RNA Viruses Linked to Eukaryotic Hosts in Thawed Permafrost

Wu, Ruonan; Bottos, Eric M.; Danna, Vincent G.; Stegen, James C.; Jansson, Janet K.; Davison, Michelle R.; Chu, ed., Haiyan

doi:10.1128/msystems.00582-22

Title: RNA Viruses Linked to Eukaryotic Hosts in Thawed Permafrost

Journal Article · Tue Dec 20 00:00:00 EST 2022 · mSystems

DOI:https://doi.org/10.1128/msystems.00582-22· OSTI ID:1906224

^[1]; Bottos, Eric M. ^[2]; Danna, Vincent G. ^[1];

^[1];

^[1]; Davison, Michelle R. ^[1]; Chu, ed., Haiyan

Earth and Biological Sciences Directorate, Pacific Northwest National Lab, Richland, Washington, USA
Department of Biological Sciences, Thompson Rivers University, Kamloops, British Columbia, Canada

Arctic permafrost is thawing due to global warming, with unknown consequences on the microbial inhabitants or associated viruses. DNA viruses have previously been shown to be abundant and active in thawing permafrost, but little is known about RNA viruses in these systems. To address this knowledge gap, we assessed the composition of RNA viruses in thawed permafrost samples that were incubated for 97 days at 4°C to simulate thaw conditions. A diverse RNA viral community was assembled from metatranscriptome data including double-stranded RNA viruses, dominated by Reoviridae and Hypoviridae, and negative and positive single-stranded RNA viruses, with relatively high representations of Rhabdoviridae and Leviviridae, respectively. Sequences corresponding to potential plant and human pathogens were also detected. The detected RNA viruses primarily targeted dominant eukaryotic taxa in the samples (e.g., fungi, Metazoa and Viridiplantae) and the viral community structures were significantly associated with predicted host populations. These results indicate that RNA viruses are linked to eukaryotic host dynamics. Several of the RNA viral sequences contained auxiliary metabolic genes encoding proteins involved in carbon utilization (e.g., polygalacturosase), implying their potential roles in carbon cycling in thawed permafrost.

View Journal Article

Cite

Export

Save

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Laboratory Directed Research and Development (LDRD) Program

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1906224

Alternate ID(s):: OSTI ID: 1907852

Report Number(s):: PNNL-SA-170030; e00582-22

Journal Information:: mSystems, Journal Name: mSystems Vol. 7 Journal Issue: 6; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (70)

