Single-virus genomics reveals hidden cosmopolitan and abundant viruses

Martinez-Hernandez, Francisco; Fornas, Oscar; Lluesma Gomez, Monica; Bolduc, Benjamin; de la Cruz Peña, Maria Jose; Martínez, Joaquín MartÃ­nez; Anton, Josefa; Gasol, Josep M.; Rosselli, Riccardo; Rodriguez-Valera, Francisco; Sullivan, Matthew B.; Acinas, Silvia G.; Martinez-Garcia, Manuel

doi:10.1038/ncomms15892

Title: Single-virus genomics reveals hidden cosmopolitan and abundant viruses

Journal Article · Fri Jun 23 00:00:00 EDT 2017 · Nature Communications

DOI:https://doi.org/10.1038/ncomms15892· OSTI ID:1424950

Martinez-Hernandez, Francisco ^[1]; Fornas, Oscar ^[2]; Lluesma Gomez, Monica ^[1]; Bolduc, Benjamin ^[3]; de la Cruz Peña, Maria Jose ^[1]; Martínez, Joaquín MartÃnez ^[4]; Anton, Josefa ^[1]; Gasol, Josep M. ^[5]; Rosselli, Riccardo ^[6]; Rodriguez-Valera, Francisco ^[6]; Sullivan, Matthew B. ^[7]; Acinas, Silvia G. ^[5]; Martinez-Garcia, Manuel ^[1]

University of Alicante (Spain). Department of Physiology, Genetics, and Microbiology
The Barcelona Institute for Science and Technology (BIST) (Spain). Centre for Genomic Regulation (CRG; Universitat Pompeu Fabra (UPF), Barcelona (Spain)
The Ohio State Univ., Columbus, OH (United States). Department of Microbiology
Bigelow Laboratory for Ocean Sciences, East Boothbay, ME (United States)
Institut de Ciencies del Mar (ICM), Barcelona (Spain). Department of Marine Biology and Oceanography
Universidad Miguel Hernandez, San Juan (Spain). Evolutionary Genomics Group, Departamento de Produccion Vegetal y Microbiologia
The Ohio State Univ., Columbus, OH (United States). Department of Microbiology and Department of Civil, Environmental and Geodetic Engineering

Microbes drive ecosystems under constraints imposed by viruses. However, a lack of virus genome information hinders our ability to answer fundamental, biological questions concerning microbial communities. Here we apply single-virus genomics (SVGs) to assess whether portions of marine viral communities are missed by current techniques. The majority of the here-identified 44 viral single-amplified genomes (vSAGs) are more abundant in global ocean virome data sets than published metagenome-assembled viral genomes or isolates. This indicates that vSAGs likely best represent the dsDNA viral populations dominating the oceans. Species-specific recruitment patterns and virome simulation data suggest that vSAGs are highly microdiverse and that microdiversity hinders the metagenomic assembly, which could explain why their genomes have not been identified before. Altogether, SVGs enable the discovery of some of the likely most abundant and ecologically relevant marine viral species, such as vSAG 37-F6, which were overlooked by other methodologies.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of Arizona, Tucson, AZ (United States)

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

Grant/Contract Number:: SC0010580

OSTI ID:: 1424950

Journal Information:: Nature Communications, Vol. 8; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 95 works

Citation information provided by
Web of Science

References (64)

