Journal of Microbiology

, Volume 53, Issue 3, pp 181–192 | Cite as

Counts and sequences, observations that continue to change our understanding of viruses in nature

  • K. Eri Wommack
  • Daniel J. Nasko
  • Jessica Chopyk
  • Eric G. Sakowski
Review

Abstract

The discovery of abundant viruses in the oceans and on land has ushered in a quarter century of groundbreaking advancements in our understanding of viruses within ecosystems. Two types of observations from environmental samples — direct counts of viral particles and viral metagenomic sequences — have been critical to these discoveries. Accurate direct counts have established ecosystem-scale trends in the impacts of viral infection on microbial host populations and have shown that viral communities within aquatic and soil environments respond to both short term and seasonal environmental change. Direct counts have been critical for estimating viral production rate, a measurement essential to quantifying the implications of viral infection for the biogeochemical cycling of nutrients within ecosystems. While direct counts have defined the magnitude of viral processes; shotgun sequences of environmental viral DNA — virome sequences — have enabled researchers to estimate the diversity and composition of natural viral communities. Virome-enabled studies have found the virioplankton to contain thousands of viral genotypes in communities where the most dominant viral population accounts for a small fraction of total abundance followed by a long tail of diverse populations. Detailed examination of long virome sequences has led to new understanding of genotype-to-phenotype connections within marine viruses and revealed that viruses carry metabolic genes that are important to maintaining cellular energy during viral replication. Increased access to long virome sequences will undoubtedly reveal more genetic secrets of viruses and enable us to build a genomics rulebook for predicting key biological and ecological features of unknown viruses.

Keywords

informational proteins viral ecology viromics 

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References

  1. Adriaenssens, E.M. and Cowan, D.A. 2014. Using signature genes as tools to assess environmental viral ecology and diversity. Appl. Environ. Microbiol. 80, 4470–4480.PubMedCentralPubMedCrossRefGoogle Scholar
  2. Anantharaman, K., Duhaime, M.B., Breier, J.A., Wendt, K.A., Toner, B.M., and Dick, G.J. 2014. Sulfur oxidation genes in diverse deepsea viruses. Science (New York, NY) 344, 757–760.CrossRefGoogle Scholar
  3. Angly, F.E., Felts, B., Breitbart, M., Salamon, P., Edwards, R.A., Carlson, C., Chan, A.M., Haynes, M., Kelley, S., Liu, H., et al 2006. The marine viromes of four oceanic regions. PLoS Biol. DOI 10.1371/journal.pbio.0040368.Google Scholar
  4. Angly, F., Rodriguez-Brito, B., Bangor, D., McNairnie, P., Breitbart, M., Salamon, P., Felts, B., Nulton, J., Mahaffy, J., and Rohwer, F. 2005. PHACCS, an online tool for estimating the structure and diversity of uncultured viral communities using metagenomic information. BMC Bioinformatics 6, 41.PubMedCentralPubMedCrossRefGoogle Scholar
  5. Angly, F.E., Willner, D., Prieto-Davó, A., Edwards, R.A., Schmieder, R., Vega-Thurber, R., Antonopoulos, D.A., Barott, K., Cottrell, M.T., Desnues, C., et al 2009. The GAAS metagenomic tool and its estimations of viral and microbial average genome size in four major biomes. PLoS Comput. Biol. 5, e1000593.Google Scholar
