High temporal and spatial diversity in marine RNA viruses implies that they have an important role in mortality and structuring plankton communities

Frontiers in Microbiology

Volumn 5, Issue DEC, 2014, Pages

  Gustavsen, Julia A ^a   Winget, Danielle M ^a,c   Tian, Xi ^a   Suttle, Curtis A ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b CANADIAN INSTITUTE FOR ADVANCED RESEARCH   (Canada)

^c SEATTLE PACIFIC UNIVERSITY   (United States)

Author keywords

Phytoplankton mortality; picornavirales; Pyrosequencing; RNA viruses; Viral diversity; Viral ecology

Indexed keywords

RNA DIRECTED RNA POLYMERASE; RNA POLYMERASE;

AMPLICON; ARTICLE; CANADA; DNA SEQUENCE; ENERGY TRANSFER; MARINE SPECIES; MICROBIAL DIVERSITY; NONHUMAN; NUCLEIC ACID ANALYSIS; NUTRIENT CYCLING; PHYLOGENY; PHYTOPLANKTON; PICORNAVIRALES; POLYMERASE CHAIN REACTION; POPULATION GENETIC STRUCTURE; PYROSEQUENCING; RNA VIRUS; SEQUENCE ANALYSIS; TAXONOMIC RANK;

EUKARYOTA; OTUS; RNA VIRUSES;

EID: 84920677058     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00703     Document Type: Article

