The Pacific Ocean Virome (POV): A Marine Viral Metagenomic Dataset and Associated Protein Clusters for Quantitative Viral Ecology

Hurwitz, Bonnie L.; Sullivan, Matthew B.

doi:10.1371/journal.pone.0057355

Title: The Pacific Ocean Virome (POV): A Marine Viral Metagenomic Dataset and Associated Protein Clusters for Quantitative Viral Ecology

Journal Article · Wed Feb 27 19:00:00 EST 2013 · PLoS ONE

DOI: https://doi.org/10.1371/journal.pone.0057355 · OSTI ID:1904076

Hurwitz, Bonnie L. ^[1]; Sullivan, Matthew B. ^[2]

Univ. of Arizona, Tucson, AZ (United States); OSTI
Univ. of Arizona, Tucson, AZ (United States)

Bacteria and their viruses (phage) are fundamental drivers of many ecosystem processes including global biogeochemistry and horizontal gene transfer. While databases and resources for studying function in uncultured bacterial communities are relatively advanced, many fewer exist for their viral counterparts. The issue is largely technical in that the majority (often 90%) of viral sequences are functionally ‘unknown’ making viruses a virtually untapped resource of functional and physiological information. Here, we provide a community resource that organizes this unknown sequence space into 27 K high confidence protein clusters using 32 viral metagenomes from four biogeographic regions in the Pacific Ocean that vary by season, depth, and proximity to land, and include some of the first deep pelagic ocean viral metagenomes. These protein clusters more than double currently available viral protein clusters, including those from environmental datasets. Further, a protein cluster guided analysis of functional diversity revealed that richness decreased (i) from deep to surface waters, (ii) from winter to summer, (iii) and with distance from shore in surface waters only. These data provide a framework from which to draw on for future metadata-enabled functional inquiries of the vast viral unknown.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Sponsoring Organization:: Gordon and Betty Moore Foundation; National Science Foundation (NSF); USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1904076

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 2 Vol. 8; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (109)

