Skip to main content
SpringerLink
Log in

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

  • Review
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Bergh, O., Borsheim, K.Y., Bratbak, G., and Heldal, M. 1989. High abundance of viruses found in aquatic environments. Nature (London) 340, 467–468.

    Article  CAS  Google Scholar 

  • Breitbart, M., Miyake, J.H., and Rohwer, F. 2004. Global distribution of nearly identical phage-encoded DNA sequences. FEMS Microbiol. Lett. 236, 249–256.

    Article  CAS  PubMed  Google Scholar 

  • Breitbart, M. and Rohwer, F. 2005. Here a virus, there a virus, everywhere the same virus? Trends Microbiol. 13, 278–284.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brum, J.R., Culley, A.I., and Steward, G.F. 2013. Assembly of a marine viral metagenome after physical fractionation. PLoS One 8, e60604.

  • 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 

  • Chen, C.Y. 2014. DNA polymerases drive DNA sequencing-bysynthesis technologies: both past and present. Front. Microbiol. 5, 305.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Culley, A.I., Lang, A.S., and Suttle, C.A. 2006. Metagenomic analysis of coastal RNA virus communities. Science 312, 1795–1798.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Duhaime, M.B. and Sullivan, M.B. 2012. Ocean viruses: rigorously evaluating the metagenomic sample-to-sequence pipeline. Virology 434, 181–186.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • Labonté, J.M. and Suttle, C.A. 2013. Previously unknown and highly divergent ssDNA viruses populate the oceans. ISME J. 7, 2169–2177.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nordlund, P. and Reichard, P. 2006. Ribonucleotide reductases. Annu. Rev. Biochem. 75, 681–706.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Pedrós-Alió, C. 2012. The rare bacterial biosphere. Ann. Rev. Mar. Sci. 4, 449–466.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • Proctor, L.M., Fuhrman, J.A., and Ledbetter, M.C. 1988. Marine bacteriophages and bacterial mortality. Eos 69, 1111–1112.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Rohwer, F. and Edwards, R. 2002. The phage proteomic tree: a genome-based taxonomy for phage. J. Bacteriol. 184, 4529–4535.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

  • 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.

  • Suttle, C.A. 2005. Viruses in the sea. Nature 437, 356–361.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Wagner-Döbler, I. and Biebl, H. 2006. Environmental biology of the marine Roseobacter lineage. Microbiol. 60, 255–280.

    Article  Google Scholar 

  • Weinbauer, M.G. 2004. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28, 127–181.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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 

  • Whitman, W.B., Coleman, D.C., and Wiebe, W.J. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA 95, 6578–6583.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm, S.W. and Suttle, C.A. 1999. Viruses and nutrient cycles in the sea. Bioscience 49, 781–788.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Willner, D., Thurber, R.V., and Rohwer, F. 2009. Metagenomic signatures of 86 microbial and viral metagenomes. Environ. Microbiol. 11, 1752–1766.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Winget, D.M. and Wommack, K.E. 2009. Diel and daily fluctuations in virioplankton production in coastal ecosystems. Environ. Microbiol. 11, 2904–2914.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Wommack, K.E., Bhavsar, J., and Ravel, J. 2008. Metagenomics: read length matters. Appl. Environ. Microbiol. 74, 1453–1463.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wommack, K.E. and Colwell, R.R. 2000. Virioplankton: Viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64, 69–114.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Yilmaz, S., Allgaier, M., and Hugenholtz, P. 2010. Multiple displacement amplification compromises quantitative analysis of metagenomes. Nat. Methods 7, 943–944.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Delaware Biotechnology Institute, University of Delaware, Newark Delaware, USA

    K. Eri Wommack, Daniel J. Nasko, Jessica Chopyk & Eric G. Sakowski

Authors
  1. K. Eri Wommack
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel J. Nasko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jessica Chopyk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eric G. Sakowski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. Eri Wommack.

Additional information

Supplemental material for this article may be found at http://www.springerlink.com/content/120956.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wommack, K.E., Nasko, D.J., Chopyk, J. et al. Counts and sequences, observations that continue to change our understanding of viruses in nature. J Microbiol. 53, 181–192 (2015). https://doi.org/10.1007/s12275-015-5068-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-015-5068-6

Keywords

Search

Navigation