Single-cell genomics-based analysis of virus–host interactions in marine surface bacterioplankton Labonté, Jessica M.; Swan, Brandon K.; Poulos, Bonnie The ISME Journal, Vol. 9, Issue 11 https://doi.org/10.1038/ismej.2015.48	journal	April 2015
riboFrame: An Improved Method for Microbial Taxonomy Profiling from Non-Targeted Metagenomics Ramazzotti, Matteo; Berná, Luisa; Donati, Claudio Frontiers in Genetics, Vol. 6 https://doi.org/10.3389/fgene.2015.00329	journal	November 2015
The Marine Viromes of Four Oceanic Regions Angly, Florent E.; Felts, Ben; Breitbart, Mya PLoS Biology, Vol. 4, Issue 11 https://doi.org/10.1371/journal.pbio.0040368	journal	November 2006
Explaining microbial population genomics through phage predation Rodriguez-Valera, Francisco; Martin-Cuadrado, Ana-Belen; Rodriguez-Brito, Beltran Nature Reviews Microbiology, Vol. 7, Issue 11 https://doi.org/10.1038/nrmicro2235	journal	November 2009
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data Kearse, M.; Moir, R.; Wilson, A. Bioinformatics, Vol. 28, Issue 12 https://doi.org/10.1093/bioinformatics/bts199	journal	April 2012
The human gut virome: Inter-individual variation and dynamic response to diet Minot, S.; Sinha, R.; Chen, J. Genome Research, Vol. 21, Issue 10 https://doi.org/10.1101/gr.122705.111	journal	August 2011
Quality control and preprocessing of metagenomic datasets Schmieder, R.; Edwards, R. Bioinformatics, Vol. 27, Issue 6 https://doi.org/10.1093/bioinformatics/btr026	journal	January 2011
Environmental proteomics of microbial plankton in a highly productive coastal upwelling system Sowell, Sarah M.; Abraham, Paul E.; Shah, Manesh The ISME Journal, Vol. 5, Issue 5 https://doi.org/10.1038/ismej.2010.168	journal	November 2010
Evaluation of viral genome assembly and diversity estimation in deep metagenomes Aguirre de Cárcer, Daniel; Angly, Florent E.; Alcamí, Antonio BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-989	journal	January 2014
Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer Gregory, Ann C.; Solonenko, Sergei A.; Ignacio-Espinoza, J. Cesar BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-3286-x	journal	November 2016
Reticulate Representation of Evolutionary and Functional Relationships between Phage Genomes Lima-Mendez, G.; Van Helden, J.; Toussaint, A. Molecular Biology and Evolution, Vol. 25, Issue 4 https://doi.org/10.1093/molbev/msn023	journal	February 2008
Virus taxonomy in the age of metagenomics Simmonds, Peter; Adams, Mike J.; Benkő, Mária Nature Reviews Microbiology, Vol. 15, Issue 3 https://doi.org/10.1038/nrmicro.2016.177	journal	January 2017
Microbial community associated with the colonial ascidian Cystodytes dellechiajei Martínez-García, Manuel; Díaz-Valdés, Marta; Wanner, Gerhard Environmental Microbiology, Vol. 9, Issue 2 https://doi.org/10.1111/j.1462-2920.2006.01170.x	journal	February 2007
A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes Dutilh, Bas E.; Cassman, Noriko; McNair, Katelyn Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5498	journal	July 2014
Artificial Neural Networks Trained to Detect Viral and Phage Structural Proteins Seguritan, Victor; Alves, Nelson; Arnoult, Michael PLoS Computational Biology, Vol. 8, Issue 8 https://doi.org/10.1371/journal.pcbi.1002657	journal	August 2012