Ecology of prokaryotic viruses Weinbauer, Markus G. FEMS Microbiology Reviews, Vol. 28, Issue 2 https://doi.org/10.1016/j.femsre.2003.08.001	journal	May 2004
Spatial variability overwhelms seasonal patterns in bacterioplankton communities across a river to ocean gradient Fortunato, Caroline S.; Herfort, Lydie; Zuber, Peter The ISME Journal, Vol. 6, Issue 3 https://doi.org/10.1038/ismej.2011.135	journal	October 2011
The Western English Channel contains a persistent microbial seed bank Caporaso, J. Gregory; Paszkiewicz, Konrad; Field, Dawn The ISME Journal, Vol. 6, Issue 6 https://doi.org/10.1038/ismej.2011.162	journal	November 2011
Comparative metagenomics of microbial traits within oceanic viral communities Sharon, Itai; Battchikova, Natalia; Aro, Eva-Mari The ISME Journal, Vol. 5, Issue 7 https://doi.org/10.1038/ismej.2011.2	journal	February 2011
Diversity and population structure of Marine Group A bacteria in the Northeast subarctic Pacific Ocean Allers, Elke; Wright, Jody J.; Konwar, Kishori M. The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.108	journal	November 2012
Cyanophages infecting the oceanic cyanobacterium Prochlorococcus Sullivan, Matthew B.; Waterbury, John B.; Chisholm, Sallie W. Nature, Vol. 424, Issue 6952 https://doi.org/10.1038/nature01929	journal	August 2003
Functional metagenomic profiling of nine biomes Dinsdale, Elizabeth A.; Edwards, Robert A.; Hall, Dana Nature, Vol. 452, Issue 7187 https://doi.org/10.1038/nature06810	journal	March 2008
Viruses manipulate the marine environment Rohwer, Forest; Thurber, Rebecca Vega Nature, Vol. 459, Issue 7244 https://doi.org/10.1038/nature08060	journal	May 2009
Multiple displacement amplification compromises quantitative analysis of metagenomes Yilmaz, Suzan; Allgaier, Martin; Hugenholtz, Philip Nature Methods, Vol. 7, Issue 12 https://doi.org/10.1038/nmeth1210-943	journal	November 2010
Microbial diversity in the deep sea and the underexplored "rare biosphere" Sogin, M. L.; Morrison, H. G.; Huber, J. A. Proceedings of the National Academy of Sciences, Vol. 103, Issue 32 https://doi.org/10.1073/pnas.0605127103	journal	July 2006
Genomic analysis of uncultured marine viral communities Breitbart, M.; Salamon, P.; Andresen, B. Proceedings of the National Academy of Sciences, Vol. 99, Issue 22 https://doi.org/10.1073/pnas.202488399	journal	October 2002
Prokaryotes: The unseen majority Whitman, W. B.; Coleman, D. C.; Wiebe, W. J. Proceedings of the National Academy of Sciences, Vol. 95, Issue 12 https://doi.org/10.1073/pnas.95.12.6578	journal	June 1998
IMG ER: a system for microbial genome annotation expert review and curation Markowitz, Victor M.; Mavromatis, Konstantinos; Ivanova, Natalia N. Bioinformatics, Vol. 25, Issue 17 https://doi.org/10.1093/bioinformatics/btp393	journal	June 2009
Metavir: a web server dedicated to virome analysis Roux, Simon; Faubladier, Michaël; Mahul, Antoine Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr519	journal	September 2011
Real Time Metagenomics: Using k-mers to annotate metagenomes Edwards, Robert A.; Olson, Robert; Disz, Terry Bioinformatics, Vol. 28, Issue 24 https://doi.org/10.1093/bioinformatics/bts599	journal	October 2012
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
SIMAP: the similarity matrix of proteins Rattei, T. Nucleic Acids Research, Vol. 34, Issue 90001 https://doi.org/10.1093/nar/gkj106	journal	January 2006
Diversity and population structure of a near–shore marine–sediment viral community Breitbart, Mya; Felts, Ben; Kelley, Scott Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 271, Issue 1539 https://doi.org/10.1098/rspb.2003.2628	journal	March 2004
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs Zerbino, D. R.; Birney, E. Genome Research, Vol. 18, Issue 5 https://doi.org/10.1101/gr.074492.107	journal	February 2008
Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen Hess, M.; Sczyrba, A.; Egan, R. Science, Vol. 331, Issue 6016 https://doi.org/10.1126/science.1200387	journal	January 2011
Amplification of Uncultured Single-Stranded DNA Viruses from Rice Paddy Soil Kim, K. -H.; Chang, H. -W.; Nam, Y. -D. Applied and Environmental Microbiology, Vol. 74, Issue 19 https://doi.org/10.1128/aem.01275-08	journal	August 2008
Occurrence and Expression of Gene Transfer Agent Genes in Marine Bacterioplankton Biers, Erin J.; Wang, Kui; Pennington, Catherine Applied and Environmental Microbiology, Vol. 74, Issue 10 https://doi.org/10.1128/aem.02129-07	journal	May 2008
