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Courtesy of Caltech Information Science and Technology Initiative – Wierman Cray 2 Supercomputer

Grants List


Courtesy of Amy M. Chan, University of British Columbia - marine phages

Broad Institute

Marine Phage, Virus and Virome Sequencing Pipeline

To support the Broad Institute to sequence and perform initial characterizations of marine phage and virus genomes and the genomic content of environmental marine virus assemblages.

Title: Marine Phage, Virus and Virome Sequencing Pipeline
Date Awarded: Nov 2008
Amount: $1,848,572
Term: 28 months
Grant ID: GBMF1799
Funding Area: Science, Marine Microbiology Initiative
Organization Name: Broad Institute

Viruses constitute a critical component of the marine ecosystem, shaping the diversity, ecology and evolution of the microorganisms with which they interact and infect. It is estimated that there are greater than 1 billion virus particles in a liter of seawater, and yet we are only beginning to understand the nuances of how these tiny players impact marine microbial ecosystems. DNA sequencing technologies are enabling new insights into the vast diversity of laboratory-isolated viruses and natural populations collected from seawater to stimulate new hypotheses regarding how viruses interact with microbes to influence marine elemental cycling.

To better understand the genomic diversity of marine phage (which infect bacteria and archaea) and viruses (which infect microeukaryotes), the Broad Institute, the Marine Microbiology Initiative (MMI) at the Gordon and Betty Moore Foundation, and the international virus ecology research community initiated the Marine Phage, Virus and Virome Sequencing Project. The effort resulted in 127 annotated phage and virus genomes and 137 viral metagenomes (sequences of whole virus communities). All data are publicly available through NCBI, with accompanying accession information here. The project included a phylogenetic breath of bacterial hosts, including a diverse range of cyanophage and vibriophage, and unique algal-infecting viruses. Each metagenome received approximately one quarter of a 454 FLX sequencing plate. This community resource project enabled major participation by the international marine virus ecology community and greatly increased the number of environmental viral genomes and metagenomes.

The results of this effort encompass a wealth of new knowledge gained due to a significant increase in the amount of viral DNA sequence available to researchers, new bioinformatics training opportunities, and new ways to quantify and describe a hitherto ‘black box’ of viral ecology. Highlights from the project include delineation of new viral families and a more robust biogeography of viral lineages in the global oceans (for example, Holmfeldt et al., 2013Labonté and Suttle, 2013Kelly et al., 2013), and new insights into host-viral interactions (for example, Ankrah et al., 2014).

The project forms a portfolio with the Microbial Genome Sequencing Project to sequence diverse marine bacterial and archaeal isolates; the Environmental Metagenomics Sequencing Portfolio to sequence whole microbial communities from locations around the world; and the Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP) to sequence the gene content of hundreds of single-celled marine eukaryote cultures.


The following workshops have highlighted the Marine Phage, Virus and Virome Sequencing Project, and have helped researchers exchange ideas and forge new collaborations.

Environmental Virology: A workshop on experimental methods, informatics tools, and theory, January 6-12, 2013, Tucson, AZ, USA 

A Viromics Workshop: Tools and Tricks to See the ‘Virus’ in Diverse Sequence Datasets, May 17, 2014, Boston, MA, USA

Aquatic Virus Workshop 7, November 3-7, St. Petersburg, FL, USA  

Aquatic Virus Workshop 6, October 30-November 3, 2011, Texel, The Netherlands

Bioinformatics Resource

A bioinformatics pipeline, the Viral Informatics Resource for Metagenome Exploration (VIROME), has been supported (Grant #2732) to enable classification of viral metagenome sequences based on homology search results against a curated reference database of known and environmental sequences.

Data Availability

All data are publicly available through NCBI, with accompanying accession information available for download. Data are also available through iMicrobe via project pages for the genomes and metagenomes.