Origins and evolution of viruses of eukaryotes: The ultimate modularity Koonin, Eugene V.; Dolja, Valerian V.; Krupovic, Mart Virology, Vol. 479-480 https://doi.org/10.1016/j.virol.2015.02.039	journal	May 2015
Widespread Horizontal Gene Transfer from Double-Stranded RNA Viruses to Eukaryotic Nuclear Genomes Liu, H.; Fu, Y.; Jiang, D. Journal of Virology, Vol. 84, Issue 22 https://doi.org/10.1128/JVI.00955-10	journal	September 2010
DRAM for distilling microbial metabolism to automate the curation of microbiome function Shaffer, Michael; Borton, Mikayla A.; McGivern, Bridget B. Nucleic Acids Research, Vol. 48, Issue 16 https://doi.org/10.1093/nar/gkaa621	journal	August 2020
Expression of a truncated tomato polygalacturonase gene inhibits expression of the endogenous gene in transgenic plants Smith, C. J. S.; Watson, C. F.; Bird, C. R. MGG Molecular & General Genetics, Vol. 224, Issue 3 https://doi.org/10.1007/BF00262443	journal	December 1990
Bacterial and protozoan dynamics upon thawing and freezing of an active layer permafrost soil Schostag, Morten; Priemé, Anders; Jacquiod, Samuel The ISME Journal, Vol. 13, Issue 5 https://doi.org/10.1038/s41396-019-0351-x	journal	January 2019
A Novel Partitivirus in the Hypovirulent Isolate QT5-19 of the Plant Pathogenic Fungus Botrytis cinerea Kamaruzzaman, Md; He, Guoyuan; Wu, Mingde Viruses, Vol. 11, Issue 1 https://doi.org/10.3390/v11010024	journal	January 2019
eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences Huerta-Cepas, Jaime; Szklarczyk, Damian; Forslund, Kristoffer Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1248	journal	November 2015
Global status of tospovirus epidemics in diverse cropping systems: Successes achieved and challenges ahead Pappu, H. R.; Jones, R. A. C.; Jain, R. K. Virus Research, Vol. 141, Issue 2 https://doi.org/10.1016/j.virusres.2009.01.009	journal	May 2009
Ambisense polarity of genome RNA of orthomyxoviruses and coronaviruses Zhirnov, Oleg World Journal of Virology, Vol. 10, Issue 5 https://doi.org/10.5501/wjv.v10.i5.256	journal	September 2021
Host-linked soil viral ecology along a permafrost thaw gradient Emerson, Joanne B.; Roux, Simon; Brum, Jennifer R. Nature Microbiology, Vol. 3, Issue 8 https://doi.org/10.1038/s41564-018-0190-y	journal	July 2018
Eukaryotic large nucleo-cytoplasmic DNA viruses: Clusters of orthologous genes and reconstruction of viral genome evolution Yutin, Natalya; Wolf, Yuri I.; Raoult, Didier Virology Journal, Vol. 6, Issue 1 https://doi.org/10.1186/1743-422X-6-223	journal	January 2009
Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing Trubl, Gareth; Jang, Ho Bin; Roux, Simon mSystems, Vol. 3, Issue 5 https://doi.org/10.1128/mSystems.00076-18	journal	October 2018
The structure of a plant-specific partitivirus capsid reveals a unique coat protein domain architecture with an intrinsically disordered protrusion Byrne, Matthew; Kashyap, Aseem; Esquirol, Lygie Communications Biology, Vol. 4, Issue 1 https://doi.org/10.1038/s42003-021-02687-w	journal	October 2021
Influence of exogenous organic matter on prokaryotic and eukaryotic microbiota in an agricultural soil. A multidisciplinary approach Pezzolla, Daniela; Marconi, Gianpiero; Turchetti, Benedetta Soil Biology and Biochemistry, Vol. 82 https://doi.org/10.1016/j.soilbio.2014.12.008	journal	March 2015
Estimating DNA coverage and abundance in metagenomes using a gamma approximation Hooper, Sean D.; Dalevi, Daniel; Pati, Amrita Bioinformatics, Vol. 26, Issue 3 https://doi.org/10.1093/bioinformatics/btp687	journal	December 2009
The evolution of novel fungal genes from non-retroviral RNA viruses Taylor, Derek J.; Bruenn, Jeremy BMC Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1741-7007-7-88	journal	December 2009
Plant Polygalacturonases Involved in Cell Elongation and Separation—The Same but Different? Babu, Yashodar; Bayer, Martin Plants, Vol. 3, Issue 4 https://doi.org/10.3390/plants3040613	journal	December 2014
Nontargeted virus sequence discovery pipeline and virus clustering for metagenomic data Paez-Espino, David; Pavlopoulos, Georgios A.; Ivanova, Natalia N. Nature Protocols, Vol. 12, Issue 8 https://doi.org/10.1038/nprot.2017.063	journal	July 2017