Single-Cell Genomics Reveals Hundreds of Coexisting Subpopulations in Wild Prochlorococcus Kashtan, N.; Roggensack, S. E.; Rodrigue, S. Science, Vol. 344, Issue 6182 https://doi.org/10.1126/science.1248575	journal	April 2014
Mauve: Multiple Alignment of Conserved Genomic Sequence With Rearrangements Darling, A. C. E. Genome Research, Vol. 14, Issue 7 https://doi.org/10.1101/gr.2289704	journal	June 2004
A Single‐Nucleotide Polymorphism in a Herpesvirus DNA Polymerase Is Sufficient to Cause Lethal Neurological Disease Van de Walle, Gerlinde R.; Goupil, Ryan; Wishon, Cassandra The Journal of Infectious Diseases, Vol. 200, Issue 1 https://doi.org/10.1086/599316	journal	July 2009
Patterns and ecological drivers of ocean viral communities Brum, J. R.; Ignacio-Espinoza, J. C.; Roux, S. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.1261498	journal	May 2015
Gegenees: Fragmented Alignment of Multiple Genomes for Determining Phylogenomic Distances and Genetic Signatures Unique for Specified Target Groups Ågren, Joakim; Sundström, Anders; Håfström, Therese PLoS ONE, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pone.0039107	journal	June 2012
Marine viruses — major players in the global ecosystem Suttle, Curtis A. Nature Reviews Microbiology, Vol. 5, Issue 10 https://doi.org/10.1038/nrmicro1750	journal	October 2007
The Pacific Ocean Virome (POV): A Marine Viral Metagenomic Dataset and Associated Protein Clusters for Quantitative Viral Ecology Hurwitz, Bonnie L.; Sullivan, Matthew B. PLoS ONE, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pone.0057355	journal	February 2013
MetaGene: prokaryotic gene finding from environmental genome shotgun sequences Noguchi, Hideki; Park, Jungho; Takagi, Toshihisa Nucleic Acids Research, Vol. 34, Issue 19 https://doi.org/10.1093/nar/gkl723	journal	October 2006
Viral tagging reveals discrete populations in Synechococcus viral genome sequence space Deng, Li; Ignacio-Espinoza, J. Cesar; Gregory, Ann C. Nature, Vol. 513, Issue 7517 https://doi.org/10.1038/nature13459	journal	July 2014
Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses Roux, Simon; Brum, Jennifer R.; Dutilh, Bas E. Nature, Vol. 537, Issue 7622 https://doi.org/10.1038/nature19366	journal	September 2016
Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: changes in the genetic diversity of bacterial populations SchÃ¤fer, Hendrik; Bernard, Laetitia; Courties, Claude FEMS Microbiology Ecology, Vol. 34, Issue 3 https://doi.org/10.1111/j.1574-6941.2001.tb00775.x	journal	January 2001
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
Visualization of bacteriophage P1 infection by cryo-electron tomography of tiny Escherichia coli Liu, Jun; Chen, Cheng-Yen; Shiomi, Daisuke Virology, Vol. 417, Issue 2 https://doi.org/10.1016/j.virol.2011.06.005	journal	September 2011
ProDeGe: a computational protocol for fully automated decontamination of genomes Tennessen, Kristin; Andersen, Evan; Clingenpeel, Scott The ISME Journal, Vol. 10, Issue 1 https://doi.org/10.1038/ismej.2015.100	journal	June 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
Bacterial Vesicles in Marine Ecosystems Biller, S. J.; Schubotz, F.; Roggensack, S. E. Science, Vol. 343, Issue 6167 https://doi.org/10.1126/science.1243457	journal	January 2014
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth Peng, Y.; Leung, H. C. M.; Yiu, S. M. Bioinformatics, Vol. 28, Issue 11 https://doi.org/10.1093/bioinformatics/bts174	journal	April 2012