Publications as of August 2015

    1. Sullivan, M. B., B. Krastins, J. L. Hughes, L. Kelly, M. Chase, D. Sarracino, & S. W. Chisholm. (2009). The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial 'mobilome'. Environ Microbiol, 11(11), 2935-2951. doi: 10.1111/j.1462-2920.2009.02081.x
    2. Henn, M. R., M. B. Sullivan, N. Strange-Thomann, M. S. Osburne, A. M. Berlin, L. Kelly, C. Yandava, C. Kodira, Q. Zeng, M. Weiand, T. Sparrow, S. Saif, G. Giannoukos, S.K. Young, C. Nusbaum, B. W. Birren, & S. W. Chisholm. (2010). Analysis of High-Throughput Sequencing and Annotation Strategies for Phage Genomes. PLoS One, 5(2), e9083. doi: 10.1371/journal.pone.0009083.t001
    3. Anderson, R. E., W. J. Brazelton, & J. A. Baross. (2011). Is the genetic landscape of the deep subsurface biosphere affected by viruses? Front Microbiol, 2, 219. doi: 10.3389/fmicb.2011.00219
    4. Anderson, R. E., W. J. Brazelton, & J. A. Baross. (2011). Using CRISPRs as a metagenomic tool to identify microbial hosts of a diffuse flow hydrothermal vent viral assemblage. FEMS Microbiol Ecol, 77(1), 120-133. doi: 10.1111/j.1574-6941.2011.01090.x
    5. Fogg, P. C., A. P. Hynes, E. Digby, A. S. Lang, & J. T. Beatty. (2011). Characterization of a newly discovered Mu-like bacteriophage, RcapMu, in Rhodobacter capsulatus strain SB1003. Virology, 421(2), 211-221. doi: 10.1016/j.virol.2011.09.028
    6. Hewson, I., J. M. Brown, C. A. Burge, C. S. Couch, B. A. LaBarre, M. E. Mouchka, M. Naito, & C. D. Harvell. (2011). Description of viral assemblages associated with the Gorgonia ventalina holobiont. Coral Reefs, 31(2), 487-491. doi: 10.1007/s00338-011-0864-x
    7. Nissimov, J. I., C. A. Worthy, P. Rooks, J. A. Napier, S. A. Kimmance, M. R. Henn, H. Ogata, & M. J. Allen. (2011). Draft genome sequence of the coccolithovirus EhV-84. Stand Genomic Sci, 5(1), 1-11. doi: 10.4056/sigs.1884581
    8. Nissimov, J. I., C. A. Worthy, P. Rooks, J. A. Napier, S. A. Kimmance, M. R. Henn, H. Ogata, & M. J. Allen. (2011). Draft genome sequence of the Coccolithovirus Emiliania huxleyi virus 203. J Virol, 85(24), 13468-13469. doi: 10.1128/JVI.06440-11
    9. Thompson, L. R., Q. Zeng, L. Kelly, K. H. Huang, A. U. Singer, J. Stubbe, & S. W. Chisholm. (2011). Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc Natl Acad Sci U S A, 108(39), E757-764. doi: 10.1073/pnas.1102164108
    10. Baudoux, A. C., R. W. Hendrix, G. C. Lander, X. Bailly, S. Podell, C. Paillard, J. E. Johnson, C. S. Potter, B. Carragher, & F. Azam. (2012). Genomic and functional analysis of Vibrio phage SIO-2 reveals novel insights into ecology and evolution of marine siphoviruses. Environ Microbiol, 14(8), 2071-2086. doi: 10.1111/j.1462-2920.2011.02685.x
    11. Bolduc, B., D. P. Shaughnessy, Y. I. Wolf, E. V. Koonin, F. F. Roberto, & M. Young. (2012). Identification of novel positive-strand RNA viruses by metagenomic analysis of archaea-dominated Yellowstone hot springs. J Virol, 86(10), 5562-5573. doi: 10.1128/JVI.07196-11
    12. Diemer, G. S., & K. M. Stedman. (2012). A novel virus genome discovered in an extreme environment suggests recombination between unrelated groups of RNA and DNA viruses. Biol Direct, 7(13). doi: 10.1186/1745-6150-7-13
    13. Huang, S., K. Wang, N. Jiao, & F. Chen. (2012). Genome sequences of siphoviruses infecting marine Synechococcus unveil a diverse cyanophage group and extensive phage-host genetic exchanges. Environ Microbiol, 14(2), 540-558. doi: 10.1111/j.1462-2920.2011.02667.x