  6. Behrenfeld, M.J., Bale, A.J., Kolber, Z.S., Aiken, J., and Falkowski, P.G. 1996. Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean. Nature 383, 508–511.CrossRefGoogle Scholar
  7. Bench, S.R., Hanson, T.E., Williamson, K.E., Ghosh, D., Radosovich, M., Wang, K., and Wommack, K.E. 2007. Metagenomic characterization of Chesapeake Bay virioplankton. Appl. Environ. Microbiol. 73, 7629–7641.Google Scholar
  8. Bergh, O., Borsheim, K.Y., Bratbak, G., and Heldal, M. 1989. High abundance of viruses found in aquatic environments. Nature (London) 340, 467–468.CrossRefGoogle Scholar
  9. Breitbart, M., Miyake, J.H., and Rohwer, F. 2004. Global distribution of nearly identical phage-encoded DNA sequences. FEMS Microbiol. Lett. 236, 249–256.PubMedCrossRefGoogle Scholar
  10. Breitbart, M. and Rohwer, F. 2005. Here a virus, there a virus, everywhere the same virus? Trends Microbiol. 13, 278–284.PubMedCrossRefGoogle Scholar
  11. Breitbart, M., Salamon, P., Andresen, B., Mahaffy, J.M., Segall, A.M., Mead, D., Azam, F., and Rohwer, F. 2002. Genomic analysis of uncultured marine viral communities. Proc. Natl. Acad. Sci. USA 99, 14250–14255.PubMedCentralPubMedCrossRefGoogle Scholar
  12. Brum, J.R., Culley, A.I., and Steward, G.F. 2013. Assembly of a marine viral metagenome after physical fractionation. PLoS One 8, e60604.Google Scholar
  13. Brussaard, C.P.D., Payet, J.P., Winter, C., and Weinbauer, M.G. 2010. Quantification of aquatic viruses by flow cytometry. In. American Society of Limnology and Oceanography, pp. 102–109.Google Scholar
  14. Chen, C.Y. 2014. DNA polymerases drive DNA sequencing-bysynthesis technologies: both past and present. Front. Microbiol. 5, 305.Google Scholar
  15. Clasen, J.L., Brigden, S.M., Payet, J.P., and Suttle, C.A. 2008. Evidence that viral abundance across oceans and lakes is driven by different biological factors. Freshw. Biol. 53, 1090–1100.CrossRefGoogle Scholar
  16. Culley, A.I., Lang, A.S., and Suttle, C.A. 2006. Metagenomic analysis of coastal RNA virus communities. Science 312, 1795–1798.PubMedCrossRefGoogle Scholar
  17. Cunningham, B.R., Brum, J.R., Schwenck, S.M., Sullivan, M.B., and John, S.G. 2015. An inexpensive, accurate and precise wetmount method for enumerating aquatic viruses. Appl. Environ. Microbiol. in revision.Google Scholar
  18. Danovaro, R., Dell’Anno, A., Corinaldesi, C., Magagnini, M., Noble, R., Tamburini, C., and Weinbauer, M. 2008. Major viral impact on the functioning of benthic deep-sea ecosystems. Nature 454, 1084–1087.PubMedCrossRefGoogle Scholar
  19. de Cárcer, D.A., Angly, F.E., and Alcamí, A. 2014. Evaluation of viral genome assembly and diversity estimation in deep metagenomes. BMC Genomics 15, 989–989.CrossRefGoogle Scholar
  20. Dell’Anno, A., Corinaldesi, C., Magagnini, M., and Danovaro, R. 2009. Determination of viral production in aquatic sediments using the dilution-based approach. Nature Protocols 4, 1013–1022.PubMedCrossRefGoogle Scholar
  21. Deng, L., Gregory, A., Yilmaz, S., Poulos, B.T., Hugenholtz, P., and Sullivan, M.B. 2012. Contrasting life strategies of viruses that infect photo- and heterotrophic bacteria, as revealed by viral tagging. mBio 3, pii: e00373-12.Google Scholar
  22. Deng, L., Ignacio-Espinoza, J.C., Gregory, A.C., Poulos, B.T., Weitz, J.S., Hugenholtz, P., and Sullivan, M.B. 2014. Viral tagging reveals discrete populations in Synechococcus viral genome sequence space. Nature 513, 242–245.PubMedCrossRefGoogle Scholar