Cultivated Single-Stranded DNA Phages That Infect Marine Bacteroidetes Prove Difficult To Detect with DNA-Binding Stains Holmfeldt, Karin; Odić, Duško; Sullivan, Matthew B. Applied and Environmental Microbiology, Vol. 78, Issue 3 https://doi.org/10.1128/aem.06580-11	journal	December 2011
Resistance to Co-Occurring Phages Enables Marine Synechococcus Communities To Coexist with Cyanophages Abundant in Seawater † Waterbury, John B.; Valois, Frederica W. Applied and Environmental Microbiology, Vol. 59, Issue 10 https://doi.org/10.1128/aem.59.10.3393-3399.1993	journal	January 1993
Dynamics and Distribution of Cyanophages and Their Effect on Marine Synechococcus spp. † Suttle, Curtis A.; Chan, Amy M. Applied and Environmental Microbiology, Vol. 60, Issue 9 https://doi.org/10.1128/aem.60.9.3167-3174.1994	journal	January 1994
Distribution, Isolation, Host Specificity, and Diversity of Cyanophages Infecting Marine Synechococcus spp. in River Estuaries Lu, Jingrang; Chen, Feng; Hodson, Robert E. Applied and Environmental Microbiology, Vol. 67, Issue 7 https://doi.org/10.1128/aem.67.7.3285-3290.2001	journal	July 2001
Virioplankton: Viruses in Aquatic Ecosystems Wommack, K. E.; Colwell, R. R. Microbiology and Molecular Biology Reviews, Vol. 64, Issue 1 https://doi.org/10.1128/mmbr.64.1.69-114.2000	journal	March 2000
Metagenomics: Application of Genomics to Uncultured Microorganisms Handelsman, J. Microbiology and Molecular Biology Reviews, Vol. 68, Issue 4 https://doi.org/10.1128/mmbr.68.4.669-685.2004	journal	December 2004
The Uncultured Microbial Majority Rappé, Michael S.; Giovannoni, Stephen J. Annual Review of Microbiology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.micro.57.030502.090759	journal	October 2003
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
Gene identification and protein classification in microbial metagenomic sequence data via incremental clustering Yooseph, Shibu; Li, Weizhong; Sutton, Granger BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-182	journal	April 2008
The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes Meyer, F.; Paarmann, D.; D'Souza, M. BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-386	journal	September 2008
Metagenomics Offers a Big-Picture View of the Diversity and Distribution of Marine Viruses Hoff, Mary PLoS Biology, Vol. 4, Issue 11 https://doi.org/10.1371/journal.pbio.0040406	journal	November 2006
A Holistic Approach to Marine Eco-Systems Biology Karsenti, Eric; Acinas, Silvia G.; Bork, Peer PLoS Biology, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pbio.1001177	journal	October 2011
Metagenomic Analysis of Lysogeny in Tampa Bay: Implications for Prophage Gene Expression McDaniel, Lauren; Breitbart, Mya; Mobberley, Jennifer PLoS ONE, Vol. 3, Issue 9 https://doi.org/10.1371/journal.pone.0003263	journal	September 2008
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
Exploring the Vast Diversity of Marine Viruses Breitbart, Mya; Thompson, Luke; Suttle, Curtis Oceanography, Vol. 20, Issue 2 https://doi.org/10.5670/oceanog.2007.58	journal	June 2007
Seasonal fluctuations of temperature, salinity, nitrate, chlorophyll and primary production at station H3/M1 over 1989–1996 in Monterey Bay, California Timothy Pennington, J.; Chavez, Francisco P. Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 47, Issue 5-6 https://doi.org/10.1016/S0967-0645(99)00132-0	journal	May 2000
Prophage-like gene transfer agents—Novel mechanisms of gene exchange for Methanococcus, Desulfovibrio, Brachyspira, and Rhodobacter species Stanton, Thad B. Anaerobe, Vol. 13, Issue 2 https://doi.org/10.1016/j.anaerobe.2007.03.004	journal	April 2007
Ecology of prokaryotic viruses Weinbauer, Markus G. FEMS Microbiology Reviews, Vol. 28, Issue 2 https://doi.org/10.1016/j.femsre.2003.08.001	journal	May 2004
Persistently declining oxygen levels in the interior waters of the eastern subarctic Pacific Whitney, Frank A.; Freeland, Howard J.; Robert, Marie Progress in Oceanography, Vol. 75, Issue 2 https://doi.org/10.1016/j.pocean.2007.08.007	journal	October 2007
Importance of widespread gene transfer agent genes in α-proteobacteria Lang, Andrew S.; Beatty, J. Thomas Trends in Microbiology, Vol. 15, Issue 2 https://doi.org/10.1016/j.tim.2006.12.001	journal	February 2007
Ocean viruses: Rigorously evaluating the metagenomic sample-to-sequence pipeline Duhaime, Melissa B.; Sullivan, Matthew B. Virology, Vol. 434, Issue 2 https://doi.org/10.1016/j.virol.2012.09.036	journal	December 2012
Marine viruses and their biogeochemical and ecological effects Fuhrman, Jed A. Nature, Vol. 399, Issue 6736 https://doi.org/10.1038/21119	journal	June 1999
