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Title: Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America

Viruses impact nearly all organisms on Earth, with ripples of influence in agriculture, health, and biogeochemical processes. However, very little is known about RNA viruses in an environmental context, and even less is known about their diversity and ecology in soil, 1 of the most complex microbial systems. Here, we assembled 48 individual metatranscriptomes from 4 habitats within a planted soil sampled over a 22-d time series: Rhizosphere alone, detritosphere alone, rhizosphere with added root detritus, and unamended soil (4 time points and 3 biological replicates). We resolved the RNA viral community, uncovering a high diversity of viral sequences. We also investigated possible host organisms by analyzing metatranscriptome marker genes. Based on viral phylogeny, much of the diversity was Narnaviridae that may parasitize fungi or Leviviridae, which may infect Proteobacteria. Both host and viral communities appear to be highly dynamic, and rapidly diverged depending on experimental conditions. The viral and host communities were structured based on the presence of root litter. Clear temporal dynamics by Leviviridae and their hosts indicated that viruses were replicating. With this time-resolved analysis, we show that RNA viruses are diverse, abundant, and active in soil. When viral infection causes host cell death, it may mobilize cell carbon in a process that may represent an overlooked component of soil carbon cycling.

Sponsoring Organization:
USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
Grant/Contract Number:
AC52-07NA27344; AC02-05CH11231; SC0010570; SC0016247; SC0010566; SC0016247
OSTI ID:
1575852
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 51 Vol. 116; ISSN 0027-8424
Publisher:
National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
English

References (104)