Abundant SAR11 viruses in the ocean Zhao, Yanlin; Temperton, Ben; Thrash, J. Cameron Nature, Vol. 494, Issue 7437 https://doi.org/10.1038/nature11921	journal	February 2013
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
Single Virus Genomics: A New Tool for Virus Discovery Allen, Lisa Zeigler; Ishoey, Thomas; Novotny, Mark A. PLoS ONE, Vol. 6, Issue 3 https://doi.org/10.1371/journal.pone.0017722	journal	March 2011
Capturing Single Cell Genomes of Active Polysaccharide Degraders: An Unexpected Contribution of Verrucomicrobia Martinez-Garcia, Manuel; Brazel, David M.; Swan, Brandon K. PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0035314	journal	April 2012
Optimization of Procedures for Counting Viruses by Flow Cytometry Brussaard, C. P. D. Applied and Environmental Microbiology, Vol. 70, Issue 3 https://doi.org/10.1128/AEM.70.3.1506-1513.2004	journal	March 2004
Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes Albertsen, Mads; Hugenholtz, Philip; Skarshewski, Adam Nature Biotechnology, Vol. 31, Issue 6 https://doi.org/10.1038/nbt.2579	journal	May 2013
Structure and function of the global ocean microbiome Sunagawa, S.; Coelho, L. P.; Chaffron, S. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.1261359	journal	May 2015
Common Contaminants in Next-Generation Sequencing That Hinder Discovery of Low-Abundance Microbes Laurence, Martin; Hatzis, Christos; Brash, Douglas E. PLoS ONE, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pone.0097876	journal	May 2014
Healthy human gut phageome Manrique, Pilar; Bolduc, Benjamin; Walk, Seth T. Proceedings of the National Academy of Sciences, Vol. 113, Issue 37 https://doi.org/10.1073/pnas.1601060113	journal	August 2016
Metavir 2: new tools for viral metagenome comparison and assembled virome analysis Roux, Simon; Tournayre, Jeremy; Mahul, Antoine BMC Bioinformatics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2105-15-76	journal	January 2014
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Single-cell genome sequencing: current state of the science Gawad, Charles; Koh, Winston; Quake, Stephen R. Nature Reviews Genetics, Vol. 17, Issue 3 https://doi.org/10.1038/nrg.2015.16	journal	January 2016
iVirus: facilitating new insights in viral ecology with software and community data sets imbedded in a cyberinfrastructure Bolduc, Benjamin; Youens-Clark, Ken; Roux, Simon The ISME Journal, Vol. 11, Issue 1 https://doi.org/10.1038/ismej.2016.89	journal	July 2016
The Discovery of phiAGATE, A Novel Phage Infecting Bacillus pumilus, Leads to New Insights into the Phylogeny of the Subfamily Spounavirinae Barylski, Jakub; Nowicki, Grzegorz; Goździcka-Józefiak, Anna PLoS ONE, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pone.0086632	journal	January 2014
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
Obtaining genomes from uncultivated environmental microorganisms using FACS–based single-cell genomics Rinke, Christian; Lee, Janey; Nath, Nandita Nature Protocols, Vol. 9, Issue 5 https://doi.org/10.1038/nprot.2014.067	journal	April 2014
Virus and prokaryote enumeration from planktonic aquatic environments by epifluorescence microscopy with SYBR Green I Patel, Anand; Noble, Rachel T.; Steele, Joshua A. Nature Protocols, Vol. 2, Issue 2 https://doi.org/10.1038/nprot.2007.6	journal	February 2007