References (101)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410. doi: 10.1016/S0022-2836(05)80360-2
2. Amend, A. S., Seifert, K. A., and Bruns, T. D. (2010). Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol. Ecol. 19, 5555-5565. doi: 10.1111/j.1365-294X.2010.04898.x
3. Angly, F. E., Felts, B., Breitbart, M., Salamon, P., Edwards, R. A., Carlson, C., et al. (2006). The marine viromes of four oceanic regions. PLoS Biol. 4:e368. doi: 10.1371/journal.pbio.0040368
4. Bellec, L., Clerissi, C., Edern, R., Foulon, E., Simon, N., Grimsley, N., et al. (2014). Cophylogenetic interactions between marine viruses and eukaryotic picophytoplankton. BMC Evol. Biol. 14:59. doi: 10.1186/1471-2148-14-59
5. Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., and Wheeler, D. L. (2007). GenBank. Nucleic Acids Res. 35, D21-D25. doi: 10.1093/nar/gkl986
6. Bergh, O., Borsheim, K. Y., Bratbak, G., and Heldal, M. (1989). High abundance of viruses found in aquatic environments. Nature 340, 467-468. doi: 10.1038/340467a0
7. Bettarel, Y., Bouvier, T., and Bouvy, M. (2009). Viral persistence in water as evaluated from a tropical/temperate cross-incubation. J. Plankton Res. 31, 909-916. doi: 10.1093/plankt/fbp041
8. Bratbak, G., Egge, J., and Heldal, M. (1993). Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination algal blooms. Mar. Ecol. Prog. Ser. 93, 39-48. doi: 10.3354/meps093039
9. Breitbart, M., and Rohwer, F. (2005). Here a virus, there a virus, everywhere the same virus? Trends Microbiol. 13, 278-284. doi: 10.1016/j.tim.2005.04.003
10. Brussaard, C. P. (2004). Viral control of phytoplankton populations-a review. J. Eukaryot. Microbiol. 51, 125-138. doi: 10.1111/j.1550-7408.2004.tb00537.x
11. Brussaard, C. P. D., Noordeloos, A. A. M., Sandaa, R.-A., Heldal, M., and Bratbak, G. (2004). Discovery of a dsRNA virus infecting the marine photosynthetic protist Micromonas pusilla. Virology 319, 280-291. doi: 10.1016/j.virol.2003.10.033
12. Capella-Gutierrez, S., Silla-Martinez, J. M., and Gabaldon, T. (2009). trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972-1973. doi: 10.1093/bioinformatics/btp348
13. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336. doi: 10.1038/nmeth.f.303
14. Caporaso, J. G., Lauber, C. L., Walters, W. A., Berg-Lyons, D., Lozupone, C. A., Turnbaugh, P. J., et al. (2011). Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. U.S.A. 108, 4516-4522. doi: 10.1073/pnas.1000080107
15. Chen, F., Wang, K., Huang, S., Cai, H., Zhao, M., Jiao, N., et al. (2009). Diverse and dynamic populations of cyanobacterial podoviruses in the Chesapeake Bay unveiled through DNA polymerase gene sequences. Environ. Microbiol. 11, 2884-2892. doi: 10.1111/j.1462-2920.2009.02033.x
16. Chesson, P. (2000). Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343-366. doi: 10.1146/annurev.ecolsys.31.1.343
17. Chow, C.-E. T., and Fuhrman, J. A. (2012). Seasonality and monthly dynamics of marine myovirus communities: marine myovirus community dynamics at SPOT. Environ. Microbiol. 14, 2171-2183. doi: 10.1111/j.1462-2920.2012.02744.x
18. Clasen, J., Hanson, C., Ibrahim, Y., Weihe, C., Marston, M., and Martiny, J. (2013). Diversity and temporal dynamics of Southern California coastal marine cyanophage isolates. Aquat. Microb. Ecol. 69, 17-31. doi: 10.3354/ame01613
19. Clasen, J. L., and Suttle, C. A. (2009). Identification of freshwater Phycodnaviridae and their potential phytoplankton hosts, using DNA pol sequence fragments and a genetic-distance analysis. Appl. Environ. Microbiol. 75, 991-997. doi: 10.1128/AEM.02024-08
20. Combe, M., and Sanjuán, R. (2014). Variation in RNA virus mutation rates across host cells. PLoS Pathog. 10:e1003855. doi: 10.1371/journal.ppat.1003855
21. Culley, A. I., Lang, A., and Suttle, C. A. (2003). High diversity of unknown picorna-like viruses in the sea. Nature 424, 1054-1057. doi: 10.1038/nature01933
22. Culley, A. I., Lang, A., and Suttle, C. A. (2006). Metagenomic analysis of coastal RNA virus communities. Science 312, 1795-1798. doi: 10.1126/science.1127404