  23. Dick, G.J., Andersson, A.F., Baker, B.J., Simmons, S.L., Thomas, B.C., Yelton, A.P., and Banfield, J.F. 2009. Community-wide analysis of microbial genome sequence signatures. Genome Biol. 10, R85.PubMedCentralPubMedCrossRefGoogle Scholar
  24. Diemer, G.S. and Stedman, K.M. 2012. A novel virus genome discovered in an extreme environment suggests recombination between unrelated groups of RNA and DNA viruses. Biol. Direct 7, 13.PubMedCentralPubMedCrossRefGoogle Scholar
  25. Doublié, S., Tabor, S., Long, A.M., Richardson, C.C., and Ellenberger, T. 1998. Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 A resolution. Nature 391, 251–258.PubMedCrossRefGoogle Scholar
  26. Duhaime, M.B., Deng, L., Poulos, B.T., and Sullivan, M.B. 2012. Towards quantitative metagenomics of wild viruses and other ultra-low concentration DNA samples: a rigorous assessment and optimization of the linker amplification method. Environ. Microbiol. 14, 2526–2537.Google Scholar
  27. Duhaime, M.B. and Sullivan, M.B. 2012. Ocean viruses: rigorously evaluating the metagenomic sample-to-sequence pipeline. Virology 434, 181–186.PubMedCrossRefGoogle Scholar
  28. Field, C., Behrenfeld, M., Randerson, J., and Falkowski, P. 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science (New York, NY) 281, 237–240.CrossRefGoogle Scholar
  29. Gimenes, M.V., Zanotto, P.M.d.A., Suttle, C.A., da Cunha, H.B., and Mehnert, D.U. 2011. Phylodynamics and movement of Phycodnaviruses among aquatic environments. ISME J. 6, 237–247.PubMedCentralPubMedCrossRefGoogle Scholar
  30. Goldsmith, D.B., Crosti, G., Dwivedi, B., McDaniel, L.D., Varsani, A., Suttle, C.A., Weinbauer, M.G., Sandaa, R.A., and Breitbart, M. 2011. Development of phoH as a novel signature gene for assessing marine phage diversity. Appl. Environ. Microbiol. 77, 7730–7739.Google Scholar
  31. Haaber, J. and Middelboe, M. 2009. Viral lysis of Phaeocystis pouchetii: implications for algal population dynamics and heterotrophic C, N and P cycling. ISME J. 3, 430–441.PubMedCrossRefGoogle Scholar
  32. Hara, S., Koike, I., Terauchi, K., Kamiya, H., and Tanoue, E. 1996. Abundance of viruses in deep oceanic waters. Mar. Ecol. Prog. Ser. 145, 269–277.CrossRefGoogle Scholar
  33. Helton, R.R., Cottrell, M.T., Kirchman, D.L., and Wommack, K.E. 2005. Evaluation of incubation-based methods for estimating virioplankton production in estuaries. Aquat. Microb. Ecol. 41, 209–219.CrossRefGoogle Scholar
  34. Hewson, I. and Fuhrman, J.A. 2003. Viriobenthos production and virioplankton sorptive scavenging by suspended sediment particles in coastal and pelagic waters. Microb. Ecol. 46, 337–347.PubMedCrossRefGoogle Scholar
  35. Holmfeldt, K., Solonenko, N., Shah, M., Corrier, K., Riemann, L., Verberkmoes, N.C., and Sullivan, M.B. 2013. Twelve previously unknown phage genera are ubiquitous in global oceans. Proc. Natl. Acad. Sci. USA 110, 12798–12803.PubMedCentralPubMedCrossRefGoogle Scholar
  36. Hurwitz, B.L., Deng, L., Poulos, B.T., and Sullivan, M.B. 2012. Evaluation of methods to concentrate and purify ocean virus communities through comparative, replicated metagenomics. Environ. Microbiol. 15, 1428–1440.Google Scholar
  37. Hurwitz, B.L. and Sullivan, M.B. 2013. The Pacific Ocean virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS One 8, e57355.Google Scholar