An efficient algorithm for large-scale detection of protein families Enright, A. J. Nucleic Acids Research, Vol. 30, Issue 7 https://doi.org/10.1093/nar/30.7.1575	journal	April 2002
Viral dark matter and virus–host interactions resolved from publicly available microbial genomes Roux, Simon; Hallam, Steven J.; Woyke, Tanja eLife, Vol. 4 https://doi.org/10.7554/eLife.08490	journal	July 2015
vConTACT: an iVirus tool to classify double-stranded DNA viruses that infect Archaea and Bacteria Bolduc, Benjamin; Jang, Ho Bin; Doulcier, Guilhem PeerJ, Vol. 5 https://doi.org/10.7717/peerj.3243	journal	January 2017
Genomic island variability facilitates Prochlorococcus–virus coexistence Avrani, Sarit; Wurtzel, Omri; Sharon, Itai Nature, Vol. 474, Issue 7353 https://doi.org/10.1038/nature10172	journal	June 2011
Potential for Chemolithoautotrophy Among Ubiquitous Bacteria Lineages in the Dark Ocean Swan, B. K.; Martinez-Garcia, M.; Preston, C. M. Science, Vol. 333, Issue 6047 https://doi.org/10.1126/science.1203690	journal	September 2011
Insights into the phylogeny and coding potential of microbial dark matter Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12352	journal	July 2013
Virus-host swinging party in the oceans: Incorporating biological complexity into paradigms of antagonistic coexistence Avrani, Sarit; Schwartz, Daniel A.; Lindell, Debbie Mobile Genetic Elements, Vol. 2, Issue 2 https://doi.org/10.4161/mge.20031	journal	March 2012
Genomes of Abundant and Widespread Viruses from the Deep Ocean Mizuno, Carolina Megumi; Ghai, Rohit; Saghaï, Aurélien mBio, Vol. 7, Issue 4 https://doi.org/10.1128/mBio.00805-16	journal	July 2016
Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean Swan, B. K.; Tupper, B.; Sczyrba, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 28 https://doi.org/10.1073/pnas.1304246110	journal	June 2013
Expanding the Marine Virosphere Using Metagenomics Mizuno, Carolina Megumi; Rodriguez-Valera, Francisco; Kimes, Nikole E. PLoS Genetics, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pgen.1003987	journal	December 2013
Alignment-free $d_2^*$ oligonucleotide frequency dissimilarity measure improves prediction of hosts from metagenomically-derived viral sequences Ahlgren, Nathan A.; Ren, Jie; Lu, Yang Young Nucleic Acids Research, Vol. 45, Issue 1 https://doi.org/10.1093/nar/gkw1002	journal	November 2016
Improved Environmental Genomes via Integration of Metagenomic and Single-Cell Assemblies Mende, Daniel R.; Aylward, Frank O.; Eppley, John M. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00143	journal	February 2016
Marine viruses, a genetic reservoir revealed by targeted viromics Martínez, Joaquín Martínez; Swan, Brandon K.; Wilson, William H. The ISME Journal, Vol. 8, Issue 5 https://doi.org/10.1038/ismej.2013.214	journal	December 2013
High-throughput single-cell sequencing identifies photoheterotrophs and chemoautotrophs in freshwater bacterioplankton Martinez-Garcia, Manuel; Swan, Brandon K.; Poulton, Nicole J. The ISME Journal, Vol. 6, Issue 1 https://doi.org/10.1038/ismej.2011.84	journal	June 2011
Human oral viruses are personal, persistent and gender-consistent Abeles, Shira R.; Robles-Sikisaka, Refugio; Ly, Melissa The ISME Journal, Vol. 8, Issue 9 https://doi.org/10.1038/ismej.2014.31	journal	March 2014