Lysogenic virus–host interactions predominate at deep-sea diffuse-flow hydrothermal vents Williamson, Shannon J.; Cary, S. Craig; Williamson, Kurt E. The ISME Journal, Vol. 2, Issue 11 https://doi.org/10.1038/ismej.2008.73	journal	August 2008
Spatial variability overwhelms seasonal patterns in bacterioplankton communities across a river to ocean gradient Fortunato, Caroline S.; Herfort, Lydie; Zuber, Peter The ISME Journal, Vol. 6, Issue 3 https://doi.org/10.1038/ismej.2011.135	journal	October 2011
The Western English Channel contains a persistent microbial seed bank Caporaso, J. Gregory; Paszkiewicz, Konrad; Field, Dawn The ISME Journal, Vol. 6, Issue 6 https://doi.org/10.1038/ismej.2011.162	journal	November 2011
Comparative metagenomics of microbial traits within oceanic viral communities Sharon, Itai; Battchikova, Natalia; Aro, Eva-Mari The ISME Journal, Vol. 5, Issue 7 https://doi.org/10.1038/ismej.2011.2	journal	February 2011
Diversity and population structure of Marine Group A bacteria in the Northeast subarctic Pacific Ocean Allers, Elke; Wright, Jody J.; Konwar, Kishori M. The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.108	journal	November 2012
Cyanophages infecting the oceanic cyanobacterium Prochlorococcus Sullivan, Matthew B.; Waterbury, John B.; Chisholm, Sallie W. Nature, Vol. 424, Issue 6952 https://doi.org/10.1038/nature01929	journal	August 2003
Community structure and metabolism through reconstruction of microbial genomes from the environment Tyson, Gene W.; Chapman, Jarrod; Hugenholtz, Philip Nature, Vol. 428, Issue 6978 https://doi.org/10.1038/nature02340	journal	February 2004
Functional metagenomic profiling of nine biomes Dinsdale, Elizabeth A.; Edwards, Robert A.; Hall, Dana Nature, Vol. 452, Issue 7187 https://doi.org/10.1038/nature06810	journal	March 2008
Viruses manipulate the marine environment Rohwer, Forest; Thurber, Rebecca Vega Nature, Vol. 459, Issue 7244 https://doi.org/10.1038/nature08060	journal	May 2009
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
Multiple displacement amplification compromises quantitative analysis of metagenomes Yilmaz, Suzan; Allgaier, Martin; Hugenholtz, Philip Nature Methods, Vol. 7, Issue 12 https://doi.org/10.1038/nmeth1210-943	journal	November 2010
Laboratory procedures to generate viral metagenomes Thurber, Rebecca V.; Haynes, Matthew; Breitbart, Mya Nature Protocols, Vol. 4, Issue 4 https://doi.org/10.1038/nprot.2009.10	journal	March 2009
Viral metagenomics Edwards, Robert A.; Rohwer, Forest Nature Reviews Microbiology, Vol. 3, Issue 6 https://doi.org/10.1038/nrmicro1163	journal	May 2005
Microbial diversity in the deep sea and the underexplored "rare biosphere" Sogin, M. L.; Morrison, H. G.; Huber, J. A. Proceedings of the National Academy of Sciences, Vol. 103, Issue 32 https://doi.org/10.1073/pnas.0605127103	journal	July 2006
Genomic analysis of uncultured marine viral communities Breitbart, M.; Salamon, P.; Andresen, B. Proceedings of the National Academy of Sciences, Vol. 99, Issue 22 https://doi.org/10.1073/pnas.202488399	journal	October 2002
Prokaryotes: The unseen majority Whitman, W. B.; Coleman, D. C.; Wiebe, W. J. Proceedings of the National Academy of Sciences, Vol. 95, Issue 12 https://doi.org/10.1073/pnas.95.12.6578	journal	June 1998
IMG ER: a system for microbial genome annotation expert review and curation Markowitz, Victor M.; Mavromatis, Konstantinos; Ivanova, Natalia N. Bioinformatics, Vol. 25, Issue 17 https://doi.org/10.1093/bioinformatics/btp393	journal	June 2009
Metavir: a web server dedicated to virome analysis Roux, Simon; Faubladier, Michaël; Mahul, Antoine Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr519	journal	September 2011
Real Time Metagenomics: Using k-mers to annotate metagenomes Edwards, Robert A.; Olson, Robert; Disz, Terry Bioinformatics, Vol. 28, Issue 24 https://doi.org/10.1093/bioinformatics/bts599	journal	October 2012
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
SIMAP: the similarity matrix of proteins Rattei, T. Nucleic Acids Research, Vol. 34, Issue 90001 https://doi.org/10.1093/nar/gkj106	journal	January 2006
Diversity and population structure of a near–shore marine–sediment viral community Breitbart, Mya; Felts, Ben; Kelley, Scott Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 271, Issue 1539 https://doi.org/10.1098/rspb.2003.2628	journal	March 2004
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs Zerbino, D. R.; Birney, E. Genome Research, Vol. 18, Issue 5 https://doi.org/10.1101/gr.074492.107	journal	February 2008