  38. John, S., Mendez, C., Deng, L., Poulos, B., Kauffman, A., Kern, S., Brum, J., Polz, M., Boyle, E., and Sullivan, M. 2010. A simple and efficient method for concentration of ocean viruses by chemical flocculation. Environ. Microbiol. Rep. 3, 195–202.CrossRefGoogle Scholar
  39. Jover, L.F., Effler, T.C., Buchan, A., Wilhelm, S.W., and Weitz, J.S. 2014. The elemental composition of virus particles: implications for marine biogeochemical cycles. Nat. Rev. Microbiol. 12, 519–528.PubMedCrossRefGoogle Scholar
  40. Kang, I., Oh, H.M., Kang, D., and Cho, J.C. 2013. Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans. Proc. Natl. Acad. Sci. USA 110, 12343–12348.PubMedCentralPubMedCrossRefGoogle Scholar
  41. Kiefer, J.R., Mao, C., Braman, J.C., and Beese, L.S. 1998. Visualizing DNA replication in a catalytically active Bacillus DNA polymerase crystal. Nature 391, 304–307.PubMedCrossRefGoogle Scholar
  42. Kolberg, M., Strand, K.R., Graff, P., and Andersson, K.K. 2004. Structure, function, and mechanism of ribonucleotide reductases. Biochim. Biophys. Acta 1699, 1–34.PubMedCrossRefGoogle Scholar
  43. Labonté, J.M., Reid, K.E., and Suttle, C.A. 2009. Phylogenetic analysis indicates evolutionary diversity and environmental segregation of marine podovirus DNA polymerase gene sequences. Appl. Environ. Microbiol. 75, 3634–3640.PubMedCentralPubMedCrossRefGoogle Scholar
  44. Labonté, J.M. and Suttle, C.A. 2013. Previously unknown and highly divergent ssDNA viruses populate the oceans. ISME J. 7, 2169–2177.PubMedCentralPubMedCrossRefGoogle Scholar
  45. Lindell, D., Jaffe, J.D., Johnson, Z.I., Church, G.M., and Chisholm, S.W. 2005. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438, 86–89.PubMedCrossRefGoogle Scholar
  46. Lindell, D., Sullivan, M.B., Johnson, Z.I., Tolonen, A.C., Rohwer, F., and Chisholm, S.W. 2004. Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc. Natl. Acad. Sci. USA 101, 11013–11018.PubMedCentralPubMedCrossRefGoogle Scholar
  47. Loh, E. and Loeb, L.A. 2005. Mutability of DNA polymerase I: implications for the creation of mutant DNA polymerases. DNA Repair 4, 1390–1398.PubMedCrossRefGoogle Scholar
  48. Mann, N.H., Cook, A., Millard, A., Bailey, S., and Clokie, M. 2003. Marine ecosystems: Bacterial photosynthesis genes in a virus. Nature 424, 741–741.PubMedCrossRefGoogle Scholar
  49. Marine, R., McCarren, C., Vorrasane, V., Nasko, D., Crowgey, E., Polson, S.W., and Wommack, K.E. 2014. Caught in the middle with multiple displacement amplification: the myth of pooling for avoiding multiple displacement amplification bias in a metagenome. Microbiome 2, 3.PubMedCentralPubMedCrossRefGoogle Scholar
  50. Martínez, J.M., Swan, B.K., and Wilson, W.H. 2014. Marine viruses, a genetic reservoir revealed by targeted viromics. ISME J. 8, 1079–1088.CrossRefGoogle Scholar
  51. Maurice, C.F., Mouillot, D., Bettarel, Y., De Wit, R., Sarmento, H., and Bouvier, T. 2010. Disentangling the relative influence of bacterioplankton phylogeny and metabolism on lysogeny in reservoirs and lagoons. ISME J. 5, 831–842.PubMedCentralPubMedCrossRefGoogle Scholar
  52. Mioni, C.E., Poorvin, L., and Wilhelm, S.W. 2005. Virus and siderophore-mediated transfer of available Fe between heterotrophic bacteria: characterization using an Fe-specific bioreporter. Aquat. Microb. Ecol. 41, 233–245.CrossRefGoogle Scholar
  53. Moore, J.K., Doney, S.C., Glover, D.M., and Fung, I.Y. 2002. Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean. Deep-Sea Res. Part II-Top. Stud. Oceanogr. 49, 463–507.CrossRefGoogle Scholar