    14. Marston, M. F., F. J. Pierciey, Jr., A. Shepard, G. Gearin, J. Qi, C. Yandava, S. C. Schuster, M. R. Henn, & J. B. Martiny. (2012). Rapid diversification of coevolving marine Synechococcus and a virus. Proc Natl Acad Sci U S A, 109(12), 4544-4549. doi: 10.1073/pnas.1120310109
    15. Nissimov, J. I., C. A. Worthy, P. Rooks, J. A. Napier, S. A. Kimmance, M. R. Henn, H. Ogata, & M. J. Allen. (2012). Draft genome sequence of four coccolithoviruses: Emiliania huxleyi virus EhV-88, EhV-201, EhV-207, and EhV-208. J Virol, 86(5), 2896-2897. doi: 10.1128/JVI.07046-11
    16. Nissimov, J. I., C. A. Worthy, P. Rooks, J. A. Napier, S. A. Kimmance, M. R. Henn, H. Ogata, & M. J. Allen. (2012). Draft genome sequence of the coccolithovirus Emiliania huxleyi virus 202. J Virol, 86(4), 2380-2381. doi: 10.1128/JVI.06863-11
    17. Schlenker, C., A. Goel, B. P. Tripet, S. Menon, T. Willi, M. Dlakic, M. J. Young, C. M. Lawrence, & V. Copie. (2012). Structural studies of E73 from a hyperthermophilic archaeal virus identify the "RH3" domain, an elaborated ribbon-helix-helix motif involved in DNA recognition. Biochemistry, 51(13), 2899-2910. doi: 10.1021/bi201791s
    18. Anderson, R. E., W. J. Brazelton, & J. A. Baross. (2013). The Deep Viriosphere: Assessing the Viral Impact on Microbial Community Dynamics in the Deep Subsurface. Rev Mineral Geochem, 75(1), 649-675. doi: 10.2138/rmg.2013.75.20
    19. Ankrah, N. Y., A. L. May, J. L. Middleton, D. R. Jones, M. K. Hadden, J. R. Gooding, G. R. Lecleir, S. W. Wilhelm, S. R. Campagna, & A. Buchan. (2013). Phage infection of an environmentally relevant marine bacterium alters host metabolism and lysate composition. ISME J. doi: 10.1038/ismej.2013.216
    20. Colangelo-Lillis, J. R., & J. W. Deming. (2013). Genomic analysis of cold-active Colwelliaphage 9A and psychrophilic phage-host interactions. Extremophiles, 17(1), 99-114. doi: 10.1007/s00792-012-0497-1
    21. Correa, A. M., R. M. Welsh, & R. L. Vega Thurber. (2013). Unique nucleocytoplasmic dsDNA and +ssRNA viruses are associated with the dinoflagellate endosymbionts of corals. ISME J, 7(1), 13-27. doi: 10.1038/ismej.2012.75
    22. Engelhardt, T., M. Sahlberg, H. Cypionka, & B. Engelen. (2013). Biogeography of Rhizobium radiobacter and distribution of associated temperate phages in deep subseafloor sediments. ISME J, 7(1), 199-209. doi: 10.1038/ismej.2012.92
    23. Holmfeldt, K., N. Solonenko, M. Shah, K. Corrier, L. Riemann, N. C. Verberkmoes, & M. B. Sullivan. (2013). Twelve previously unknown phage genera are ubiquitous in global oceans. Proc Natl Acad Sci U S A, 110(31), 12798-12803. doi: 10.1073/pnas.1305956110
    24. Hurwitz, B. L., & M. B. Sullivan. (2013). The Pacific Ocean Virome (POV): A Marine Viral Metagenomic Dataset and Associated Protein Clusters for Quantitative Viral Ecology. PLoS One, 8(2), e57355. doi: 10.1371/journal.pone.0057355.t001
    25. Kelly, L., H. Ding, K. H. Huang, M. S. Osburne, & S. W. Chisholm. (2013). Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent. ISME J. doi: 10.1038/ismej.2013.58
    26. Labonte, J. M., & C. A. Suttle. (2013). Metagenomic and whole-genome analysis reveals new lineages of gokushoviruses and biogeographic separation in the sea. Front Microbiol, 4, 404. doi: 10.3389/fmicb.2013.00404
    27. Labonte, Jessica M., & Curtis A. Suttle. (2013). Previously unknown and highly divergent ssDNA viruses populate the oceans. ISME J, 7(11), 2169-2177. doi: 10.1038/ismej.2013.110
    28. Labrie, S. J., K. Frois-Moniz, M. S. Osburne, L. Kelly, S. E. Roggensack, M. B. Sullivan, G. Gearin, Q. Zeng, M. Fitzgerald, M. R. Henn, & S. W. Chisholm. (2013). Genomes of marine cyanopodoviruses reveal multiple origins of diversity. Environ Microbiol, 15(5), 1356-1376. doi: 10.1111/1462-2920.12053
