Rising to the challenge: Accelerated pace of discovery transforms marine virology

Nature Reviews Microbiology

Volumn 13, Issue 3, 2015, Pages 147-159

  Brum, Jennifer R ^a   Sullivan, Matthew B ^a  

^a University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECOLOGY; ENVIRONMENTAL FACTOR; HUMAN; MARINE VIROLOGY; METAGENOMICS; MICROBIAL METABOLISM; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REPRODUCIBILITY; REVIEW; THEORETICAL MODEL; VIROLOGY; VIRUS CELL INTERACTION; VIRUS CULTURE; BIOTA; PROCEDURES; TRENDS;

SEA WATER;

BIOTA; METAGENOMICS; SEAWATER; VIROLOGY;

EID: 84923568014     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3404     Document Type: Review

References (129)

1. Bergh, O., Borsheim, K. Y., Bratbak, G.&Heldal, M. High abundance of viruses found in aquatic environments. Nature 340, 467-468 (1989).
2. Staley, J.&Konopka, A. Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu. Rev. Microbiol. 39, 321-346 (1985).
3. Proctor, L. M.&Fuhrman, J. A. Viral mortality of marine bacteria and cyanobacteria. Nature 343, 60-62 (1990).
4. Falkowski, P. G., Fenchel, T.&Delong, E. F. The microbial engines that drive Earth's biogeochemical cycles. Science 320, 1034-1039 (2008).
5. Fuhrman, J. in Microbial Ecology of the Oceans (ed. Kirchman, D. L.) Ch. 11 (Wiley-Liss, 2000).
6. Fuhrman, J. A. Marine viruses and their biogeochemical and ecological effects. Nature 399, 541-548 (1999).
7. Wommack, K. E.&Colwell, R. R. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64, 69-114 (2000).
8. Thingstad, T. F. 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 (2000).
9. Suttle, C. A.&Chan, A. M. Marine cyanophages infecting oceanic and coastal strains of Synechococcus: abundance, morphology, cross-infectivity and growth characteristics. Mar. Ecol. Prog. Ser. 92, 99-109 (1993).
10. Waterbury, J. B.&Valois, F. W. Resistance to co-occurring phages enables marine Synechococcus communities to coexist with cyanophages abundant in seawater. Appl. Environ. Microbiol. 59, 3393-3399 (1993).
11. Sullivan, M. B., Waterbury, J. B.&Chisholm, S. W. Cyanophage infecting the oceanic cyanobacterium Prochlorococcus. Nature 424, 1047-1051 (2003).
12. Sullivan, M. B., Coleman, M. L., Weigele, P., Rohwer, F.&Chisholm, S. W. Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol. 3, 790-806 (2005).
13. Rappe, M. S.&Giovannoni, S. J. The uncultured microbial majority. Annu. Rev. Microbiol. 57, 369-394 (2003).
14. DeLong, E. F.&Pace, N. R. Environmental diversity of bacteria and archaea. Syst. Biol. 50, 470-478 (2001).
15. Pace, N. R. A molecular view of microbial diversity and the biosphere. Science 276, 734-740 (1997).
16. Edwards, R. A.&Rohwer, F. Viral metagenomics. Nature Rev. Microbiol. 3, 504-510 (2005).
17. Fuller, N. J., Wilson, W. H., Joint, I. R.&Mann, N. H. Occurrence of a sequence in marine cyanophages similar to that of T4 g20 and its application to PCR-based detection and quantification techniques. Appl. Environ. Microbiol. 64, 2051-2060 (1998).
18. Tetart, F. et al. Phylogeny of the major head and tail genes of the wide-ranging T4-type bacteriophages. J. Bacteriol. 183, 358-366 (2001).
19. Culley, A. I., Lang, A. S.&Suttle, C. A. High diversity of unknown picorna-like viruses in the sea. Nature 424, 1054-1057 (2003).
