Moisture modulates soil reservoirs of active DNA and RNA viruses

Wu, Ruonan; Davison, Michelle R.; Gao, Yuqian; Nicora, Carrie D.; Mcdermott, Jason E.; Burnum-Johnson, Kristin E.; Hofmockel, Kirsten S.; Jansson, Janet K.

doi:10.1038/s42003-021-02514-2

Title: Moisture modulates soil reservoirs of active DNA and RNA viruses

Journal Article · 26 August 2021 · Communications Biology

DOI: https://doi.org/10.1038/s42003-021-02514-2 · OSTI ID:1902562

; Davison, Michelle R.;

;

Abstract Soil is known to harbor viruses, but the majority are uncharacterized and their responses to environmental changes are unknown. Here, we used a multi-omics approach (metagenomics, metatranscriptomics and metaproteomics) to detect active DNA viruses and RNA viruses in a native prairie soil and to determine their responses to extremes in soil moisture. The majority of transcribed DNA viruses were bacteriophage, but some were assigned to eukaryotic hosts, mainly insects. We also demonstrated that higher soil moisture increased transcription of a subset of DNA viruses. Metaproteome data validated that the specific viral transcripts were translated into proteins, including chaperonins known to be essential for virion replication and assembly. The soil viral chaperonins were phylogenetically distinct from previously described marine viral chaperonins. The soil also had a high abundance of RNA viruses, with highest representation of Reoviridae . Leviviridae were the most diverse RNA viruses in the samples, with higher amounts in wet soil. This study demonstrates that extreme shifts in soil moisture have dramatic impacts on the composition, activity and potential functions of both DNA and RNA soil viruses.

View Journal Article

Cite

Export

Save

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

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1902562

Report Number(s):: PNNL-SA--160635; 992; PII: 2514

Journal Information:: Communications Biology, Journal Name: Communications Biology Journal Issue: 1 Vol. 4; ISSN 2399-3642

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (65)