Single-cell and population level viral infection dynamics revealed by phageFISH, a method to visualize intracellular and free viruses: phageFISH - visualizing intracellular and free viruses Allers, Elke; Moraru, Cristina; Duhaime, Melissa B. Environmental Microbiology, Vol. 15, Issue 8 https://doi.org/10.1111/1462-2920.12100	journal	March 2013
Towards quantitative metagenomics of wild viruses and other ultra-low concentration DNA samples: a rigorous assessment and optimization of the linker amplification method: Linker amplification for ultra-low DNA samples Duhaime, Melissa B.; Deng, Li; Poulos, Bonnie T. Environmental Microbiology, Vol. 14, Issue 9 https://doi.org/10.1111/j.1462-2920.2012.02791.x	journal	June 2012
Evaluation of methods to concentrate and purify ocean virus communities through comparative, replicated metagenomics: Viral community concentration and purification Hurwitz, Bonnie L.; Deng, Li; Poulos, Bonnie T. Environmental Microbiology, Vol. 15, Issue 5 https://doi.org/10.1111/j.1462-2920.2012.02836.x	journal	July 2012
A simple and efficient method for concentration of ocean viruses by chemical flocculation: Virus concentration by flocculation with iron John, Seth G.; Mendez, Carolina B.; Deng, Li Environmental Microbiology Reports, Vol. 3, Issue 2 https://doi.org/10.1111/j.1758-2229.2010.00208.x	journal	August 2010
Environmental Genome Shotgun Sequencing of the Sargasso Sea Venter, J. C. Science, Vol. 304, Issue 5667 https://doi.org/10.1126/science.1093857	journal	April 2004
Metagenomic Analysis of Coastal RNA Virus Communities Culley, A. I. Science, Vol. 312, Issue 5781 https://doi.org/10.1126/science.1127404	journal	June 2006
The Microbial Engines That Drive Earth's Biogeochemical Cycles Falkowski, P. G.; Fenchel, T.; Delong, E. F. Science, Vol. 320, Issue 5879 https://doi.org/10.1126/science.1153213	journal	May 2008
Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen Hess, M.; Sczyrba, A.; Egan, R. Science, Vol. 331, Issue 6016 https://doi.org/10.1126/science.1200387	journal	January 2011
Probing Individual Environmental Bacteria for Viruses by Using Microfluidic Digital PCR Tadmor, A. D.; Ottesen, E. A.; Leadbetter, J. R. Science, Vol. 333, Issue 6038 https://doi.org/10.1126/science.1200758	journal	June 2011
A Molecular View of Microbial Diversity and the Biosphere Pace, N. R. Science, Vol. 276, Issue 5313, p. 734-740 https://doi.org/10.1126/science.276.5313.734	journal	May 1997
Hydroxyapatite-Mediated Separation of Double-Stranded DNA, Single-Stranded DNA, and RNA Genomes from Natural Viral Assemblages Andrews-Pfannkoch, C.; Fadrosh, D. W.; Thorpe, J. Applied and Environmental Microbiology, Vol. 76, Issue 15 https://doi.org/10.1128/AEM.00204-10	journal	June 2010
Amplification Methods Bias Metagenomic Libraries of Uncultured Single-Stranded and Double-Stranded DNA Viruses Kim, Kyoung-Ho; Bae, Jin-Woo Applied and Environmental Microbiology, Vol. 77, Issue 21 https://doi.org/10.1128/AEM.00289-11	journal	September 2011
Metagenomic Characterization of Chesapeake Bay Virioplankton Bench, Shellie R.; Hanson, Thomas E.; Williamson, Kurt E. Applied and Environmental Microbiology, Vol. 73, Issue 23 https://doi.org/10.1128/AEM.00938-07	journal	October 2007
Amplification of Uncultured Single-Stranded DNA Viruses from Rice Paddy Soil Kim, K. -H.; Chang, H. -W.; Nam, Y. -D. Applied and Environmental Microbiology, Vol. 74, Issue 19 https://doi.org/10.1128/AEM.01275-08	journal	August 2008
Occurrence and Expression of Gene Transfer Agent Genes in Marine Bacterioplankton Biers, Erin J.; Wang, Kui; Pennington, Catherine Applied and Environmental Microbiology, Vol. 74, Issue 10 https://doi.org/10.1128/AEM.02129-07	journal	May 2008
Cultivated Single-Stranded DNA Phages That Infect Marine Bacteroidetes Prove Difficult To Detect with DNA-Binding Stains Holmfeldt, Karin; Odić, Duško; Sullivan, Matthew B. Applied and Environmental Microbiology, Vol. 78, Issue 3 https://doi.org/10.1128/AEM.06580-11	journal	December 2011
Resistance to Co-Occurring Phages Enables Marine Synechococcus Communities To Coexist with Cyanophages Abundant in Seawater † Waterbury, John B.; Valois, Frederica W. Applied and Environmental Microbiology, Vol. 59, Issue 10 https://doi.org/10.1128/AEM.59.10.3393-3399.1993	journal	January 1993
Dynamics and Distribution of Cyanophages and Their Effect on Marine Synechococcus spp. † Suttle, Curtis A.; Chan, Amy M. Applied and Environmental Microbiology, Vol. 60, Issue 9 https://doi.org/10.1128/AEM.60.9.3167-3174.1994	journal	January 1994
Distribution, Isolation, Host Specificity, and Diversity of Cyanophages Infecting Marine Synechococcus spp. in River Estuaries Lu, Jingrang; Chen, Feng; Hodson, Robert E. Applied and Environmental Microbiology, Vol. 67, Issue 7 https://doi.org/10.1128/AEM.67.7.3285-3290.2001	journal	July 2001