20. Steward, G. F., Montiel, J. L.&Azam, F. Genome size distributions indicate variability and similarities among marine viral assemblages from diverse environments. Limnol. Oceanogr. 45, 1697-1706 (2000).
21. Wommack, K. E., Ravel, J., Hill, R. T., Chun, J.&Colwell, R. R. Population dynamics of Chesapeake Bay virioplankton: total community analysis by pulsed-field gel electrophoresis. Appl. Environ. Microbiol. 65, 231-240 (1999).
22. Breitbart, M. et al. Genomic analysis of uncultured marine viral communities. Proc. Natl Acad. Sci. USA 99, 14250-14255 (2002).
23. Breitbart, M. et al. Diversity and population structure of a near-shore marine-sediment viral community. Proc. R. Soc. Lond. B. 271, 565-574 (2004).
24. Hurwitz, B. L.&Sullivan, M. B. The Pacific Ocean Virome (POV): A marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS ONE 8, e57355 (2013).
25. Breitbart, M. Marine viruses: truth or dare. Annu. Rev. Mar. Sci. 4, 425-448 (2012).
26. Willner, D.&Hugenholtz, P. From deep sequencing to viral tagging: recent advances in viral metagenomics. Bioessays 35, 436-442 (2013).
27. Brum, J. R. Concentration, production, and turnover of viruses and dissolved DNA pools at Station ALOHA, North Pacific Subtropical Gyre. Aquat. Microb. Ecol. 41, 103-113 (2005).
28. Steward, G. F. et al. Are we missing half of the viruses in the ocean? ISME J. 7, 672-679 (2013).
29. Fuhrman, J. A.&Azam, F. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: Evaluation and field results. Mar. Biol. 66, 109-120 (1982).
30. Angly, F. E. et al. The marine viromes of four oceanic regions. PLoS Biol. 4, 2121-2131 (2006).
31. Steward, G. F.&Preston, C. M. Analysis of a viral metagenomic library from 200 m depth in Monterey Bay, California constructed by direct shotgun cloning. Virol. J. 8, 287-301 (2011).
32. Wommack, K. E., Bhavsar, J.&Ravel, J. Metagenomics: read length matters. Appl. Environ. Microbiol. 74, 1453-1463 (2008).
33. John, S. G. et al. A simple and efficient method for concentration of ocean viruses by chemical flocculation. Environ. Microbiol. Rep. 3, 195-202 (2011).
34. Hurwitz, B. L., Deng, L., Poulos, B. T.&Sullivan, M. B. Evaluation of methods to concentrate and purify ocean virus communities through comparative, replicated metagenomics. Environ. Microbiol. 15, 1428-1440 (2013).
35. Solonenko, S. et al. Sequencing platform and library preparation choices impact viral metagenomes. BMC Genomics 14, 320 (2013).
36. Duhaime, M. B. D., Deng, L., Poulos, B. T.&Sullivan, M. B. 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 (2012).
37. Duhaime, M. B.&Sullivan, M. B. Ocean viruses: rigorously evaluating the metagenomic sample-to-sequence pipeline. Virology 434, 181-186 (2012).
38. Solonenko, S. A.&Sullivan, M. B. in Methods in Enzymology (ed. DeLong, E. F.) Vol. 531 Ch. 8 (Academic Press, 2013).
39. Rusch, D. B. et al. The Sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol. 5, e77 (2007).
40. Holmfeldt, K., Odic, D., Sullivan, M. B., Middelboe, M.&Riemann, L. Cultivated single stranded DNA phages that infect marine Bacteroidetes prove difficult to detect with DNA binding stains. Appl. Environ. Microbiol. 78, 892-894 (2012).
41. Tomaru, Y.&Nagasaki, K. Flow cytometric detection and enumeration of DNA and RNA viruses infecting marine eukaryotic microalgae. J. Oceanogr. 63, 215-221 (2007).
42. Brussaard, C. P. D., Marie, D.&Bratbak, G. Flow cytometric detection of viruses. J. Virol. Methods 85, 175-182 (2000).