Functions and mechanisms: polygalacturonases from plant pathogenic fungi as pathogenicity and virulence factors Nakamura, Masayuki; Iwai, Hisashi Journal of General Plant Pathology, Vol. 85, Issue 4 https://doi.org/10.1007/s10327-019-00856-8	journal	April 2019
Retention of the virus-derived sequences in the nuclear genome of grapevine as a potential pathway to virus resistance Bertsch, Christophe; Beuve, Monique; Dolja, Valerian V. Biology Direct, Vol. 4, Issue 1 https://doi.org/10.1186/1745-6150-4-21	journal	January 2009
RNA Replication without RNA-Dependent RNA Polymerase: Surprises from Hepatitis Delta Virus Lai, Michael M. C. Journal of Virology, Vol. 79, Issue 13 https://doi.org/10.1128/JVI.79.13.7951-7958.2005	journal	July 2005
Active virus-host interactions at sub-freezing temperatures in Arctic peat soil Trubl, Gareth; Kimbrel, Jeffrey A.; Liquet-Gonzalez, Jose Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-021-01154-2	journal	October 2021
The alkalophilic fungus Sodiomyces alkalinus hosts beta- and gammapartitiviruses together with a new fusarivirus Hrabáková, Lenka; Grum-Grzhimaylo, Alexey A.; Koloniuk, Igor PLOS ONE, Vol. 12, Issue 11 https://doi.org/10.1371/journal.pone.0187799	journal	November 2017
Interactions between bacterial and phage communities in natural environments Chevallereau, Anne; Pons, Benoît J.; van Houte, Stineke Nature Reviews Microbiology, Vol. 20, Issue 1 https://doi.org/10.1038/s41579-021-00602-y	journal	August 2021
Rice black‐streaked dwarf virus : From multiparty interactions among plant–virus–vector to intermittent epidemics Wu, Nan; Zhang, Lu; Ren, Yingdang Molecular Plant Pathology, Vol. 21, Issue 8 https://doi.org/10.1111/mpp.12946	journal	June 2020
RNA Synthesis and Capping by Non-segmented Negative Strand RNA Viral Polymerases: Lessons From a Prototypic Virus Ogino, Tomoaki; Green, Todd J. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01490	journal	July 2019
Factors Contributing to Anthrax Outbreaks in the Circumpolar North Hueffer, Karsten; Drown, Devin; Romanovsky, Vladimir EcoHealth, Vol. 17, Issue 1 https://doi.org/10.1007/s10393-020-01474-z	journal	January 2020
RNA-viromics reveals diverse communities of soil RNA viruses with the potential to affect grassland ecosystems across multiple trophic levels Hillary, Luke S.; Adriaenssens, Evelien M.; Jones, David L. ISME Communications, Vol. 2, Issue 1 https://doi.org/10.1038/s43705-022-00110-x	journal	April 2022
Permafrost as a potential pathogen reservoir Wu, Ruonan; Trubl, Gareth; Taş, Neslihan One Earth, Vol. 5, Issue 4 https://doi.org/10.1016/j.oneear.2022.03.010	journal	April 2022
Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil Starr, Evan P.; Nuccio, Erin E.; Pett-Ridge, Jennifer Proceedings of the National Academy of Sciences, Vol. 116, Issue 51 https://doi.org/10.1073/pnas.1908291116	journal	November 2019
Top 10 plant viruses in molecular plant pathology: Top 10 plant viruses Scholthof, Karen-Beth G.; Adkins, Scott; Czosnek, Henryk Molecular Plant Pathology, Vol. 12, Issue 9 https://doi.org/10.1111/j.1364-3703.2011.00752.x	journal	October 2011
The Genus Tospovirus: Emerging Bunyaviruses that Threaten Food Security Oliver, J. E.; Whitfield, A. E. Annual Review of Virology, Vol. 3, Issue 1 https://doi.org/10.1146/annurev-virology-100114-055036	journal	September 2016
Climatic Factors Influencing the Anthrax Outbreak of 2016 in Siberia, Russia Ezhova, Ekaterina; Orlov, Dmitry; Suhonen, Elli EcoHealth, Vol. 18, Issue 2 https://doi.org/10.1007/s10393-021-01549-5	journal	June 2021
VirSorter2: a multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses Guo, Jiarong; Bolduc, Ben; Zayed, Ahmed A. Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-020-00990-y	journal	February 2021
Identification of multiple independent horizontal gene transfers into poxviruses using a comparative genomics approach Bratke, Kirsten A.; McLysaght, Aoife BMC Evolutionary Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2148-8-67	journal	January 2008
The rhabdoviruses of Entamoeba histolytica and Entamoeba invadens Bird, R. G.; McCaul, T. F. Annals of Tropical Medicine & Parasitology, Vol. 70, Issue 1 https://doi.org/10.1080/00034983.1976.11687098	journal	March 1976