Virioplankton: Viruses in Aquatic Ecosystems Wommack, K. E.; Colwell, R. R. Microbiology and Molecular Biology Reviews, Vol. 64, Issue 1 https://doi.org/10.1128/MMBR.64.1.69-114.2000	journal	March 2000
Metagenomics: Application of Genomics to Uncultured Microorganisms Handelsman, J. Microbiology and Molecular Biology Reviews, Vol. 68, Issue 4 https://doi.org/10.1128/MMBR.68.4.669-685.2004	journal	December 2004
Contrasting Life Strategies of Viruses that Infect Photo- and Heterotrophic Bacteria, as Revealed by Viral Tagging Deng, Li; Gregory, Ann; Yilmaz, Suzan mBio, Vol. 3, Issue 6 https://doi.org/10.1128/mBio.00373-12	journal	October 2012
Marine Viruses: Truth or Dare Breitbart, Mya Annual Review of Marine Science, Vol. 4, Issue 1 https://doi.org/10.1146/annurev-marine-120709-142805	journal	January 2012
The Uncultured Microbial Majority Rappé, Michael S.; Giovannoni, Stephen J. Annual Review of Microbiology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.micro.57.030502.090759	journal	October 2003
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
Artificial and natural duplicates in pyrosequencing reads of metagenomic data Niu, Beifang; Fu, Limin; Sun, Shulei BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-187	journal	January 2010
Gene identification and protein classification in microbial metagenomic sequence data via incremental clustering Yooseph, Shibu; Li, Weizhong; Sutton, Granger BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-182	journal	April 2008
The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes Meyer, F.; Paarmann, D.; D'Souza, M. BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-386	journal	September 2008
Analysis of a viral metagenomic library from 200 m depth in Monterey Bay, California constructed by direct shotgun cloning Steward, Grieg F.; Preston, Christina M. Virology Journal, Vol. 8, Issue 1 https://doi.org/10.1186/1743-422X-8-287	journal	June 2011
Accuracy and quality of massively parallel DNA pyrosequencing Huse, Susan M.; Huber, Julie A.; Morrison, Hilary G. Genome Biology, Vol. 8, Issue 7 https://doi.org/10.1186/gb-2007-8-7-r143	journal	January 2007
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
The Sorcerer II Global Ocean Sampling Expedition: Expanding the Universe of Protein Families Yooseph, Shibu; Sutton, Granger; Rusch, Douglas B. PLoS Biology, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pbio.0050016	journal	March 2007
The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific Rusch, Douglas B.; Halpern, Aaron L.; Sutton, Granger PLoS Biology, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pbio.0050077	journal	March 2007
A Holistic Approach to Marine Eco-Systems Biology Karsenti, Eric; Acinas, Silvia G.; Bork, Peer PLoS Biology, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pbio.1001177	journal	October 2011
The Sorcerer II Global Ocean Sampling Expedition: Metagenomic Characterization of Viruses within Aquatic Microbial Samples Williamson, Shannon J.; Rusch, Douglas B.; Yooseph, Shibu PLoS ONE, Vol. 3, Issue 1 https://doi.org/10.1371/journal.pone.0001456	journal	January 2008
Metagenomic Analysis of Lysogeny in Tampa Bay: Implications for Prophage Gene Expression McDaniel, Lauren; Breitbart, Mya; Mobberley, Jennifer PLoS ONE, Vol. 3, Issue 9 https://doi.org/10.1371/journal.pone.0003263	journal	September 2008
Analysis of High-Throughput Sequencing and Annotation Strategies for Phage Genomes Henn, Matthew R.; Sullivan, Matthew B.; Stange-Thomann, Nicole PLoS ONE, Vol. 5, Issue 2 https://doi.org/10.1371/journal.pone.0009083	journal	February 2010
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
Assessing the Diversity and Specificity of Two Freshwater Viral Communities through Metagenomics Roux, Simon; Enault, Francois; Robin, Agnès PLoS ONE, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pone.0033641	journal	March 2012
Temporal variability in nitrification rates and related biogeochemical factors in Monterey Bay, California, USA Ward, Bb Marine Ecology Progress Series, Vol. 292 https://doi.org/10.3354/meps292097	journal	January 2005
VIROME: a standard operating procedure for analysis of viral metagenome sequences Wommack, K. Eric; Bhavsar, Jaysheel; Polson, Shawn W. Standards in Genomic Sciences, Vol. 6, Issue 3 https://doi.org/10.4056/sigs.2945050	journal	July 2012
Exploring the Vast Diversity of Marine Viruses Breitbart, Mya; Thompson, Luke; Suttle, Curtis Oceanography, Vol. 20, Issue 2 https://doi.org/10.5670/oceanog.2007.58	journal	June 2007