Mini‐Metagenomics and Nucleotide Composition Aid the Identification and Host Association of Novel Bacteriophage Sequences Deaton, Jonathan; Yu, Feiqiao Brian; Quake, Stephen R. Advanced Biosystems, Vol. 3, Issue 11 https://doi.org/10.1002/adbi.201900108	journal	May 2019
Closterovirus Encoded HSP70 Homolog and p61 in Addition to Both Coat Proteins Function in Efficient Virion Assembly Satyanarayana, Tatineni; Gowda, Siddarame; Mawassi, Munir Virology, Vol. 278, Issue 1 https://doi.org/10.1006/viro.2000.0638	journal	December 2000
Phylogeny, Genome Evolution, and Host Specificity of Single-Stranded RNA Bacteriophage (Family Leviviridae) Bollback, Jonathan P.; Huelsenbeck, John P. Journal of Molecular Evolution, Vol. 52, Issue 2 https://doi.org/10.1007/s002390010140	journal	February 2001
The population biology of bacterial viruses: Why be temperate Stewart, Frank M.; Levin, Bruce R. Theoretical Population Biology, Vol. 26, Issue 1 https://doi.org/10.1016/0040-5809(84)90026-1	journal	August 1984
Viral concentration methods for diversity studies in soil samples Dias, Roberto Sousa; Abe, Aneli Eiko; Lima, Helena Santiago Applied Soil Ecology, Vol. 155 https://doi.org/10.1016/j.apsoil.2020.103666	journal	November 2020
Bacteriophages as sources of small non-coding RNA molecules Bloch, Sylwia; Lewandowska, Natalia; Węgrzyn, Grzegorz Plasmid, Vol. 113 https://doi.org/10.1016/j.plasmid.2020.102527	journal	January 2021
Addressing the challenge of soil metaproteome complexity by improving metaproteome depth of coverage through two-dimensional liquid chromatography Callister, Stephen J.; Fillmore, Thomas L.; Nicora, Carrie D. Soil Biology and Biochemistry, Vol. 125 https://doi.org/10.1016/j.soilbio.2018.07.018	journal	October 2018
Virocell Metabolism: Metabolic Innovations During Host–Virus Interactions in the Ocean Rosenwasser, Shilo; Ziv, Carmit; Creveld, Shiri Graff van Trends in Microbiology, Vol. 24, Issue 10 https://doi.org/10.1016/j.tim.2016.06.006	journal	October 2016
Ion mobility spectrometry and the omics: Distinguishing isomers, molecular classes and contaminant ions in complex samples Burnum-Johnson, Kristin E.; Zheng, Xueyun; Dodds, James N. TrAC Trends in Analytical Chemistry, Vol. 116 https://doi.org/10.1016/j.trac.2019.04.022	journal	July 2019
Are we missing half of the viruses in the ocean? Steward, Grieg F.; Culley, Alexander I.; Mueller, Jaclyn A. The ISME Journal, Vol. 7, Issue 3 https://doi.org/10.1038/ismej.2012.121	journal	November 2012
Genomes and gene expression across light and productivity gradients in eastern subtropical Pacific microbial communities Dupont, Chris L.; McCrow, John P.; Valas, Ruben The ISME Journal, Vol. 9, Issue 5 https://doi.org/10.1038/ismej.2014.198	journal	October 2014
Aquifer environment selects for microbial species cohorts in sediment and groundwater Hug, Laura A.; Thomas, Brian C.; Brown, Christopher T. The ISME Journal, Vol. 9, Issue 8 https://doi.org/10.1038/ismej.2015.2	journal	February 2015
Novel chaperonins are prevalent in the virioplankton and demonstrate links to viral biology and ecology Marine, Rachel L.; Nasko, Daniel J.; Wray, Jeffrey The ISME Journal, Vol. 11, Issue 11 https://doi.org/10.1038/ismej.2017.102	journal	July 2017
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
Uncovering Earth’s virome Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A. Nature, Vol. 536, Issue 7617 https://doi.org/10.1038/nature19094	journal	August 2016
MS-GF+ makes progress towards a universal database search tool for proteomics Kim, Sangtae; Pevzner, Pavel A. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6277	journal	October 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
Reassortment in segmented RNA viruses: mechanisms and outcomes McDonald, Sarah M.; Nelson, Martha I.; Turner, Paul E. Nature Reviews Microbiology, Vol. 14, Issue 7 https://doi.org/10.1038/nrmicro.2016.46	journal	May 2016
A CRISPR toolbox to study virus–host interactions Puschnik, Andreas S.; Majzoub, Karim; Ooi, Yaw Shin Nature Reviews Microbiology, Vol. 15, Issue 6 https://doi.org/10.1038/nrmicro.2017.29	journal	April 2017
Hidden diversity of soil giant viruses Schulz, Frederik; Alteio, Lauren; Goudeau, Danielle Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07335-2	journal	November 2018
Dynamic marine viral infections and major contribution to photosynthetic processes shown by spatiotemporal picoplankton metatranscriptomes Sieradzki, Ella T.; Ignacio-Espinoza, J. Cesar; Needham, David M. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-09106-z	journal	March 2019