    29. Schoenfeld, T. W., S. K. Murugapiran, J. A. Dodsworth, S. Floyd, M. Lodes, D. A. Mead, & B. P. Hedlund. (2013). Lateral gene transfer of family A DNA polymerases between thermophilic viruses, aquificae, and apicomplexa. Mol Biol Evol, 30(7), 1653-1664. doi: 10.1093/molbev/mst078
    30. Snyder, J. C., S. K. Brumfield, K. M. Kerchner, T. E. Quax, D. Prangishvili, & M. J. Young. (2013). Insights into a viral lytic pathway from an archaeal virus-host system. J Virol, 87(4), 2186-2192. doi: 10.1128/JVI.02956-12
    31. Snyder, J. C., & M. J. Young. (2013). Lytic viruses infecting organisms from the three domains of life. Biochem Soc Trans, 41(1), 309-313. doi: 10.1042/BST20120326
    32. Solonenko, S.A., J. C. Ignacio-Espinoza, A. Alberti, C. Cruaud, S. J. Hallam, K. T. Konstantinidis, G. W. Tyson, P. Wincker, & M. B. Sullivan. (2013). Sequencing platform and library preparation choices impact viral metagenomes. BMC Genomics, 14(320). doi: 10.1186/1471-2164-14-320
    33. Stedman, K. (2013). Mechanisms for RNA capture by ssDNA viruses: grand theft RNA. J Mol Evol, 76(6), 359-364. doi: 10.1007/s00239-013-9569-9
    34. Steward, G. F., A. I. Culley, J. A. Mueller, E. M. Wood-Charlson, M. Belcaid, & G. Poisson. (2013). Are we missing half of the viruses in the ocean? ISME J, 7(3), 672-679. doi: 10.1038/ismej.2012.121
    35. Zhao, Y., B. Temperton, J. C. Thrash, M. S. Schwalbach, K. L. Vergin, Z. C. Landry, M. Ellisman, T. Deerinck, M. B. Sullivan, & S. J. Giovannoni. (2013). Abundant SAR11 viruses in the ocean. Nature, 494(7437), 357-360. doi: 10.1038/nature11921
    36. Ponsero, A. J., F. Chen, J. T. Lennon, & S. W. Wilhelm. (2013). Complete Genome Sequence of Cyanobacterial Siphovirus KBS2A. Genome Announc., 1(4), e00472-00413. doi: 10.1128/genomeA.00472-13
    37. McDaniel, L. D., K. Rosario, M. Breitbart, & J. H. Paul. (2014). Comparative metagenomics: natural populations of induced prophages demonstrate highly unique, lower diversity viral sequences. Environ Microbiol, 16(2), 570-585. doi: 10.1111/1462-2920.12184
    38. Schmidt, H. F., E. G. Sakowski, S. J. Williamson, S. W. Polson, & K. E. Wommack. (2014). Shotgun metagenomics indicates novel family A DNA polymerases predominate within marine virioplankton. ISME J, 8(1), 103-114. doi: 10.1038/ismej.2013.124
    39. Winter, C., J. A. L. Garcia, M. G. Weinbauer, M. S. DuBow, & G. J. Herndl. (2014) Comparison of Deep-Water Viromes from the Atlantic Ocean and the Mediterranean Sea. PLoS One, 9(6). e100600. doi:10.1371/journal.pone.0100600
    40. Paul, B. G., S. C. Bagby, E. Czornyj, D. Arambula, S. Handa, A. Sczyrba, P. Ghosh, J. F. Miller, & D. L. Valentine. (2015). Targeted diversity generation by intraterrestrial archaea and archaeal viruses. Nature Communications, 6. doi: 10.1038/ncomms7585
    41. Sullivan, M. B., K. H. Huang, J. C. Ignacio-Espinoza, A. M. Berlin, L. Kelly, P. R. Weigele, A. S. DeFrancesco, S. E. Kern, L. R. Thompson, S. Young, C. Yandava, R. Fu, B. Krastins, M. Chase, D. Sarracino, M. S. Osburne, M. R. Henn, & S. W. Chisholm. (2010). Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environmental Microbiology, 12: 3035–3056. doi: 10.1111/j.1462-2920.2010.02280
    42. Santini, S., S. Jeudy, J. Bartoli, O. Poirot, M. Lescot, C. Abergel, V. Barbe, K. E. Wommack, A. A. M. Noordeloos, C. P. D. Brussard, & J. M. Claverie. (2013). Genome of Phaeocystis globose virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes. Proceedings of the National Academy of Sciences, 110(26): 10800-10805. doi: 10.1073/pnas.1303251110

