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Expansion of the global RNA virome reveals diverse clades of bacteriophages

Journal Article · · Cell
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High-throughput RNA sequencing offers broad opportunities to explore the Earth RNA virome. Mining 5,150 diverse metatranscriptomes uncovered >2.5 million RNA virus contigs. Analysis of >330,000 RNA-dependent RNA polymerases (RdRPs) shows that this expansion corresponds to a 5-fold increase of the known RNA virus diversity. Gene content analysis revealed multiple protein domains previously not found in RNA viruses and implicated in virus-host interactions. Extended RdRP phylogeny supports the monophyly of the five established phyla and reveals two putative additional bacteriophage phyla and numerous putative additional classes and orders. The dramatically expanded phylum Lenarviricota, consisting of bacterial and related eukaryotic viruses, now accounts for a third of the RNA virome. Identification of CRISPR spacer matches and bacteriolytic proteins suggests that subsets of picobirnaviruses and partitiviruses, previously associated with eukaryotes, infect prokaryotic hosts.
Research Organization:
Boston Univ., MA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB); USDOE Office of Science (SC), Biological and Environmental Research (BER)
Contributing Organization:
RNA Virus Discovery Consortium
Grant/Contract Number:
AC02-05CH11231; FG02-94ER20137; SC0020403
OSTI ID:
2570216
Alternate ID(s):
OSTI ID: 1969343
Journal Information:
Cell, Journal Name: Cell Journal Issue: 21 Vol. 185; ISSN 0092-8674
Publisher:
ElsevierCopyright Statement
Country of Publication:
United States
Language:
English

References (114)