Cited By (33)

Minimum Information about an Uncultivated Virus Genome (MIUViG) Roux, Simon; Adriaenssens, Evelien M.; Dutilh, Bas E. Nature Biotechnology, Vol. 37, Issue 1 https://doi.org/10.1038/nbt.4306	journal	December 2018
Low activity of lytic pelagiphages in coastal marine waters Alonso-Sáez, Laura; Morán, Xosé Anxelu G.; Clokie, Martha RJ The ISME Journal, Vol. 12, Issue 8 https://doi.org/10.1038/s41396-018-0185-y	journal	June 2018
Single-cell genomics uncover Pelagibacter as the putative host of the extremely abundant uncultured 37-F6 viral population in the ocean Martinez-Hernandez, Francisco; Fornas, Òscar; Lluesma Gomez, Monica The ISME Journal, Vol. 13, Issue 1 https://doi.org/10.1038/s41396-018-0278-7	journal	September 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
Phage puppet masters of the marine microbial realm Breitbart, Mya; Bonnain, Chelsea; Malki, Kema Nature Microbiology, Vol. 3, Issue 7 https://doi.org/10.1038/s41564-018-0166-y	journal	June 2018
Defining the human gut host–phage network through single-cell viral tagging Džunková, Mária; Low, Soo Jen; Daly, Joshua N. Nature Microbiology, Vol. 4, Issue 12 https://doi.org/10.1038/s41564-019-0526-2	journal	August 2019
Long-term stability and Red Queen-like strain dynamics in marine viruses Ignacio-Espinoza, J. Cesar; Ahlgren, Nathan A.; Fuhrman, Jed A. Nature Microbiology, Vol. 5, Issue 2 https://doi.org/10.1038/s41564-019-0628-x	journal	December 2019
Phage diversity, genomics and phylogeny Dion, Moïra B.; Oechslin, Frank; Moineau, Sylvain Nature Reviews Microbiology, Vol. 18, Issue 3 https://doi.org/10.1038/s41579-019-0311-5	journal	February 2020
Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks Bin Jang, Ho; Bolduc, Benjamin; Zablocki, Olivier Nature Biotechnology, Vol. 37, Issue 6 https://doi.org/10.1038/s41587-019-0100-8	journal	May 2019
Novel phage-host interactions and evolution as revealed by a cyanomyovirus isolated from an estuarine environment: An evolutionarily and ecologically new cyanophage Xu, Yongle; Zhang, Rui; Wang, Nannan Environmental Microbiology, Vol. 20, Issue 8 https://doi.org/10.1111/1462-2920.14326	journal	August 2018
Prokaryotic and viral community structure in the singular chaotropic salt lake Salar de Uyuni Ramos‐Barbero, María Dolores; Martínez, José M.; Almansa, Cristina Environmental Microbiology, Vol. 21, Issue 6 https://doi.org/10.1111/1462-2920.14549	journal	February 2019
Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake Okazaki, Yusuke; Nishimura, Yosuke; Yoshida, Takashi Environmental Microbiology, Vol. 21, Issue 12 https://doi.org/10.1111/1462-2920.14816	journal	September 2019
Ecogenomics of the SAR11 clade Haro‐Moreno, Jose M.; Rodriguez‐Valera, Francisco; Rosselli, Riccardo Environmental Microbiology, Vol. 22, Issue 5 https://doi.org/10.1111/1462-2920.14896	journal	December 2019
A vision for a ‘microbcentric’ future Cavicchioli, Ricardo Microbial Biotechnology, Vol. 12, Issue 1 https://doi.org/10.1111/1751-7915.13262	journal	April 2018
Absolute quantification of infecting viral particles by chip‐based digital polymerase chain reaction McMullen, Africa; Martinez‐Hernandez, Francisco; Martinez‐Garcia, Manuel Environmental Microbiology Reports https://doi.org/10.1111/1758-2229.12804	journal	November 2019
Diel cycling of the cosmopolitan abundant Pelagibacter virus 37‐F6: one of the most abundant viruses on earth Martinez‐Hernandez, Francisco; Luo, Elaine; Tominaga, Kento Environmental Microbiology Reports, Vol. 12, Issue 2 https://doi.org/10.1111/1758-2229.12825	journal	February 2020
Complete Genome Sequence of Sinorhizobium Phage ΦM6, the First Terrestrial Phage of a Marine Phage Group Brewer, Tess E.; Washburn, Brian K.; Lynn, Jason S. Microbiology Resource Announcements, Vol. 7, Issue 13 https://doi.org/10.1128/mra.01143-18	journal	October 2018
A Viral Ecogenomics Framework To Uncover the Secrets of Nature’s “Microbe Whisperers” Roux, Simon mSystems, Vol. 4, Issue 3 https://doi.org/10.1128/msystems.00111-19	journal	May 2019