Cited By (54)

Combining metagenomics, metatranscriptomics and viromics to explore novel microbial interactions: towards a systems-level understanding of human microbiome Bikel, Shirley; Valdez-Lara, Alejandra; Cornejo-Granados, Fernanda Computational and Structural Biotechnology Journal, Vol. 13 https://doi.org/10.1016/j.csbj.2015.06.001	journal	January 2015
Assessing Species Diversity Using Metavirome Data: Methods and Challenges Herath, Damayanthi; Jayasundara, Duleepa; Ackland, David Computational and Structural Biotechnology Journal, Vol. 15 https://doi.org/10.1016/j.csbj.2017.09.001	journal	January 2017
Seasonal time bombs: dominant temperate viruses affect Southern Ocean microbial dynamics Brum, Jennifer R.; Hurwitz, Bonnie L.; Schofield, Oscar The ISME Journal, Vol. 10, Issue 2 https://doi.org/10.1038/ismej.2015.125	journal	August 2015
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
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
Cyanophage-encoded lipid desaturases: oceanic distribution, diversity and function Roitman, Sheila; Hornung, Ellen; Flores-Uribe, José The ISME Journal, Vol. 12, Issue 2 https://doi.org/10.1038/ismej.2017.159	journal	October 2017
Assessing viral taxonomic composition in benthic marine ecosystems: reliability and efficiency of different bioinformatic tools for viral metagenomic analyses Tangherlini, M.; Dell’Anno, A.; Zeigler Allen, L. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep28428	journal	June 2016
Deep sequencing analysis of viral infection and evolution allows rapid and detailed characterization of viral mutant spectrum Isakov, Ofer; Bordería, Antonio V.; Golan, David Bioinformatics, Vol. 31, Issue 13 https://doi.org/10.1093/bioinformatics/btv101	journal	February 2015
EXTRACT: interactive extraction of environment metadata and term suggestion for metagenomic sample annotation Pafilis, Evangelos; Buttigieg, Pier Luigi; Ferrell, Barbra Database, Vol. 2016 https://doi.org/10.1093/database/baw005	journal	January 2016
Bacteriophage strain typing by rapid single molecule analysis Grunwald, Assaf; Dahan, Moran; Giesbertz, Anna Nucleic Acids Research, Vol. 43, Issue 18 https://doi.org/10.1093/nar/gkv563	journal	May 2015
Biodiversity and distribution of polar freshwater DNA viruses Aguirre de Cárcer, Daniel; López-Bueno, Alberto; Pearce, David A. Science Advances, Vol. 1, Issue 5 https://doi.org/10.1126/sciadv.1400127	journal	June 2015
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
Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean Nishimura, Yosuke; Watai, Hiroyasu; Honda, Takashi mSphere, Vol. 2, Issue 2 https://doi.org/10.1128/msphere.00359-16	journal	March 2017
Comparison of different assembly and annotation tools on analysis of simulated viral metagenomic communities in the gut Vázquez-Castellanos, Jorge F.; García-López, Rodrigo; Pérez-Brocal, Vicente BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-37	journal	January 2014
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
Genomic, proteomic and bioinformatic analysis of two temperate phages in Roseobacter clade bacteria isolated from the deep-sea water Tang, Kai; Lin, Dan; Zheng, Qiang BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-3886-0	journal	June 2017
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
Complete genome sequences of bacteriophages P12002L and P12002S, two lytic phages that infect a marine Polaribacter strain Kang, Ilnam; Jang, Hani; Cho, Jang-Cheon Standards in Genomic Sciences, Vol. 10, Issue 1 https://doi.org/10.1186/s40793-015-0076-z	journal	October 2015
Complete genome sequence of Paracoccus marcusii phage vB_PmaS-R3 isolated from the South China Sea Xu, Yongle; Zhang, Rui; Jiao, Nianzhi Standards in Genomic Sciences, Vol. 10, Issue 1 https://doi.org/10.1186/s40793-015-0089-7	journal	November 2015
Complete genome sequence of bacteriophage P8625, the first lytic phage that infects Verrucomicrobia Choi, Ahyoung; Kang, Ilnam; Yang, Seung-Jo Standards in Genomic Sciences, Vol. 10, Issue 1 https://doi.org/10.1186/s40793-015-0091-0	journal	November 2015
Complete genome sequence of Pseudoalteromonas phage vB_PspS-H40/1 (formerly H40/1) that infects Pseudoalteromonas sp. strain H40 and is used as biological tracer in hydrological transport studies Kallies, René; Kiesel, Bärbel; Schmidt, Matthias Standards in Genomic Sciences, Vol. 12, Issue 1 https://doi.org/10.1186/s40793-017-0235-5	journal	February 2017
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
Genome diversity of marine phages recovered from Mediterranean metagenomes: Size matters López-Pérez, Mario; Haro-Moreno, Jose M.; Gonzalez-Serrano, Rafael PLOS Genetics, Vol. 13, Issue 9 https://doi.org/10.1371/journal.pgen.1007018	journal	September 2017
Life-Style and Genome Structure of Marine Pseudoalteromonas Siphovirus B8b Isolated from the Northwestern Mediterranean Sea Lara, Elena; Holmfeldt, Karin; Solonenko, Natalie PLOS ONE, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pone.0114829	journal	January 2015
Transporting Ocean Viromes: Invasion of the Aquatic Biosphere Kim, Yiseul; Aw, Tiong Gim; Rose, Joan B. PLOS ONE, Vol. 11, Issue 4 https://doi.org/10.1371/journal.pone.0152671	journal	April 2016
Diversity in a Polymicrobial Community Revealed by Analysis of Viromes, Endolysins and CRISPR Spacers Davison, Michelle; Treangen, Todd J.; Koren, Sergey PLOS ONE, Vol. 11, Issue 9 https://doi.org/10.1371/journal.pone.0160574	journal	September 2016
Gut Bacteriophage: Current Understanding and Challenges Sutton, Thomas D. S.; Hill, Colin Frontiers in Endocrinology, Vol. 10 https://doi.org/10.3389/fendo.2019.00784	journal	November 2019
New perspectives in benthic deep-sea microbial ecology Corinaldesi, Cinzia Frontiers in Marine Science, Vol. 2 https://doi.org/10.3389/fmars.2015.00017	journal	March 2015
Bridging the Gap between Knowing and Modeling Viruses in Marine Systems—An Upcoming Frontier Mateus, Marcos D. Frontiers in Marine Science, Vol. 3 https://doi.org/10.3389/fmars.2016.00284	journal	January 2017