43. Brum, J. R., Schenck, R. O.&Sullivan, M. B. Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses. ISME J. 7, 1738-1751 (2013).
44. Bettarel, Y., Sime-Ngando, T., Amblard, C.&Laveran, H. A comparison of methods for counting viruses in aquatic systems. Appl. Environ. Microbiol. 66, 2283-2289 (2000).
45. Hennes, K. P.&Suttle, C. A. Direct counts of viruses in natural waters and laboratory cultures by epifluorescence microscopy. Limnol. Oceanogr. 40, 1050-1055 (1995).
46. Weinbauer, M. G.&Suttle, C. A. Comparison of epifluorescence and transmission electron microscopy for counting viruses in natural marine waters. Aquat. Microb. Ecol. 13, 225-232 (1997).
47. Noble, R. T.&Fuhrman, J. A. Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat. Microb. Ecol. 14, 113-118 (1998).
48. Marie, D., Brussaard, C. P. D., Thyrhaug, R., Bratbak, G.&Vaulot, D. Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl. Environ. Microbiol. 65, 45-52 (1999).
49. Lang, A. S., Rise, M. L., Culley, A. I.&Steward, G. F. RNA viruses in the sea. FEMS Microbiol. Rev. 33, 295-323 (2009).
50. Tucker, K. P., Parsons, R., Symonds, E. M.&Breitbart, M. Diversity and distribution of single-stranded DNA phages in the North Atlantic Ocean. ISME J. 5, 822-830 (2011).
51. Rosario, K., Duffy, S.&Breitbart, M. Diverse circovirus-like genome architectures revealed by environmental metagenomics. J. Gen. Virol. 90, 2418-2424 (2009).
52. Roux, S., Krupovic, M., Poulet, A., Debroas, D.&Enault, F. Evolution and diversity of the Microviridae viral family through a collection of 81 new complete genomes assembled from virome reads. PLoS ONE 7, e40418 (2012).
53. Labonte, J. M.&Suttle, C. A. Previously unknown and highly divergent ssDNA viruses populate the oceans. ISME J. 7, 2169-2177 (2013).
54. Culley, A. I., Lang, A. S.&Suttle, C. A. Metagenomic analysis of coastal RNA virus communities. Science 312, 1795-1798 (2006).
55. Culley, A. I., Suttle, C. A.&Steward, G. F. in Manual of Aquatic Viral Ecology (eds Wilhelm, S. W., Weinbauer, M.G.&Suttle, C.A.) Ch. 19 (ASLO, 2010).
56. Kim, K.-H.&Bae, J.-W. Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl. Environ. Microbiol. 77, 7663-7668 (2011).
57. Gansauge, M.-T.&Meyer, M. Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA. Nature Protoc. 8, 737-748 (2013).
58. Yooseph, S. et al. The Sorcerer II global ocean sampling expedition: expanding the universe of protein families. PLoS Biol. 5, e16 (2007).
59. Ignacio-Espinoza, C. J., Solonenko, S. A.&Sullivan, M. B. The global virome: not as big as we thought? Curr. Opin. Virol. 3, 566-571 (2013).
60. Rohwer, F. Global phage diversity. Cell 113, 141 (2003).
61. Hurwitz, B. L., Brum, J. R.&Sullivan, M. B. Depth-stratified functional and taxonomic niche specialization in the 'core' and 'flexible' Pacific Ocean Virome. ISME J. http://dx.doi.org/10.1038/ismej.2014.143 (2014).
62. Hurwitz, B., Westvald, A., Brum, J.&Sullivan, M. Modeling ecological drivers in marine viral communities using comparative metagenomics and network analyses. Proc. Natl Acad. Sci. USA 111, 10714-10719 (2014).
63. Roux, S. et al. Metavir: a web server dedicated to virome analysis. Bioinformatics 27, 3074-3075 (2011).
64. Seguritan, V. et al. Artificial neural networks trained to detect viral and phage structural proteins. PLoS Comput. Biol. 8, e1002657 (2012).