BEDTools: The Swiss-Army Tool for Genome Feature Analysis: BEDTools: the Swiss-Army Tool for Genome Feature Analysis journal September 2014
Manual classification strategies in the ECOD database: ECOD Manual Classification Strategies journal May 2015
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen journal January 2001
Tumor necrosis factor receptor family members in the immune system journal December 1998
EMBOSS: The European Molecular Biology Open Software Suite journal June 2000
Functional Interaction between RNA Polymerase α Subunit C-Terminal Domain and σ70 in UP-Element- and Activator-Dependent Transcription journal June 2003
Jaks and cytokine receptors—An intimate relationship journal November 2006
Marine DNA Viral Macro- and Microdiversity from Pole to Pole journal May 2019
Gene Expression Changes and Community Turnover Differentially Shape the Global Ocean Metatranscriptome journal November 2019
An RNA Repair Operon Regulated by Damaged tRNAs journal December 2020
The logic of virus evolution journal July 2022
Comparative analysis of the active sites of orthologous endolysins of the Escherichia lytic bacteriophages T5, RB43, and RB49 journal January 2021
A Combined Transmembrane Topology and Signal Peptide Prediction Method journal May 2004
A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at its Core journal July 2018
Single-gene lysis in the metagenomic era journal August 2020
ITPA (inosine triphosphate pyrophosphatase): From surveillance of nucleotide pools to human disease and pharmacogenetics journal October 2013
Viral IAPs, then and now journal March 2015
Origins and evolution of viruses of eukaryotes: The ultimate modularity journal May 2015
Mitovirus UGA(Trp) codon usage parallels that of host mitochondria journal July 2017
Extensive conservation of prokaryotic ribosomal binding sites in known and novel picobirnaviruses journal March 2018
Multiple divergent picobirnaviruses with functional prokaryotic Shine-Dalgarno ribosome binding sites present in cloacal sample of a diarrheic chicken journal December 2018
Comparative and functional genomics of closteroviruses journal April 2006
Metagenomics reshapes the concepts of RNA virus evolution by revealing extensive horizontal virus transfer journal January 2018
Discovery of highly divergent lineages of plant-associated astro-like viruses sheds light on the emergence of potyviruses journal January 2019
MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices journal June 2016
Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses journal September 2016
Redefining the invertebrate RNA virosphere journal November 2016
MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets journal October 2017
Single-virus genomics reveals hidden cosmopolitan and abundant viruses journal June 2017
Fast and sensitive protein alignment using DIAMOND journal November 2014
Virus taxonomy in the age of metagenomics journal January 2017
A global ocean atlas of eukaryotic genes journal January 2018
Rapid de novo evolution of lysis genes in single-stranded RNA phages journal November 2020
Analysis of metagenome-assembled viral genomes from the human gut reveals diverse putative CrAss-like phages with unique genomic features journal February 2021
NUDT2 initiates viral RNA degradation by removal of 5′-phosphates journal November 2021
The new scope of virus taxonomy: partitioning the virosphere into 15 hierarchical ranks journal April 2020
Doubling of the known set of RNA viruses by metagenomic analysis of an aquatic virome journal July 2020
Evolutionary classification of CRISPR–Cas systems: a burst of class 2 and derived variants journal December 2019
Giant virus diversity and host interactions through global metagenomics journal January 2020
Petabase-scale sequence alignment catalyses viral discovery journal January 2022
CheckV assesses the quality and completeness of metagenome-assembled viral genomes journal December 2020
Generating lineage-resolved, complete metagenome-assembled genomes from complex microbial communities journal January 2022
Moisture modulates soil reservoirs of active DNA and RNA viruses journal August 2021
Identification of novel components of NAD-utilizing metabolic pathways and prediction of their biochemical functions journal January 2012
Shifting the genomic gold standard for the prokaryotic species definition journal October 2009
Structure of the Lassa virus nucleoprotein reveals a dsRNA-specific 3′ to 5′ exonuclease activity essential for immune suppression journal January 2011
Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil journal November 2019
Prokaryotic rRNA-mRNA interactions are involved in all translation steps and shape bacterial transcripts journal September 2021
A Fast and Symmetric DUST Implementation to Mask Low-Complexity DNA Sequences journal June 2006
Protein homology detection by HMM-HMM comparison journal November 2004
CD-HIT: accelerated for clustering the next-generation sequencing data journal October 2012
nhmmer: DNA homology search with profile HMMs journal July 2013
InterProScan 5: genome-scale protein function classification journal January 2014
MMseqs software suite for fast and deep clustering and searching of large protein sequence sets journal January 2016
The PRINTS database: a fine-grained protein sequence annotation and analysis resource--its status in 2012 journal January 2012
ggtreeExtra: Compact Visualization of Richly Annotated Phylogenetic Data journal June 2021
Consequences of Stop Codon Reassignment on Protein Evolution in Ciliates with Alternative Genetic Codes journal November 2007
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies journal November 2014
Within-Gene Shine–Dalgarno Sequences Are Not Selected for Function journal August 2018
Two Methods for Mapping and Visualizing Associated Data on Phylogeny Using Ggtree journal October 2018
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs journal September 1997
An efficient algorithm for large-scale detection of protein families journal April 2002
COG database update: focus on microbial diversity, model organisms, and widespread pathogens journal November 2020
CATH: increased structural coverage of functional space journal November 2020
Pfam: The protein families database in 2021 journal October 2020
The IMG/M data management and analysis system v.6.0: new tools and advanced capabilities journal October 2020
IMG/VR v3: an integrated ecological and evolutionary framework for interrogating genomes of uncultivated viruses journal November 2020
Genomes OnLine Database (GOLD) v.8: overview and updates journal November 2020
tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes journal August 2021
Advantages of combined transmembrane topology and signal peptide prediction--the Phobius web server journal May 2007
NCBI BLAST: a better web interface journal May 2008
HMMER web server: interactive sequence similarity searching journal May 2011
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools journal November 2012
SCOP2 prototype: a new approach to protein structure mining journal November 2013
Crass: identification and reconstruction of CRISPR from unassembled metagenomic data journal March 2013
MobiDB 2.0: an improved database of intrinsically disordered and mobile proteins journal October 2014
Database resources of the National Center for Biotechnology Information journal November 2017
HMMER web server: 2018 update journal June 2018
The SCOP database in 2020: expanded classification of representative family and superfamily domains of known protein structures journal November 2019
CDD/SPARCLE: the conserved domain database in 2020 journal November 2019
The virome from a collection of endomycorrhizal fungi reveals new viral taxa with unprecedented genome organization journal July 2020
Discovery of divided RdRp sequences and a hitherto unknown genomic complexity in fungal viruses journal December 2020
ICTV Virus Taxonomy Profile: Partitiviridae journal January 2018
Matplotlib: A 2D Graphics Environment journal January 2007
Expansion of known ssRNA phage genomes: From tens to over a thousand journal February 2020
Stop codon reassignments in the wild journal May 2014
Cryptic and abundant marine viruses at the evolutionary origins of Earth’s RNA virome journal April 2022
Are There 10 31 Virus Particles on Earth, or More, or Fewer? journal February 2020
Cultivation and Genomic, Nutritional, and Lipid Biomarker Characterization of Roseiflexus Strains Closely Related to Predominant In Situ Populations Inhabiting Yellowstone Hot Spring Microbial Mats journal April 2010
Partitiviruses Infecting Drosophila melanogaster and Aedes aegypti Exhibit Efficient Biparental Vertical Transmission journal September 2020
Molecular Aspects and Comparative Genomics of Bacteriophage Endolysins journal February 2013
Global Organization and Proposed Megataxonomy of the Virus World journal March 2020
Can Sequence Phylogenies Safely Infer the Origin of the Global Virome? journal April 2019
On the Origin of Reverse Transcriptase-Using CRISPR-Cas Systems and Their Hyperdiverse, Enigmatic Spacer Repertoires journal September 2017
Origins and Evolution of the Global RNA Virome journal November 2018
The Baltic Sea Virome: Diversity and Transcriptional Activity of DNA and RNA Viruses journal February 2017
DOE JGI Metagenome Workflow journal June 2021
Illuminating the Virosphere Through Global Metagenomics journal July 2021
BLAST+: architecture and applications journal January 2009
Prodigal: prokaryotic gene recognition and translation initiation site identification journal March 2010
The σ70 family of sigma factors journal January 2003
HH-suite3 for fast remote homology detection and deep protein annotation journal September 2019
Structure-function analysis of the yeast NAD+-dependent tRNA 2'-phosphotransferase Tpt1 journal January 2005
Hyperexpansion of RNA Bacteriophage Diversity journal March 2016
Selective Pressure Causes an RNA Virus to Trade Reproductive Fitness for Increased Structural and Thermal Stability of a Viral Enzyme journal November 2012
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments journal March 2010
Evolution and Diversity of the Microviridae Viral Family through a Collection of 81 New Complete Genomes Assembled from Virome Reads journal July 2012
Diversity in a Polymicrobial Community Revealed by Analysis of Viromes, Endolysins and CRISPR Spacers journal September 2016
De novo sequence assembly requires bioinformatic checking of chimeric sequences journal August 2020
The Mimivirus L375 Nudix enzyme hydrolyzes the 5’ mRNA cap journal September 2021
Comparative and Transcriptome Analyses Uncover Key Aspects of Coding- and Long Noncoding RNAs in Flatworm Mitochondrial Genomes journal May 2016
Metatranscriptome Library Preparation Influences Analyses of Viral Community Activity During a Brown Tide Bloom journal May 2021
Linking Virus Genomes with Host Taxonomy journal March 2016