Replicating phages in the epidermal mucosa of the eel (Anguilla anguilla) Carda-DiÃ©guez, Miguel; Mizuno, Carolina Megumi; Ghai, Rohit Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00003	journal	January 2015
Genomic characteristics and environmental distributions of the uncultivated Far-T4 phages Roux, Simon; Enault, François; Ravet, Viviane Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00199	journal	March 2015
Beyond research: a primer for considerations on using viral metagenomics in the field and clinic Hall, Richard J.; Draper, Jenny L.; Nielsen, Fiona G. G. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00224	journal	March 2015
Expanding our Understanding of the Seaweed Holobiont: RNA Viruses of the Red Alga Delisea pulchra Lachnit, Tim; Thomas, Torsten; Steinberg, Peter Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01489	journal	January 2016
Abundance of Two Pelagibacter ubique Bacteriophage Genotypes along a Latitudinal Transect in the North and South Atlantic Oceans Eggleston, Erin M.; Hewson, Ian Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01534	journal	September 2016
Ultrastructure and Viral Metagenome of Bacteriophages from an Anaerobic Methane Oxidizing Methylomirabilis Bioreactor Enrichment Culture Gambelli, Lavinia; Cremers, Geert; Mesman, Rob Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01740	journal	November 2016
Environmental Viral Metagenomics Analyses in Aquaculture: Applications in Epidemiology and Disease Control Munang’andu, Hetron M. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01986	journal	December 2016
Phylogenetic Diversity of T4-Type Phages in Sediments from the Subtropical Pearl River Estuary He, Maoqiu; Cai, Lanlan; Zhang, Chuanlun Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00897	journal	May 2017
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
Evaluation of Sequencing Library Preparation Protocols for Viral Metagenomic Analysis from Pristine Aquifer Groundwaters Kallies, René; Hölzer, Martin; Brizola Toscan, Rodolfo Viruses, Vol. 11, Issue 6 https://doi.org/10.3390/v11060484	journal	May 2019
A Novel Benthic Phage Infecting Shewanella with Strong Replication Ability Wang, Zengmeng; Zhao, Jiulong; Wang, Long Viruses, Vol. 11, Issue 11 https://doi.org/10.3390/v11111081	journal	November 2019
Metagenomic Analysis of Virioplankton of the Subtropical Jiulong River Estuary, China Cai, Lanlan; Zhang, Rui; He, Ying Viruses, Vol. 8, Issue 2 https://doi.org/10.3390/v8020035	journal	February 2016
A Pelagic Microbiome (Viruses to Protists) from a Small Cup of Seawater Flaviani, Flavia; Schroeder, Declan; Balestreri, Cecilia Viruses, Vol. 9, Issue 3 https://doi.org/10.3390/v9030047	journal	March 2017
Metagenomic Approaches to Assess Bacteriophages in Various Environmental Niches Hayes, Stephen; Mahony, Jennifer; Nauta, Arjen Viruses, Vol. 9, Issue 6 https://doi.org/10.3390/v9060127	journal	May 2017
Marine Viruses: Key Players in Marine Ecosystems Middelboe, Mathias; Brussaard, Corina Viruses, Vol. 9, Issue 10 https://doi.org/10.3390/v9100302	journal	October 2017
A Polyglot Approach to Bioinformatics Data Integration: A Phylogenetic Analysis of HIV-1 Reisman, Steven; Hatzopoulos, Thomas; Läufer, Konstantin Evolutionary Bioinformatics, Vol. 12 https://doi.org/10.4137/ebo.s32757	journal	January 2016
Additional file 1 of Characterization and genomic analysis of the first Oceanospirillum phage, vB_OliS_GJ44, representing a novel siphoviral cluster Zhang, Wenjing; Liang, Yantao; Zheng, Kaiyang figshare https://doi.org/10.6084/m9.figshare.16650395	dataset	January 2021
Additional file 2 of Characterization and genomic analysis of the first Oceanospirillum phage, vB_OliS_GJ44, representing a novel siphoviral cluster Zhang, Wenjing; Liang, Yantao; Zheng, Kaiyang figshare https://doi.org/10.6084/m9.figshare.16650398.v1	dataset	January 2021
Additional file 1 of Giant viral signatures on the Greenland ice sheet Perini, Laura; Sipes, Katie; Zervas, Athanasios figshare https://doi.org/10.6084/m9.figshare.25853006.v1	dataset	January 2024
Gene swapping in the dead zone Petersen, Jillian; Dubilier, Nicole eLife, Vol. 3 https://doi.org/10.7554/elife.04600	journal	October 2014
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
Optimization of viral resuspension methods for carbon-rich soils along a permafrost thaw gradient Trubl, Gareth; Solonenko, Natalie; Chittick, Lauren PeerJ, Vol. 4 https://doi.org/10.7717/peerj.1999	journal	January 2016
Assessing Illumina technology for the high-throughput sequencing of bacteriophage genomes Rihtman, Branko; Meaden, Sean; Clokie, Martha R. J. PeerJ, Vol. 4 https://doi.org/10.7717/peerj.2055	journal	June 2016
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
Deep sequencing of the viral phoH gene reveals temporal variation, depth-specific composition, and persistent dominance of the same viral phoH genes in the Sargasso Sea Goldsmith, Dawn B.; Parsons, Rachel J.; Beyene, Damitu PeerJ, Vol. 3 https://doi.org/10.7717/peerj.997	journal	January 2015

Similar Records

Uncultivated Viral Populations Dominate Estuarine Viromes on the Spatiotemporal Scale

Journal Article · Mon Mar 15 20:00:00 EDT 2021 · mSystems · OSTI ID:1904067

Sun, Mengqi; Zhan, Yuanchao; Marsan, David; +3 more

Integrating Viral Metagenomics into an Ecological Framework

Journal Article · Mon May 24 20:00:00 EDT 2021 · Annual review of virology · OSTI ID:1811750

Sommers, Pacifica; Chatterjee, Anushila; Varsani, Arvind; +1 more

A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes

Journal Article · Wed Jul 23 20:00:00 EDT 2014 · Nature Communications · OSTI ID:1623951

Dutilh, Bas E.; Cassman, Noriko; McNair, Katelyn; +11 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Pacific Ocean
bacteriophages
gene prediction
marine ecology
metagenomics
oceans
spring
taxonomy

Title: The Pacific Ocean Virome (POV): A Marine Viral Metagenomic Dataset and Associated Protein Clusters for Quantitative Viral Ecology

Citation Formats

References (109)

Cited By (54)

Similar Records

Related Subjects