  54. Noguchi, H., Taniguchi, T., and Itoh, T. 2008. MetaGeneAnnotator: detecting species-specific patterns of ribosomal binding site for precise gene prediction in anonymous prokaryotic and phage genomes. DNA Res. 15, 387–396.PubMedCentralPubMedCrossRefGoogle Scholar
  55. Nordlund, P. and Reichard, P. 2006. Ribonucleotide reductases. Annu. Rev. Biochem. 75, 681–706.PubMedCrossRefGoogle Scholar
  56. Payet, J.P. and Suttle, C.A. 2013. To kill or not to kill: The balance between lytic and lysogenic viral infection is driven by trophic status. Limnol. Oceanogr. 58, 465–474.Google Scholar
  57. Pedrós-Alió, C. 2012. The rare bacterial biosphere. Ann. Rev. Mar. Sci. 4, 449–466.PubMedCrossRefGoogle Scholar
  58. Poorvin, L., Rinta-Kanto, J.M., Hutchins, D.A., and Wilhelm, S.W. 2004. Viral release of iron and its bioavailability to marine plankton. Limnol. Oceanogr. 49, 1734–1741.CrossRefGoogle Scholar
  59. Pride, D., Wassenaar, T., Ghose, C., and Blaser, M. 2006. Evidence of host-virus co-evolution in tetranucleotide usage patterns of bacteriophages and eukaryotic viruses. BMC Genomics 7, 8.PubMedCentralPubMedCrossRefGoogle Scholar
  60. Proctor, L.M., Fuhrman, J.A., and Ledbetter, M.C. 1988. Marine bacteriophages and bacterial mortality. Eos 69, 1111–1112.Google Scholar
  61. Rodriguez-Brito, B., Li, L., Wegley, L., Furlan, M., Angly, F., Breitbart, M., Buchanan, J., Desnues, C., Dinsdale, E., Edwards, R., et al 2010. Viral and microbial community dynamics in four aquatic environments. ISME J. 4, 739–751.PubMedCrossRefGoogle Scholar
  62. Rohwer, F. and Edwards, R. 2002. The phage proteomic tree: a genome-based taxonomy for phage. J. Bacteriol. 184, 4529–4535.PubMedCentralPubMedCrossRefGoogle Scholar
  63. Sakowski, E.G., Munsell, E.V., Hyatt, M., Kress, W., Williamson, S.J., Nasko, D.J., Polson, S.W., and Wommack, K.E. 2014. Ribonucleotide reductases reveal novel viral diversity and predict biological and ecological features of unknown marine viruses. Proc. Natl. Acad. Sci. USA 111, 15786–15791.PubMedCentralPubMedCrossRefGoogle Scholar
  64. Schmidt, H.F., Sakowski, E.G., Williamson, S.J., Polson, S.W., and Wommack, K.E. 2014. Shotgun metagenomics indicates novel family A DNA polymerases predominate within marine virioplankton. ISME J. 8, 103–114.PubMedCentralPubMedCrossRefGoogle Scholar
  65. Srinivasiah, S., Bhavsar, J., Thapar, K., Liles, M., Schoenfeld, T., and Wommack, K.E. 2008. Phages across the biosphere: contrasts of viruses in soil and aquatic environments. Res. Microbiol. 159, 349–357.PubMedCrossRefGoogle Scholar
  66. Srinivasiah, S., Lovett, J., Ghosh, D., Roy, K., Fuhrmann, J.J., Rado sevich, M., and Wommack, K.E. 2015. Dynamics of autochthonous soil viral communities parallels dynamics of host communities under nutrient stimulation. Submitted.Google Scholar
  67. Srinivasiah, S., Lovett, J., Polson, S., Bhavsar, J., Ghosh, D., Roy, K., Fuhrmann, J.J., Radosevich, M., and Wommack, K.E. 2013. Direct assessment of viral diversity in soils using RAPD-PCR. Appl. Environ. Microbiol. 79, 5450–5457.PubMedCentralPubMedCrossRefGoogle Scholar
  68. Steward, G.F., Wikner, J., Cochlan, W.P., Smith, D.C., and Azam, F. 1992. Estimation of virus production in the sea: I. method development. Mar. Microb. Food Webs 6, 57–78.Google Scholar
  69. Sullivan, M.B., Coleman, M.L., Weigele, P., Rohwer, F., and Chisholm, S.W. 2005. Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol. 3, e144.Google Scholar