Picornavirales, a proposed order of positive-sense single-stranded RNA viruses with a pseudo-T = 3 virion architecture journal February 2008
Three mitovirus strains infecting a single isolate of Fusarium circinatum are the first putative members of the family Narnaviridae detected in a fungus of the genus Fusarium journal February 2014
Taxonomy of the order Mononegavirales: update 2016 journal May 2016
A novel monopartite dsRNA virus isolated from the entomopathogenic and nematophagous fungus Purpureocillium lilacinum journal September 2016
Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2017) journal April 2017
Characterization of a novel single-stranded RNA mycovirus related to invertebrate viruses from the plant pathogen Verticillium dahliae journal November 2017
Recognition of six additional cystoviruses: Pseudomonas virus phi6 is no longer the sole species of the family Cystoviridae journal December 2017
Multiple virus infection in a single strain of Fusarium poae shown by deep sequencing journal August 2016
Dynamic regulation of mitochondrial transcription as a mechanism of cellular adaptation journal September 2012
Classification, genetic variation and pathogenicity of Lymantria dispar nucleopolyhedrovirus isolates from Asia, Europe, and North America journal February 2014
Mitochondrial Transcription Is Regulated via an ATP “Sensing” Mechanism that Couples RNA Abundance to Respiration journal May 2006
Have biopesticides come of age? journal May 2012
Genome characterization of a debilitation-associated mitovirus infecting the phytopathogenic fungus Botrytis cinerea journal October 2010
Insect vector-mediated transmission of plant viruses journal May 2015
Evidence for contemporary plant mitoviruses journal May 2018
New insight into the RNA aquatic virosphere via viromics journal January 2018
Microscale patchiness of virioplankton journal April 2006
Marine viruses and their biogeochemical and ecological effects journal June 1999
A mitochondrial target for double-stranded RNA in diseased isolates of the fungus that causes Dutch elm disease journal October 1987
Selective progressive response of soil microbial community to wild oat roots journal November 2008
Are we missing half of the viruses in the ocean? journal November 2012
Responses of soil bacterial and fungal communities to extreme desiccation and rewetting journal July 2013
Unusual biology across a group comprising more than 15% of domain Bacteria journal June 2015
Plankton networks driving carbon export in the oligotrophic ocean journal February 2016
Redefining the invertebrate RNA virosphere journal November 2016
Virus-host relationships of marine single-celled eukaryotes resolved from metatranscriptomics journal June 2017
Fast gapped-read alignment with Bowtie 2 journal March 2012
Marine viruses — major players in the global ecosystem journal October 2007
Rising to the challenge: accelerated pace of discovery transforms marine virology journal February 2015
Use and abuse of correlation analyses in microbial ecology journal June 2019
Host-linked soil viral ecology along a permafrost thaw gradient journal July 2018
Mediterranean grassland soil C–N compound turnover is dependent on rainfall and depth, and is mediated by genomically divergent microorganisms journal May 2019
Multiple viral infections in Agaricus bisporus - Characterisation of 18 unique RNA viruses and 8 ORFans identified by deep sequencing journal May 2017
Design of virus-based nanomaterials for medicine, biotechnology, and energy journal January 2016
Repeating patterns of virioplankton production within an estuarine ecosystem journal June 2011
Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups journal June 2012
The biomass distribution on Earth journal May 2018
The rhabdoviruses of Entamoeba histolytica and Entamoeba invadens journal March 1976
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses journal June 2009
PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes journal May 2010
Search and clustering orders of magnitude faster than BLAST journal August 2010
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth journal April 2012
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data journal April 2012
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies journal January 2014
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
Mitochondrial tRNAs in the lower fungus Spizellomyces punctatus: tRNA editing and UAG 'stop' codons recognized as leucine journal February 1997
HMMER web server: interactive sequence similarity searching journal May 2011
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees journal April 2016
The Pfam protein families database in 2019 journal October 2018
Hyaloraphidium curvatum: A Linear Mitochondrial Genome, tRNA Editing, and an Evolutionary Link to Lower Fungi journal March 2002
Hypovirulence and Double-Stranded RNA in Botrytis cinerea journal December 2007
Biological identifications through DNA barcodes
  • Hebert, Paul D. N.; Cywinska, Alina; Ball, Shelley L.
  • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 270, Issue 1512 https://doi.org/10.1098/rspb.2002.2218
journal February 2003
The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses journal September 1991
Nucleotide sequence of a ssRNA phage from Acinetobacter: kinship to coliphages journal June 2002
ICTV Virus Taxonomy Profile: Fimoviridae journal November 2018
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks journal November 2003
Accurate, multi-kb reads resolve complex populations and detect rare microorganisms journal February 2015
Root Factors Induce Mitochondrial-Related Gene Expression and Fungal Respiration during the Developmental Switch from Asymbiosis to Presymbiosis in the Arbuscular Mycorrhizal Fungus Gigaspora rosea journal February 2003
Creating the CIPRES Science Gateway for inference of large phylogenetic trees conference November 2010
Microbial community assembly differs across minerals in a rhizosphere microcosm journal September 2018
Sorption of dissolved organic matter by mineral soils of the Siberian forest tundra journal October 2006
BARCODING: Assessing the effect of varying sequence length on DNA barcoding of fungi: BARCODING journal January 2007
Performance of the COX1 gene as a marker for the study of metabolically active Pezizomycotina and Agaricomycetes fungal communities from the analysis of soil RNA: The COX1 gene as a fungal RNA molecular marker journal October 2010
RNA viruses in the sea journal March 2009
DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer: DNA BARCODING OF OOMYCETES WITH COI AND ITS journal June 2011
Carbon sequestration under Miscanthus: a study of 13C distribution in soil aggregates: SOIL CARBON SEQUESTRATION UNDER MISCANTHUS journal October 2009
Evolutionary and ecological links between plant and fungal viruses journal August 2018
A Virus in a Fungus in a Plant: Three-Way Symbiosis Required for Thermal Tolerance journal January 2007
Diversity of Active Viral Infections within the Sphagnum Microbiome journal September 2018
Temporal Changes in the Ectomycorrhizal Community in Two Soil Horizons of a Temperate Oak Forest journal July 2008
A New Wine Saccharomyces cerevisiae Killer Toxin (Klus), Encoded by a Double-Stranded RNA Virus, with Broad Antifungal Activity Is Evolutionarily Related to a Chromosomal Host Gene journal January 2011
Mapping of Sugar and Amino Acid Availability in Soil around Roots with Bacterial Sensors of Sucrose and Tryptophan journal January 1999
Abundance and Diversity of Viruses in Six Delaware Soils journal June 2005
High-Resolution Metatranscriptomics Reveals the Ecological Dynamics of Mosquito-Associated RNA Viruses in Western Australia journal June 2017
Genome Structure of Caulobacter Phage phiCb5 journal February 2011
A Reovirus of the Fungus Cryphonectria parasitica That Is Infectious as Particles and Related to the Coltivirus Genus of Animal Pathogens journal December 2003
Viral Repression of Fungal Pheromone Precursor Gene Expression journal February 1998
The Characterization of RNA Viruses in Tropical Seawater Using Targeted PCR and Metagenomics journal June 2014
Origins and Evolution of the Global RNA Virome journal November 2018
Identification of Novel Viruses in Amblyomma americanum , Dermacentor variabilis , and Ixodes scapularis Ticks journal March 2018
Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing journal October 2018
The Baltic Sea Virome: Diversity and Transcriptional Activity of DNA and RNA Viruses journal February 2017
Viruses of Plant Pathogenic Fungi journal September 2009
Viruses in Soil Ecosystems: An Unknown Quantity Within an Unexplored Territory journal September 2017
Prodigal: prokaryotic gene recognition and translation initiation site identification journal March 2010
Diversity of pili-specific bacteriophages: genome sequence of IncM plasmid-dependent RNA phage M journal January 2012
A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents journal January 2013
Metagenomic analysis of the turkey gut RNA virus community journal November 2010
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
Hyperexpansion of RNA Bacteriophage Diversity journal March 2016
Metagenomic Analysis of RNA Viruses in a Fresh Water Lake journal September 2009
Characterization of the 18S rRNA Gene for Designing Universal Eukaryote Specific Primers journal February 2014
Taxonomic Resolutions Based on 18S rRNA Genes: A Case Study of Subclass Copepoda journal June 2015
The mitochondrial genome of the terrestrial carnivorous plant Utricularia reniformis (Lentibulariaceae): Structure, comparative analysis and evolutionary landmarks journal July 2017
Prospecting for viral natural enemies of the fire ant Solenopsis invicta in Argentina journal February 2018
Novel RNA viruses within plant parasitic cyst nematodes journal March 2018
Viruses and Nutrient Cycles in the Sea journal October 1999
A novel single-stranded RNA virus isolated from a phytopathogenic filamentous fungus, Rosellinia necatrix, with similarity to hypo-like viruses journal July 2014
High temporal and spatial diversity in marine RNA viruses implies that they have an important role in mortality and structuring plankton communities journal December 2014
Interplays between Soil-Borne Plant Viruses and RNA Silencing-Mediated Antiviral Defense in Roots journal September 2016
Virome Characterization of a Collection of S. sclerotiorum from Australia journal January 2018
Two Novel Relative Double-Stranded RNA Mycoviruses Infecting Fusarium poae Strain SX63 journal April 2016
Assessing the use of the mitochondrial cox1 marker for use in DNA barcoding of red algae (Rhodophyta) journal August 2006
Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone journal January 2016