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
Genome-centric view of carbon processing in thawing permafrost Woodcroft, Ben J.; Singleton, Caitlin M.; Boyd, Joel A. Nature, Vol. 560, Issue 7716 https://doi.org/10.1038/s41586-018-0338-1	journal	July 2018
Illuminating structural proteins in viral “dark matter” with metaproteomics Brum, Jennifer R.; Ignacio-Espinoza, J. Cesar; Kim, Eun-Hae Proceedings of the National Academy of Sciences, Vol. 113, Issue 9 https://doi.org/10.1073/pnas.1525139113	journal	February 2016
Diel cycling and long-term persistence of viruses in the ocean’s euphotic zone Aylward, Frank O.; Boeuf, Dominique; Mende, Daniel R. Proceedings of the National Academy of Sciences, Vol. 114, Issue 43 https://doi.org/10.1073/pnas.1714821114	journal	October 2017
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
WIsH: who is the host? Predicting prokaryotic hosts from metagenomic phage contigs Galiez, Clovis; Siebert, Matthias; Enault, François Bioinformatics, Vol. 33, Issue 19 https://doi.org/10.1093/bioinformatics/btx383	journal	July 2017
Computational approaches to predict bacteriophage–host relationships Edwards, Robert A.; McNair, Katelyn; Faust, Karoline FEMS Microbiology Reviews, Vol. 40, Issue 2 https://doi.org/10.1093/femsre/fuv048	journal	December 2015
Pfam: the protein families database Finn, Robert D.; Bateman, Alex; Clements, Jody Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1223	journal	November 2013
NCBI Viral Genomes Resource Brister, J. Rodney; Ako-adjei, Danso; Bao, Yiming Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1207	journal	November 2014
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
IMG/VR v.2.0: an integrated data management and analysis system for cultivated and environmental viral genomes Paez-Espino, David; Roux, Simon; Chen, I-Min A. Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1127	journal	November 2018
A window into lysogeny: revealing temperate phage biology with transcriptomics Owen, Siân V.; Canals, Rocío; Wenner, Nicolas Microbial Genomics, Vol. 6, Issue 2 https://doi.org/10.1099/mgen.0.000330	journal	February 2020
Viral noncoding RNAs: more surprises Tycowski, Kazimierz T.; Guo, Yang Eric; Lee, Nara Genes & Development, Vol. 29, Issue 6 https://doi.org/10.1101/gad.259077.115	journal	March 2015
A switch in translation mediated by an antisense RNA. Ranade, K.; Poteete, A. R. Genes & Development, Vol. 7, Issue 8 https://doi.org/10.1101/gad.7.8.1498	journal	August 1993
Incidence of lysogeny within temperate and extreme soil environments Williamson, Kurt E.; Radosevich, Mark; Smith, David W. Environmental Microbiology, Vol. 9, Issue 10 https://doi.org/10.1111/j.1462-2920.2007.01374.x	journal	October 2007
Phage-host interactions in soil Marsh, P.; Wellington, E. M. H. FEMS Microbiology Ecology, Vol. 15, Issue 1-2 https://doi.org/10.1111/j.1574-6941.1994.tb00234.x	journal	November 1994
Expansion of known ssRNA phage genomes: From tens to over a thousand Callanan, J.; Stockdale, S. R.; Shkoporov, A. Science Advances, Vol. 6, Issue 6 https://doi.org/10.1126/sciadv.aay5981	journal	February 2020
Establishing Lysogenic Transcription in the Temperate Coliphage 186 Neufing, Petra J.; Shearwin, Keith E.; Egan, J. Barry Journal of Bacteriology, Vol. 183, Issue 7 https://doi.org/10.1128/JB.183.7.2376-2379.2001	journal	April 2001
Cressdnaviricota : a Virus Phylum Unifying Seven Families of Rep-Encoding Viruses with Single-Stranded, Circular DNA Genomes Krupovic, Mart; Varsani, Arvind; Kazlauskas, Darius Journal of Virology, Vol. 94, Issue 12 https://doi.org/10.1128/JVI.00582-20	journal	April 2020
Expression and Functional Characterization of the First Bacteriophage-Encoded Chaperonin Kurochkina, Lidia P.; Semenyuk, Pavel I.; Orlov, Victor N. Journal of Virology, Vol. 86, Issue 18 https://doi.org/10.1128/JVI.00940-12	journal	July 2012
A Reovirus of the Fungus Cryphonectria parasitica That Is Infectious as Particles and Related to the Coltivirus Genus of Animal Pathogens Hillman, B. I.; Supyani, S.; Kondo, H. Journal of Virology, Vol. 78, Issue 2 https://doi.org/10.1128/JVI.78.2.892-898.2004	journal	December 2003
Terabase Metagenome Sequencing of Grassland Soil Microbiomes Nelson, William C.; Anderson, Lindsey N.; Wu, Ruonan Microbiology Resource Announcements, Vol. 9, Issue 32 https://doi.org/10.1128/MRA.00718-20	journal	August 2020