Trends of Microdiversity Reveal Depth-Dependent Evolutionary Strategies of Viruses in the Mediterranean Coutinho, Felipe Hernandes; Rosselli, Riccardo; Rodríguez-Valera, Francisco mSystems, Vol. 4, Issue 6 https://doi.org/10.1128/msystems.00554-19	journal	November 2019
Studying the gut virome in the metagenomic era: challenges and perspectives Garmaeva, Sanzhima; Sinha, Trishla; Kurilshikov, Alexander BMC Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12915-019-0704-y	journal	October 2019
Charting the diversity of uncultured viruses of Archaea and Bacteria Coutinho, F. H.; Edwards, R. A.; Rodríguez-Valera, F. BMC Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12915-019-0723-8	journal	December 2019
Host-hijacking and planktonic piracy: how phages command the microbial high seas Warwick-Dugdale, Joanna; Buchholz, Holger H.; Allen, Michael J. Virology Journal, Vol. 16, Issue 1 https://doi.org/10.1186/s12985-019-1120-1	journal	February 2019
Phages infecting Faecalibacterium prausnitzii belong to novel viral genera that help to decipher intestinal viromes Cornuault, Jeffrey K.; Petit, Marie-Agnès; Mariadassou, Mahendra Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0452-1	journal	April 2018
Occurrence and seasonal dynamics of RNA viral genotypes in three contrasting temperate lakes Hewson, Ian; Bistolas, Kalia S. I.; Button, Jason B. PLOS ONE, Vol. 13, Issue 3 https://doi.org/10.1371/journal.pone.0194419	journal	March 2018
Parasite microbiome project: Grand challenges Dheilly, Nolwenn M.; Martínez Martínez, Joaquín; Rosario, Karyna PLOS Pathogens, Vol. 15, Issue 10 https://doi.org/10.1371/journal.ppat.1008028	journal	October 2019
A Review on Viral Metagenomics in Extreme Environments Dávila-Ramos, Sonia; Castelán-Sánchez, Hugo G.; Martínez-Ávila, Liliana Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02403	journal	October 2019
Deciphering the Human Virome with Single-Virus Genomics and Metagenomics de la Cruz Peña, Maria; Martinez-Hernandez, Francisco; Garcia-Heredia, Inmaculada Viruses, Vol. 10, Issue 3 https://doi.org/10.3390/v10030113	journal	March 2018
Viruses of Eukaryotic Algae: Diversity, Methods for Detection, and Future Directions Coy, Samantha; Gann, Eric; Pound, Helena Viruses, Vol. 10, Issue 9 https://doi.org/10.3390/v10090487	journal	September 2018
Benchmarking viromics: an in silico evaluation of metagenome-enabled estimates of viral community composition and diversity Roux, Simon; Emerson, Joanne B.; Eloe-Fadrosh, Emiley A. PeerJ, Vol. 5 https://doi.org/10.7717/peerj.3817	journal	January 2017
Proteorhodopsins dominate the expression of phototrophic mechanisms in seasonal and dynamic marine picoplankton communities Sieradzki, Ella T.; Fuhrman, Jed A.; Rivero-Calle, Sara PeerJ, Vol. 6 https://doi.org/10.7717/peerj.5798	journal	January 2018
Long-read viral metagenomics captures abundant and microdiverse viral populations and their niche-defining genomic islands Warwick-Dugdale, Joanna; Solonenko, Natalie; Moore, Karen PeerJ, Vol. 7 https://doi.org/10.7717/peerj.6800	journal	January 2019
Minimum information about an uncultivated virus genome (MIUVIG) Roux, Simon; Adriaenssens, Evelien M.; Dutilh, Bas E. ETH Zurich https://doi.org/10.3929/ethz-b-000315358	text	January 2019
Metagenomic Analysis of the Diversity of DNA Viruses in the Surface and Deep Sea of the South China Sea Liang, Yantao; Wang, Long; Wang, Zengmeng Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01951	journal	August 2019

Similar Records

VirION2: a short- and long-read sequencing and informatics workflow to study the genomic diversity of viruses in nature

Journal Article · Tue Mar 30 00:00:00 EDT 2021 · PeerJ · OSTI ID:1424950

Zablocki, Olivier; Michelsen, Michelle; Burris, Marie; +6 more

Towards optimized viral metagenomes for double-stranded and single-stranded DNA viruses from challenging soils

Journal Article · Sat Apr 06 00:00:00 EDT 2019 · OSTI ID:1424950

Trubl, Gareth; Roux, Simon; Solonenko, Natalie; +6 more