23. Culley, A. I., Mueller, J. A., Belcaid, M., Wood-Charlson, E. M., Poisson, G., and Steward, G. F. (2014). The characterization of RNA viruses in tropical seawater using targeted PCR and metagenomics. MBio 5:e01210-14-e01210-14. doi: 10.1128/mBio.01210-14
24. Culley, A. I., and Steward, G. F. (2007). New genera of RNA viruses in subtropical seawater, inferred from polymerase gene sequences. Appl. Environ. Microbiol. 73, 5937-5944. doi: 10.1128/AEM.01065-07
25. Darriba, D., Taboada, G. L., Doallo, R., and Bangor, D. (2011). ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27, 1164-1165. doi: 10.1093/bioinformatics/btr088
26. Derelle, E., Ferraz, C., Escande, M.-L., Eycheni,é, S., Cooke, R., Piganeau, G., et al. (2008). Life-cycle and genome of OtV5, a large DNA virus of the pelagic marine unicellular green alga Ostreococcus tauri. PLoS ONE 3:e2250. doi: 10.1371/journal.pone.0002250
27. Djikeng, A., Kuzmickas, R., Anderson, N. G., and Spiro, D. J. (2009). Metagenomic analysis of RNA viruses in a fresh water lake. PLoS ONE 4:e7264. doi: 10.1371/journal.pone.0007264
28. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797. doi: 10.1093/nar/gkh340
29. Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461. doi: 10.1093/bioinformatics/btq461
30. Faith, D. P. (1992). Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1-10. doi: 10.1016/0006-3207(92)91201-3
31. Frederickson, C. M., Short, S. M., and Suttle, C. A. (2003). The physical environment affects cyanophage communities in British Columbia inlets. Microb. Ecol. 46, 348-357. doi: 10.1007/s00248-003-1010-2
32. Fuhrman, J. A. (1999). Marine viruses and their biogeochemical and ecological effects. Nature 399, 541-548. doi: 10.1038/21119
33. Gibbons, S. M., Caporaso, J. G., Pirrung, M., Field, D., Knight, R., and Gilbert, J. A. (2013). Evidence for a persistent microbial seed bank throughout the global ocean. Proc. Natl. Acad. Sci. U.S.A. 110, 4651-4655. doi: 10.1073/pnas.1217767110
34. Gobet, A., Böer, S. I., Huse, S. M., van Beusekom, J. E., Quince, C., Sogin, M. L., et al. (2012). Diversity and dynamics of rare and of resident bacterial populations in coastal sands. ISME J. 6, 542-553. doi: 10.1038/ismej.2011.132
35. Heldal, M., and Bratbak, G. (1991). Production and decay of viruses in aquatic environments. Mar. Ecol. Prog. Ser. 72, 205-212. doi: 10.3354/meps072205
36. Holmes, E. (2009). Evolution and Emergence of RNA Viruses. Oxford: Oxford University Press.
37. Huang, S., Wilhelm, S. W., Jiao, N., and Chen, F. (2010). Ubiquitous cyanobacterial podoviruses in the global oceans unveiled through viral DNA polymerase gene sequences. ISME J. 4, 1243-1251. doi: 10.1038/ismej.2010.56
38. Huse, S. M., Dethlefsen, L., Huber, J. A., Mark Welch, D., Welch, D. M., Relman, D. A., et al. (2008). Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet. 4:e1000255. doi: 10.1371/journal.pgen.1000255
39. Ibarbalz, F. M., Pérez, M. V., Figuerola, E. L. M., and Erijman, L. (2014). The bias associated with amplicon sequencing does not affect the quantitative assessment of bacterial community dynamics. PLoS ONE 9:e99722. doi: 10.1371/journal.pone.0099722
40. Jameson, E., Mann, N. H., Joint, I., Sambles, C., and Mühling, M. (2011). The diversity of cyanomyovirus populations along a North-South Atlantic Ocean transect. ISME J. 5, 1713-1721. doi: 10.1038/ismej.2011.54
41. Kemp, P. F., and Aller, J. Y. (2004). Estimating prokaryotic diversity: when are 16 s rDNA libraries large enough? Limnol. Oceanogr. Methods 2, 114-125. doi: 10.4319/lom.2004.2.114
42. Kirchman, D. L., Cottrell, M. T., and Lovejoy, C. (2010). The structure of bacterial communities in the western Arctic Ocean as revealed by pyrosequencing of 16S rRNA genes. Environ. Microbiol. 12, 1132-1143. doi: 10.1111/j.1462-2920.2010.02154.x
43. Klopfer, P. H., and MacArthur, R. H. (1960). Niche size and faunal diversity. Am. Nat. 94, 293-300. doi: 10.1086/282130
44. Koonin, E. V. (1991). The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 72, 2197-2206. doi: 10.1099/0022-1317-72-9-2197