65. Holmfeldt, K. et al. Twelve previously unknown phage genera are ubiquitous in global oceans. Proc. Natl Acad. Sci. USA 110, 12798-12803 (2013).
66. Sullivan, M. B. et al. Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ. Microbiol. 12, 3035-3056 (2010).
67. Sullivan, M. B. et al. The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial 'mobilome'. Environ. Microbiol. 11, 2935-2951 (2009).
68. Wilhelm, S. W.&Suttle, C. A. Viruses and nutrient cycles in the sea. BioScience 49, 781-788 (1999).
69. Breitbart, M., Thompson, L. R., Suttle, C. A.&Sullivan, M. B. Exploring the vast diversity of marine viruses. Oceanography 20, 135-139 (2007).
70. Clokie, M. et al. Transcription of a 'photosynthetic' T4-type phage during infection of a marine cyanobacterium. Environ. Microbiol. 8, 827-835 (2006).
71. Lindell, D., Jaffe, J. D., Johnson, Z. I., Church, G. M.&Chisholm, S. W. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438, 86-89 (2005).
72. Bragg, J. G.&Chisholm, S. W. Modeling the fitness consequences of a cyanophage-encoded photosynthesis gene. PLoS ONE 3, e3550 (2008).
73. Mann, N. H., Cook, A., Millard, A., Bailey, S.&Clokie, M. Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424, 741 (2003).
74. Hurwitz, B. L., Hallam, S. J.&Sullivan, M. B. Metabolic reprogramming by viruses in the sunlit and dark oceans. Genome Biol. 14, R123 (2013).
75. Modi, S. R., Lee, H. H., Spina, C. S.&Collins, J. J. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499, 219-222 (2013).
76. Sullivan, M. B. et al. Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol. 4, e234 (2006).
77. Lindell, D. et al. Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc. Natl Acad. Sci. USA 101, 11013-11018 (2004).
78. Zeidner, G. et al. Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environ. Microbiol. 7, 1505-1513 (2005).
79. Tzahor, S. et al. A supervised learning approach for taxonomic classification of core-photosystem-II genes and transcripts in the marine environment. BMC Genomics 10, 229 (2009).
80. Anantharaman, K. et al. Sulfur oxidation genes in diverse deep-sea viruses. Science 344, 757-760 (2014).
81. Enav, H., Mandel-Getfreund, Y.&Beja, O. Comparative metagenomic analyses reveal viral-induced shifts of host metabolism towards nucleotide biosynthesis. Microbiome 2, 9 (2014).
82. Sharon, I. et al. Comparative metagenomics of microbial traits within oceanic viral communities. ISME J. 5, 1178-1190 (2011).
83. Roux, S., Krupovic, M., Debroas, D., Forterre, P.&Enault, F. Assessment of viral community functional potential from viral metagenomes may be hampered by contamination with cellular sequences. Open Biol. 3, 130160 (2013).
84. Forterre, P., Soler, N., Krupovic, M., Marguet, E.&Ackermann, H.-W. Fake virus particles generated by fluorescence microscopy. Trends Microbiol. 21, 1-5 (2013).
85. Soler, N., Krupovic, M., Marguet, E.&Forterre, P. Membrane vesicles in natural environments: a major challenge in viral ecology. ISME J. http://dx.doi.org/10.1038/ismej.2014.184 (2014).
86. Biller, S. J. et al. Bacterial vesicles in marine ecosystems. Science 343, 183-186 (2014).
87. Adams, M. K. Bacteriophages (Interscience Publications, 1959).
88. Avrani, S., Wurtzel, O., Sharon, I., Sorek, R.&Lindell, D. Genomic island variability facilitates Prochlorococcus-virus coexistence. