquatic unicellular eukaryotes.

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Application of a sequence-based taxonomic classification method to uncultured and unclassified marine single-stranded RNA viruses in the order Picornavirales

Virus Evolution ◽

10.1093/ve/vez056 ◽

2019 ◽

Vol 5 (2) ◽

Cited By ~ 3

Author(s):

Marli Vlok ◽

Andrew S Lang ◽

Curtis A Suttle

Keyword(s):

Rna Viruses ◽

Sequence Data ◽

Rna Virus ◽

Taxonomic Classification ◽

Sound Classification ◽

Virus Diversity ◽

Species Demarcation Threshold ◽

The Family ◽

Genetic Features ◽

Taxonomic Framework

Abstract Metagenomics has altered our understanding of microbial diversity and ecology. This includes its applications to viruses in marine environments that have demonstrated their enormous diversity. Within these are RNA viruses, many of which share genetic features with members of the order Picornavirales; yet, very few of these have been taxonomically classified. The only recognized family of marine RNA viruses is the Marnaviridae, which was founded based on discovery and characterization of the species Heterosigma akashiwo RNA virus. Two additional genera of marine RNA viruses, Labyrnavirus (one species) and Bacillarnavirus (three species), were subsequently defined within the order Picornavirales but not assigned to a family. We have defined a sequence-based framework for taxonomic classification of twenty marine RNA viruses into the family Marnaviridae. Using RNA-dependent RNA polymerase (RdRp) phylogeny and distance-based analyses, we assigned the genera Labyrnavirus and Bacillarnavirus to the family Marnaviridae and created four additional genera in the family: Locarnavirus (four species), Kusarnavirus (one species), Salisharnavirus (four species) and Sogarnavirus (six species). We used pairwise capsid protein comparisons to delineate species within families, with 75 per cent identity as the species demarcation threshold. The family displays high sequence diversities and Jukes–Cantor distances for both the RdRp and capsid genes, suggesting that the classified viruses are not representative of all of the virus diversity within the family and that there are many more extant taxa. Our proposed taxonomic framework provides a sound classification system for this group of viruses that will have broadly applicable principles for other viral groups. It is based on sequence data alone and provides a robust taxonomic framework to include viruses discovered via metagenomic studies, thereby greatly expanding the realm of viruses subject to taxonomic classification.

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