45. Ladau, J., Sharpton, T. J., Finucane, M. M., Jospin, G., Kembel, S. W., O'Dwyer, J., et al. (2013). Global marine bacterial diversity peaks at high latitudes in winter. ISME J. 7, 1669-1677. doi: 10.1038/ismej.2013.37
46. Lang, A. S., Culley, A. I., and Suttle, C. A. (2004). Genome sequence and characterization of a virus (HaRNAV) related to picorna-like viruses that infects the marine toxic bloom-forming alga Heterosigma akashiwo. Virology 320, 206-217. doi: 10.1016/j.virol.2003.10.015
47. Lang, A. S., Rise, M. L., Culley, A. I., and Steward, G. F. (2009). RNA viruses in the sea. FEMS Microbiol. Rev. 33, 295-323. doi: 10.1111/j.1574-6976.2008.00132.x
48. Larsen, A., Flaten, G. A. F., Sandaa, R.-A., Castberg, T., Thyrhaug, R., Erga, S. R., et al. (2004). Spring phytoplankton bloom dynamics in Norwegian coastal waters: microbial community succession and diversity. Limnol. Oceanogr. 49, 180-190. doi: 10.4319/lo.2004.49.1.0180
49. Lawrence, J. E., and Suttle, C. A. (2004). Effect of viral infection on sinking rates of Heterosigma akashiwo and its implications for bloom termination. Aquat. Microb. Ecol. 37, 1-7. doi: 10.3354/ame037001
50. Le Gall, O., Christian, P., Fauquet, C. M., King, A. M. Q., Knowles, N. J., Nakashima, N., et al. (2008). Picornavirales, a proposed order of positive-sense single-stranded RNA viruses with a pseudo-T = 3 virion architecture. Arch. Virol. 153, 715-727. doi: 10.1007/s00705-008-0041-x
51. Lee, C. K., Herbold, C. W., Polson, S. W., Wommack, K. E., Williamson, S. J., McDonald, I. R., et al. (2012). Groundtruthing next-gen sequencing for microbial ecology-biases and errors in community structure estimates from PCR amplicon pyrosequencing. PLoS ONE 7:e44224. doi: 10.1371/journal.pone.0044224
52. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., et al. (2011). CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res. 39, D225-D229. doi: 10.1093/nar/gkq1189
53. Marston, M. F., Taylor, S., Sme, N., Parsons, R. J., Noyes, T. J. E., and Martiny, J. B. H. (2013). Marine cyanophages exhibit local and regional biogeography: biogeography of marine cyanophages. Environ. Microbiol. 15, 1452-1463. doi: 10.1111/1462-2920.12062
54. Mayer, J. A., and Taylor, F. J. R. (1979). A virus which lyses the marine nanoflagellate Micromonas pusilla. Nature 281, 299-301. doi: 10.1038/281299a0
55. Mühling, M., Fuller, N. J., Millard, A., Somerfield, P. J., Marie, D., Wilson, W. H., et al. (2005). Genetic diversity of marine Synechococcus and co-occurring cyanophage communities: evidence for viral control of phytoplankton. Environ. Microbiol. 7, 499-508. doi: 10.1111/j.1462-2920.2005.00713.x
56. Murray, A. G., and Jackson, G. A. (1992). Viral dynamics: a model of the effects of size, shape, motion and abundance of single-celled planktonic organisms and other particles. Mar. Ecol. Prog. Ser. 89, 103-116. doi: 10.3354/meps089103
57. Nagasaki, K., Ando, M., Itakura, S., Imai, I., and Ishida, Y. (1994). Viral mortality in the final stage of Heterosigma akashiwo (Raphidophyceae) red tide. J. Plankton Res. 16, 1595-1599. doi: 10.1093/plankt/16.11.1595
58. Nagasaki, K., Shirai, Y., Takao, Y., Mizumoto, H., Nishida, K., and Tomaru, Y. (2005). Comparison of genome sequences of single-stranded RNA viruses infecting the bivalve-killing dinoflagellate Heterocapsa circularisquama. Appl. Environ. Microbiol. 71, 8888-8894. doi: 10.1128/AEM.71.12.8888-8894.2005
59. Nagasaki, K., Tomaru, Y., Katanozaka, N., Shirai, Y., Nishida, K., Itakura, S., et al. (2004). Isolation and characterization of a novel single-stranded RNA virus infecting the bloom-forming diatom Rhizosolenia setigera. Appl. Environ. Microbiol. 70, 704-711. doi: 10.1128/AEM.70.2.704-711.2004
60. Ng, T. F. F., Marine, R., Wang, C., Simmonds, P., Kapusinszky, B., Bodhidatta, L., et al. (2012). High variety of known and new RNA and DNA viruses of diverse origins in untreated sewage. J. Virol. 86, 12161-12175. doi: 10.1128/JVI.00869-12
61. Noble, R. T., and Fuhrman, J. A. (1997). Virus decay and its causes in coastal waters. Appl. Environ. Microbiol. 63, 77-83.
62. Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., et al. (2013). Vegan: Community Ecology Package. R package version 2.0-10. Available online at: http://CRAN.R-project.org/package=vegan
63. Paradis, E. (2012). Analysis of Phylogenetics and Evolution with R. New York, NY: Springer. doi: 10.1007/978-1-4614-1743-9
64. Parsons, T. R., Maita, Y., and Lalli, C. M. (1984). A Manual of Chemical and Biological Methods for Seawater Analysis. New York, NY: Pergamon Press.
65. Pinto, A. J., and Raskin, L. (2012). PCR biases distort bacterial and archaeal community structure in pyrosequencing datasets. PLoS ONE 7:e43093. doi: 10.1371/journal.pone.0043093
66. Price, M. N., Dehal, P. S., and Arkin, A. P. (2010). FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. doi: 10.1371/journal.pone.0009490
67. Qiu, X., Wu, L., Huang, H., McDonel, P. E., Palumbo, A. V., Tiedje, J. M., et al. (2001). Evaluation of PCR-Generated chimeras, mutations, and heteroduplexes with 16S rRNA gene-based cloning. Appl. Environ. Microbiol. 67, 880-887. doi: 10.1128/AEM.67.2.880-887.2001
68. R Core Team (2014). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available online at: http://www.R-project.org/
69. Reeder, J., and Knight, R. (2010). Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat. Methods 7, 668-669. doi: 10.1038/nmeth0910-668b
70. Rho, M., Tang, H., and Ye, Y. (2010). FragGeneScan: predicting genes in short and error-prone reads. Nucleic Acids Res. 38:e191. doi: 10.1093/nar/gkq747
71. Rodriguez-Brito, B., Li, L., Wegley, L., Furlan, M., Angly, F., Breitbart, M., et al. (2010). Viral and microbial community dynamics in four aquatic environments. ISME J. 4, 739-751. doi: 10.1038/ismej.2010.1
72. Romano, C. M., Lauck, M., Salvador, F. S., Lima, C. R., Villas-Boas, L. S., Araújo, E. S. A., et al. (2013). Inter- and intra-host viral diversity in a large seasonal DENV2 outbreak. PLoS ONE 8:e70318. doi: 10.1371/journal.pone.0070318
73. Sanfaçon, H., Wellink, J., Gall, O., Karasev, A., Vlugt, R., and Wetzel, T. (2009). Secoviridae: a proposed family of plant viruses within the order Picornavirales that combines the families Sequiviridae and Comoviridae, the unassigned genera Cheravirus and Sadwavirus, and the proposed genus Torradovirus. Arch. Virol. 154, 899-907. doi: 10.1007/s00705-009-0367-z
74. Sanjuan, R., Nebot, M. R., Chirico, N., Mansky, L. M., and Belshaw, R. (2010). Viral mutation rates. J. Virol. 84, 9733-9748. doi: 10.1128/JVI.00694-10
75. Schroeder, D. C., Oke, J., Hall, M., Malin, G., and Wilson, W. H. (2003). Virus succession observed during an Emiliania huxleyi bloom. Appl. Environ. Microbiol. 69, 2484-2490. doi: 10.1128/AEM.69.5.2484-2490.2003
76. Shirai, Y., Tomaru, Y., Takao, Y., Suzuki, H., Nagumo, T., and Nagasaki, K. (2008). Isolation and characterization of a single-stranded RNA virus infecting the marine planktonic diatom Chaetoceros tenuissimus Meunier. Appl. Environ. Microbiol. 74, 4022-4027. doi: 10.1128/AEM.00509-08
77. Short, S. M. (2012). The ecology of viruses that infect eukaryotic algae: Algal virus ecology. Environ. Microbiol. 14, 2253-2271. doi: 10.1111/j.1462-2920.2012.02706.x
78. Short, S. M., and Suttle, C. A. (2003). Temporal dynamics of natural communities of marine algal viruses and eukaryotes. Aquat. Microb. Ecol. 32, 107-119. doi: 10.3354/ame032107
79. Sogin, M. L., Morrison, H. G., Huber, J. A., Welch, D. M., Huse, S. M., Neal, P. R., et al. (2006). Microbial diversity in the deep sea and the underexplored "rare biosphere." Proc. Natl. Acad. Sci. U.S.A. 103, 12115-12120. doi: 10.1073/pnas.0605127103
80. Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web servers. Syst. Biol. 57, 758-771. doi: 10.1080/10635150802429642
81. Steward, G. F., Culley, A. I., Mueller, J. A., Wood-Charlson, E. M., Belcaid, M., and Poisson, G. (2012). Are we missing half of the viruses in the ocean? ISME J. 7, 672-679. doi: 10.1038/ismej.2012.121
82. Suttle, C. A. (2007). Marine viruses-major players in the global ecosystem. Nat. Rev. Microbiol. 5, 801-812. doi: 10.1038/nrmicro1750
83. Suttle, C. A. (2005). Viruses in the sea. Nature 437, 356-361. doi: 10.1038/nature04160