ViralZone: a knowledge resource to understand virus diversity Hulo, Chantal; de Castro, Edouard; Masson, Patrick Nucleic Acids Research, Vol. 39, Issue suppl_1 https://doi.org/10.1093/nar/gkq901	journal	October 2010
Coronavirus (COVID-19): A Review of Clinical Features, Diagnosis, and Treatment Hassan, Syed Adeel; Sheikh, Fahad N.; Jamal, Somia Cureus https://doi.org/10.7759/cureus.7355	journal	March 2020
Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes Hultman, Jenni; Waldrop, Mark P.; Mackelprang, Rachel Nature, Vol. 521, Issue 7551 https://doi.org/10.1038/nature14238	journal	March 2015
ICTV Virus Taxonomy Profile: Cystoviridae Poranen, Minna M.; Mäntynen, Sari Journal of General Virology, Vol. 98, Issue 10 https://doi.org/10.1099/jgv.0.000928	journal	October 2017
The microbial ecology of permafrost Jansson, Janet K.; Taş, Neslihan Nature Reviews Microbiology, Vol. 12, Issue 6 https://doi.org/10.1038/nrmicro3262	journal	May 2014
VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences Kieft, Kristopher; Zhou, Zhichao; Anantharaman, Karthik Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00867-0	journal	June 2020
VirFinder: a novel k-mer based tool for identifying viral sequences from assembled metagenomic data Ren, Jie; Ahlgren, Nathan A.; Lu, Yang Young Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0283-5	journal	July 2017
Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology Legendre, M.; Bartoli, J.; Shmakova, L. Proceedings of the National Academy of Sciences, Vol. 111, Issue 11 https://doi.org/10.1073/pnas.1320670111	journal	March 2014
The emerging problem of tospovirus infection and nonconventional methods of control Prins, Marcel; Goldbach, Rob Trends in Microbiology, Vol. 6, Issue 1 https://doi.org/10.1016/S0966-842X(97)01173-6	journal	January 1998
Environmental Fate of Double-Stranded RNA in Agricultural Soils Dubelman, Samuel; Fischer, Joshua; Zapata, Fatima PLoS ONE, Vol. 9, Issue 3 https://doi.org/10.1371/journal.pone.0093155	journal	March 2014
Viral Genome Size Distribution Does not Correlate with the Antiquity of the Host Lineages Campillo-Balderas, José A.; Lazcano, Antonio; Becerra, Arturo Frontiers in Ecology and Evolution, Vol. 3 https://doi.org/10.3389/fevo.2015.00143	journal	December 2015
Future threat from the past El-Sayed, Amr; Kamel, Mohamed Environmental Science and Pollution Research, Vol. 28, Issue 2 https://doi.org/10.1007/s11356-020-11234-9	journal	October 2020
Viruses as key reservoirs of antibiotic resistance genes in the environment Debroas, Didier; Siguret, Cléa The ISME Journal, Vol. 13, Issue 11 https://doi.org/10.1038/s41396-019-0478-9	journal	July 2019
ICTV Virus Taxonomy Profile: Hypoviridae Suzuki, Nobuhiro; Ghabrial, Said A.; Kim, Kook-Hyung Journal of General Virology, Vol. 99, Issue 5 https://doi.org/10.1099/jgv.0.001055	journal	May 2018
Linking Virus Genomes with Host Taxonomy Mihara, Tomoko; Nishimura, Yosuke; Shimizu, Yugo Viruses, Vol. 8, Issue 3 https://doi.org/10.3390/v8030066	journal	March 2016
Moisture modulates soil reservoirs of active DNA and RNA viruses Wu, Ruonan; Davison, Michelle R.; Gao, Yuqian Communications Biology, Vol. 4, Issue 1 https://doi.org/10.1038/s42003-021-02514-2	journal	August 2021
Novel Viruses in Mosquitoes from Brazilian Pantanal Maia, Laura Marina Siqueira; Pinto, Andressa Zelenski de Lara; Carvalho, Michellen Santos de Viruses, Vol. 11, Issue 10 https://doi.org/10.3390/v11100957	journal	October 2019
Outbreak of Anthrax in the Yamalo-Nenets Autonomous District in 2016, Epidemiological Peculiarities Popova, A. Yu.; Demina, Yu. V.; Ezhlova, E. B. Problems of Particularly Dangerous Infections, Issue 4 https://doi.org/10.21055/0370-1069-2016-4-42-46	journal	January 2016
The effects of warming and soil chemistry on bacterial community structure in Arctic tundra soils Ricketts, Michael P.; Matamala, Roser; Jastrow, Julie D. Soil Biology and Biochemistry, Vol. 148 https://doi.org/10.1016/j.soilbio.2020.107882	journal	September 2020