  70. Sullivan, M.B., Lindell, D., Lee, J.A., Thompson, L.R., Bielawski, J.P., and Chisholm, S.W. 2006. Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol. 4, e234.Google Scholar
  71. Suttle, C.A. 2005. Viruses in the sea. Nature 437, 356–361.PubMedCrossRefGoogle Scholar
  72. Suttle, C.A. and Chan, A.M. 1994. Dynamics and distribution of cyanophages and their effect on marine Synechococcus spp. Appl. Environ. Microbiol. 60, 3167–3174.PubMedCentralPubMedGoogle Scholar
  73. Suttle, C.A. and Fuhrman, J.A. 2010. MAVE: Enumeration of virus particles in aquatic or sediment samples by epifluorescence microscopy. In Wilhelm, S.W., Weinbauer, M.G., and Suttle, C.A. (eds.), pp. 145–153. Manual of Aquatic Viral Ecology. ASLO, Waco, Tex.CrossRefGoogle Scholar
  74. Tabor, S. and Richardson, C.C. 1989. Selective inactivation of the exonuclease activity of bacteriophage T7 DNA polymerase by in vitro mutagenesis. J. Biol. Chem. 264, 6447–6458.PubMedGoogle Scholar
  75. Tomaru, Y., Takao, Y., Suzuki, H., Nagumo, T., Koike, K., and Nagasaki, K. 2011. Isolation and characterization of a singlestranded DNA virus infecting Chaetoceros lorenzianus Grunow. Appl. Environ. Microbiol. 77, 5285–5293.PubMedCentralPubMedCrossRefGoogle Scholar
  76. Van Gestel, M., Merckx, R., and Vlassak, K. 2002. Microbial biomass responses to soil drying and rewetting: The fate of fast- and slow-growing microorganisms in soils from different climates. Soil Biol. Biochem. 25, 109–123.CrossRefGoogle Scholar
  77. Wagner-Döbler, I. and Biebl, H. 2006. Environmental biology of the marine Roseobacter lineage. Microbiol. 60, 255–280.CrossRefGoogle Scholar
  78. Weinbauer, M.G. 2004. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28, 127–181.PubMedCrossRefGoogle Scholar
  79. Weinbauer, M., Rowe, J., and Wilhelm, S. 2010. Determining rates of virus production in aquatic systems by the virus reduction approach, pp. 1–8. Manual of Aquatic Viral Ecology. American Society of Limnology and Oceanography.CrossRefGoogle Scholar
  80. Weitz, J.S., Stock, C.A., Wilhelm, S.W., Bourouiba, L., Coleman, M.L., Buchan, A., Follows, M.J., Fuhrman, J.A., Jover, L.F., Lennon, J.T., et al 2015. A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes. ISME J. doi:10.1038/ismej.2014.220.Google Scholar
  81. Whitman, W.B., Coleman, D.C., and Wiebe, W.J. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA 95, 6578–6583.PubMedCentralPubMedCrossRefGoogle Scholar
  82. Wilhelm, S.W., Brigden, S.M., and Suttle, C.A. 2002. A dilution technique for the direct measurement of viral production: A comparison in stratified and tidally mixed coastal waters. Microb. Ecol. 43, 168–173.PubMedCrossRefGoogle Scholar
  83. Wilhelm, S.W. and Suttle, C.A. 1999. Viruses and nutrient cycles in the sea. Bioscience 49, 781–788.CrossRefGoogle Scholar
  84. Williamson, K.E., Radosevich, M., Smith, D.W., and Wommack, K.E. 2007. Incidence of lysogeny within temperate and extreme soil environments. Environ. Microbiol. 9, 2563–2574.PubMedCrossRefGoogle Scholar
  85. Williamson, K.E., Radosevich, M., and Wommack, K.E. 2005. Abundance and diversity of viruses in six Delaware soils. Appl. Environ. Microbiol. 71, 3119–3125.PubMedCentralPubMedCrossRefGoogle Scholar
  86. Williamson, K.E., Schnitker, J.B., Radosevich, M., Smith, D.W., and Wommack, K.E. 2008. Cultivation-based assessment of lysogeny among soil bacteria. Microb. Ecol. 56, 437–447.PubMedCrossRefGoogle Scholar