    43. Snyder, J. C., B. Bolduc, M. M. Bateson, & M. J. Young. (2011). The prevalence of STIV c92-like proteins in acidic thermal environments. Advances in Virology, 2011: Article ID 650930. doi:10.1155/2011/650930

    44. Giovannelli, D., S. Ferriera, J. Johnson, S. Kravitz, I. Pérez-Rodríguez, J. Ricci, C. O’Brien, J. W. Voordeckers, E. Bini, & C. Vetriani. (2011). Draft genome sequence of Caminibacter mediatlanticus strain TB-2T, an epsilonproteobacterium isolated from a deep-sea hydrothermal vent. Standards in Genomic Sciences5(1): 135–143. doi:10.4056/sigs.2094859

    45. John, S. G., C. B. Mendez, L. Deng, B. Poulos, A. K. M. Kauffman, S. Kern, J. Brum, M. F. Polz, E. A. Boyle, & M. B. Sullivan. (2011). A simple and efficient method for concentration of ocean viruses by chemical flocculation. Environmental Microbiology Reports, 3: 195–202. doi: 10.1111/j.1758-2229.2010.00208.x

    46. Lander, G. C., A. C. Baudoux, F. Azam, C. S. Potter, B. Carragher, & J. E. Johnson. (2012). Capsomer dynamics and stabilization in the T = 12 marine bacteriophage SIO-2 and its procapsid studied by CryoEM. Structure, 20(3): 498-503. doi:10.1016/j.str.2012.01.007

    47. Uitz, J., D. Stramski, A. C. Baudoux, R. A. Reynolds, V. M. Wright, J. Dubranna, & F. Azam. (2010). Variations in the optical properties of a particle suspension associated with viral infection of marine bacteria. Limnology and Oceanography, 55(6): 2317-2330. doi: 10.4319/lo.2010.55.6.2317

    48. Polson, S. W., S. W. Wilhelm, & K. E. Wommack. (2011). Unraveling the viral tapestry (from inside the capsid out). ISME Journal, 5(2), 165-168. doi: 10.1038/ismej.2010.81

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