Frequency Analysis Techniques for Identification of Viral Genetic Data Trifonov, Vladimir; Rabadan, Raul mBio, Vol. 1, Issue 3 https://doi.org/10.1128/mBio.00156-10	journal	August 2010
Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust Van Goethem, Marc W.; Swenson, Tami L.; Trubl, Gareth mBio, Vol. 10, Issue 6 https://doi.org/10.1128/mBio.02287-19	journal	December 2019
Origins and Evolution of the Global RNA Virome Wolf, Yuri I.; Kazlauskas, Darius; Iranzo, Jaime mBio, Vol. 9, Issue 6 https://doi.org/10.1128/mBio.02329-18	journal	November 2018
Moleculo Long-Read Sequencing Facilitates Assembly and Genomic Binning from Complex Soil Metagenomes White, Richard Allen; Bottos, Eric M.; Roy Chowdhury, Taniya mSystems, Vol. 1, Issue 3 https://doi.org/10.1128/mSystems.00045-16	journal	June 2016
Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations Roy Chowdhury, Taniya; Lee, Joon-Yong; Bottos, Eric M. mSystems, Vol. 4, Issue 4 https://doi.org/10.1128/mSystems.00061-19	journal	June 2019
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 Baltic Sea Virome: Diversity and Transcriptional Activity of DNA and RNA Viruses Zeigler Allen, Lisa; McCrow, John P.; Ininbergs, Karolina mSystems, Vol. 2, Issue 1 https://doi.org/10.1128/mSystems.00125-16	journal	February 2017
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
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
Metabolic reprogramming by viruses in the sunlit and dark ocean Hurwitz, Bonnie L.; Hallam, Steven J.; Sullivan, Matthew B. Genome Biology, Vol. 14, Issue 11 https://doi.org/10.1186/gb-2013-14-11-r123	journal	January 2013
Bacteriophages isolated from Lake Michigan demonstrate broad host-range across several bacterial phyla Malki, Kema; Kula, Alex; Bruder, Katherine Virology Journal, Vol. 12, Issue 1 https://doi.org/10.1186/s12985-015-0395-0	journal	October 2015
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
Hyperexpansion of RNA Bacteriophage Diversity Krishnamurthy, Siddharth R.; Janowski, Andrew B.; Zhao, Guoyan PLOS Biology, Vol. 14, Issue 3 https://doi.org/10.1371/journal.pbio.1002409	journal	March 2016
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
Interplays between Soil-Borne Plant Viruses and RNA Silencing-Mediated Antiviral Defense in Roots Andika, Ida Bagus; Kondo, Hideki; Sun, Liying Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01458	journal	September 2016
Nutrient and Rainfall Additions Shift Phylogenetically Estimated Traits of Soil Microbial Communities Gravuer, Kelly; Eskelinen, Anu Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01271	journal	July 2017
The MPLEx Protocol for Multi-omic Analyses of Soil Samples Nicora, Carrie D.; Burnum-Johnson, Kristin E.; Nakayasu, Ernesto S. Journal of Visualized Experiments, Issue 135 https://doi.org/10.3791/57343	journal	January 2018
Transcription regulation mechanisms of bacteriophages: Recent advances and future prospects Yang, Haiquan; Ma, Yingfang; Wang, Yitian Bioengineered, Vol. 5, Issue 5 https://doi.org/10.4161/bioe.32110	journal	July 2014
CRISPRTarget: Bioinformatic prediction and analysis of crRNA targets Biswas, Ambarish; Gagnon, Joshua N.; Brouns, Stan J. J. RNA Biology, Vol. 10, Issue 5 https://doi.org/10.4161/rna.24046	journal	February 2013
Moisture Modulates Soil Reservoirs of Active DNA and RNA Viruses Wu, Ruonan; Davison, Michelle; Gao, Yuqian Zenodo https://doi.org/10.5281/zenodo.5081148	text	January 2021
The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T. PeerJ Preprints 4:e1900v1 https://doi.org/10.7287/peerj.preprints.1900v1	preprint	March 2016
VirSorter: mining viral signal from microbial genomic data Roux, Simon; Enault, Francois; Hurwitz, Bonnie L. PeerJ, Vol. 3 https://doi.org/10.7717/peerj.985	journal	January 2015

Similar Records

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

Journal Article · 2019 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1575852

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

Phosphate amendment drives bloom of RNA viruses after soil wet-up

Journal Article · 2025 · Soil Biology and Biochemistry · OSTI ID:2556965

Sieradzki, Ella T.; Allen, G. Michael; Kimbrel, Jeffrey A.; +6 more

Inter-Kingdom Viral Interactions

Dataset · 2025 · OSTI ID:2583337

Rodríguez-Ramos, Josué A.; Zimmerman, Amy E.; Wu, Ruonan; +4 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Ecology
Microbiology

Title: Moisture modulates soil reservoirs of active DNA and RNA viruses

Citation Formats

References (65)

Similar Records

Related Subjects