  87. Williamson, K.E., Wommack, K.E., and Radosevich, M. 2003. Sampling natural viral communities from soil for culture-independent analyses. Appl. Environ. Microbiol. 69, 6628–6633.PubMedCentralPubMedCrossRefGoogle Scholar
  88. Willner, D., Thurber, R.V., and Rohwer, F. 2009. Metagenomic signatures of 86 microbial and viral metagenomes. Environ. Microbiol. 11, 1752–1766.PubMedCrossRefGoogle Scholar
  89. Winget, D.M., Helton, R.R., Williamson, K.E., Bench, S.R., Williamson, S.J., and Wommack, K.E. 2011. Repeating patterns of virioplankton production within an estuarine ecosystem. Proc. Natl. Acad. Sci. USA 108, 11506–11511.PubMedCentralPubMedCrossRefGoogle Scholar
  90. Winget, D.M., Williamson, K.E., Helton, R.R., and Wommack, K.E. 2005. Tangential flow diafiltration: An improved technique for virioplankton production. Aquat. Microb. Ecol. 41, 221–232.CrossRefGoogle Scholar
  91. Winget, D.M. and Wommack, K.E. 2009. Diel and daily fluctuations in virioplankton production in coastal ecosystems. Environ. Microbiol. 11, 2904–2914.PubMedCrossRefGoogle Scholar
  92. Woese, C.R. and Fox, G.E. 1977. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl. Acad. Sci. USA 74, 5088–5090.PubMedCentralPubMedCrossRefGoogle Scholar
  93. Woese, C.R., Kandler, O., and Wheelis, M.L. 1990. Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. USA 87, 4576–4579.PubMedCentralPubMedCrossRefGoogle Scholar
  94. Wommack, K.E., Bhavsar, J., Polson, S.W., Chen, J., Dumas, M., Srinivasiah, S., Furman, M., Jamindar, S., and Nasko, D.J. 2012. VIROME: a standard operating procedure for analysis of viral metagenome sequences. Std. Genom. Sci. 6, 427–439.CrossRefGoogle Scholar
  95. Wommack, K.E., Bhavsar, J., and Ravel, J. 2008. Metagenomics: read length matters. Appl. Environ. Microbiol. 74, 1453–1463.PubMedCentralPubMedCrossRefGoogle Scholar
  96. Wommack, K.E. and Colwell, R.R. 2000. Virioplankton: Viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64, 69–114.CrossRefGoogle Scholar
  97. Wommack, K.E., Williamson, S.J., Sundbergh, A., Helton, R.R., Glazer, B.T., Portune, K., and Cary, S.C. 2004. An instrument for collecting discrete large-volume water samples suitable for ecological studies of microorganisms. Deep-Sea Res. Part I-Oceanogr. Res. Pap. 51, 1781–1792.CrossRefGoogle Scholar
  98. Yilmaz, S., Allgaier, M., and Hugenholtz, P. 2010. Multiple displacement amplification compromises quantitative analysis of metagenomes. Nat. Methods 7, 943–944.PubMedCrossRefGoogle Scholar
  99. Zhang, Y., Jiao, N., and Hong, N. 2008. Comparative study of picoplankton biomass and community structure in different provinces from subarctic to subtropical oceans. Deep-Sea Res. Part II-Top. Stud. Oceanogr. 55, 1605–1614.CrossRefGoogle Scholar
  100. Zhao, Y.Y., Temperton, B.B., Thrash, J.C.J., Schwalbach, M.S.M., Vergin, K.L.K., Landry, Z.C.Z., Ellisman, M.M., Deerinck, T.T., Sullivan, M.B.M., and Giovannoni, S.J.S. 2013. Abundant SAR11 viruses in the ocean. Nature 494, 357–360.PubMedCrossRefGoogle Scholar

Copyright information

© The Microbiological Society of Korea and Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • K. Eri Wommack
    • 1
  • Daniel J. Nasko
    • 1
  • Jessica Chopyk
    • 1
  • Eric G. Sakowski
    • 1
  1. 1.Delaware Biotechnology InstituteUniversity of DelawareNewark DelawareUSA

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