84. Suttle, C. A., Chan, A. M., and Cottrell, M. T. (1991). Use of ultrafiltration to isolate viruses from seawater which are pathogens of marine phytoplankton. Appl. Environ. Microbiol. 57, 721-726.
85. Suttle, C. A., and Chen, F. (1992). Mechanisms and rates of decay of marine viruses in seawater. Appl. Environ. Microbiol. 58, 3721-3729.
86. Tai, V., Lawrence, J. E., Lang, A. S., Chan, A. M., Culley, A. I., and Suttle, C. A. (2003). Characterization of HaRNAV, a single-stranded RNA virus causing lysis of Heterosigma akashiwo (Raphidophyceae). J. Phycol. 39, 343-352. doi: 10.1046/j.1529-8817.2003.01162.x
87. Takao, Y., Mise, K., Nagasaki, K., Okuno, T., and Honda, D. (2006). Complete nucleotide sequence and genome organization of a single-stranded RNA virus infecting the marine fungoid protist Schizochytrium sp. J. Gen. Virol. 87, 723-733. doi: 10.1099/vir.0.81204-0
88. Thingstad, T. F. (2000). Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol. Oceanogr. 45, 1320-1328. doi: 10.4319/lo.2000.45.6.1320
89. Tomaru, Y., Katanozaka, N., Nishida, K., Shirai, Y., Tarutani, K., Yamaguchi, M., et al. (2004). Isolation and characterization of two distinct types of HcRNAV, a single-stranded RNA virus infecting the bivalve-killing microalga Heterocapsa circularisquama. Aquat. Microb. Ecol. 34, 207-218. doi: 10.3354/ame034207
90. Tomaru, Y., Takao, Y., Suzuki, H., Nagumo, T., and Nagasaki, K. (2009). Isolation and characterization of a single-stranded RNA virus infecting the bloom-forming diatom Chaetoceros socialis. Appl. Environ. Microbiol. 75, 2375-2381. doi: 10.1128/AEM.02580-08
91. Van Etten, J. L., Meints, R. H., Burbank, D. E., Kuczmarski, D., Cuppels, D. A., and Lane, L. C. (1981). Isolation and characterization of a virus from the intracellular green alga symbiotic with Hydra viridis. Virology 113, 704-711. doi: 10.1016/0042-6822(81)90199-9
92. Wang, K., Wommack, K. E., and Chen, F. (2011). Abundance and distribution of Synechococcus spp. and cyanophages in the Chesapeake Bay. Appl. Environ. Microbiol. 77, 7459-7468. doi: 10.1128/AEM.00267-11
93. Watson, S. J., Welkers, M. R. A., Depledge, D. P., Coulter, E., Breuer, J. M., de Jong, M. D., et al. (2013). Viral population analysis and minority-variant detection using short read next-generation sequencing. Philos. Trans. R. Soc. B Biol. Sci. 368:20120205. doi: 10.1098/rstb.2012.0205
94. Wickham, H. (2009). Ggplot2: Elegant Graphics for Data Analysis. New York, NY: Springer.
95. Wilhelm, S. W., and Suttle, C. A. (1999). Viruses and nutrient cycles in the sea. Bioscience 49, 781-788. doi: 10.2307/1313569
96. Wilkinson, L. (2011). Venneuler: Venn and Euler Diagrams. Available online at: http://CRAN.R-project.org/package=venneuler
97. Winter, C., Bouvier, T., Weinbauer, M. G., and Thingstad, T. F. (2010). Trade-offs between competition and defense specialists among unicellular planktonic organisms: the "killing the winner" hypothesis revisited. Microbiol. Mol. Biol. Rev. 74, 42-57. doi: 10.1128/MMBR.00034-09
98. Yokoyama, R., and Honda, D. (2007). Taxonomic rearrangement of the genus Schizochytrium sensu lato based on morphology, chemotaxonomic characteristics, and 18S rRNA gene phylogeny (Thraustochytriaceae, Labyrinthulomycetes): emendation for Schizochytrium and erection of Aurantiochytrium and Oblongichytrium gen. nov. Mycoscience 48, 199-211. doi: 10.1007/S10267-006-0362-0
99. Zhang, J., and Byrne, C. (1999). Differential priming of RNA templates during cDNA synthesis markedly affects both accuracy and reproducibility of quantitative competitive reverse-transcriptase PCR. Biochem. J. 337, 231-241. doi: 10.1042/0264-6021:3370231
100. Zhou, J., Wu, L., Deng, Y., Zhi, X., Jiang, Y.-H., Tu, Q., et al. (2011). Reproducibility and quantitation of amplicon sequencing-based detection. ISME J. 5, 1303-1313. doi: 10.1038/ismej.2011.11
101. Zingone, A., Dubroca, L., Iudicone, D., Margiotta, F., Corato, F., Ribera d'Alcalà, M., et al. (2009). Coastal phytoplankton do not rest in winter. Estuaries Coasts 33, 342-361. doi: 10.1007/s12237-009-9157-9