Precipitation in a warming world: Assessing projected hydro-climate changes in California and other Mediterranean climate regions Polade, Suraj D.; Gershunov, Alexander; Cayan, Daniel R. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-11285-y	journal	September 2017
Permafrost Meta-Omics and Climate Change Mackelprang, Rachel; Saleska, Scott R.; Jacobsen, Carsten Suhr Annual Review of Earth and Planetary Sciences, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-earth-060614-105126	journal	June 2016
Evolution of adaptive immunity from transposable elements combined with innate immune systems Koonin, Eugene V.; Krupovic, Mart Nature Reviews Genetics, Vol. 16, Issue 3 https://doi.org/10.1038/nrg3859	journal	December 2014
Redox Chemistry of Soils Bartlett, Richmond J.; James, Bruce R. Advances in Agronomy, p. 151-208 https://doi.org/10.1016/S0065-2113(08)60834-2	book	January 1993
DNA Viral Diversity, Abundance, and Functional Potential Vary across Grassland Soils with a Range of Historical Moisture Regimes Wu, Ruonan; Davison, Michelle R.; Nelson, William C. mBio, Vol. 12, Issue 6 https://doi.org/10.1128/mBio.02595-21	journal	December 2021
Dispersal limitation and thermodynamic constraints govern spatial structure of permafrost microbial communities Bottos, Eric M.; Kennedy, David W.; Romero, Elvira B. FEMS Microbiology Ecology, Vol. 94, Issue 8 https://doi.org/10.1093/femsec/fiy110	journal	June 2018
The family Rhabdoviridae: mono- and bipartite negative-sense RNA viruses with diverse genome organization and common evolutionary origins Dietzgen, Ralf G.; Kondo, Hideki; Goodin, Michael M. Virus Research, Vol. 227 https://doi.org/10.1016/j.virusres.2016.10.010	journal	January 2017
Manganese limitation as a mechanism for reduced decomposition in soils under atmospheric nitrogen deposition Whalen, Emily D.; Smith, Richard G.; Grandy, A. Stuart Soil Biology and Biochemistry, Vol. 127 https://doi.org/10.1016/j.soilbio.2018.09.025	journal	December 2018
Giant Viruses of Amoebas: An Update Aherfi, Sarah; Colson, Philippe; La Scola, Bernard Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00349	journal	March 2016
Evolutionary selection against short nucleotide sequences in viruses and their related hosts Zarai, Yoram; Zafrir, Zohar; Siridechadilok, Bunpote DNA Research, Vol. 27, Issue 2 https://doi.org/10.1093/dnares/dsaa008	journal	April 2020
FOAM (Functional Ontology Assignments for Metagenomes): a Hidden Markov Model (HMM) database with environmental focus Prestat, Emmanuel; David, Maude M.; Hultman, Jenni Nucleic Acids Research, Vol. 42, Issue 19 https://doi.org/10.1093/nar/gku702	journal	September 2014
Viral quasispecies Domingo, Esteban; Perales, Celia PLOS Genetics, Vol. 15, Issue 10 https://doi.org/10.1371/journal.pgen.1008271	journal	October 2019
CD-HIT Suite: a web server for clustering and comparing biological sequences Huang, Ying; Niu, Beifang; Gao, Ying Bioinformatics, Vol. 26, Issue 5 https://doi.org/10.1093/bioinformatics/btq003	journal	January 2010
Soil microbiomes and climate change Jansson, Janet K.; Hofmockel, Kirsten S. Nature Reviews Microbiology, Vol. 18, Issue 1 https://doi.org/10.1038/s41579-019-0265-7	journal	October 2019
Redefining the invertebrate RNA virosphere Shi, Mang; Lin, Xian-Dan; Tian, Jun-Hua Nature, Vol. 540, Issue 7634 https://doi.org/10.1038/nature20167	journal	November 2016

Similar Records

Moisture modulates soil reservoirs of active DNA and RNA viruses

Journal Article · Thu Aug 26 00:00:00 EDT 2021 · Communications Biology · OSTI ID:1906224

Wu, Ruonan; Davison, Michelle R.; Gao, Yuqian; +5 more

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

Journal Article · Tue Nov 26 00:00:00 EST 2019 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1906224

Starr, Evan P.; Nuccio, Erin E.; Pett-Ridge, Jennifer; +2 more

Uncovering novel RNA viruses in permafrost

Technical Report · Thu Oct 01 00:00:00 EDT 2020 · OSTI ID:1906224

Davison, Michelle R.; Wu, Ruonan; Danna, Vincent G.; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
RNA virus
metatranscriptomics
permafrost thaw
soil virus

Title: RNA Viruses Linked to Eukaryotic Hosts in Thawed Permafrost

Citation Formats

References (70)

Similar Records

Related Subjects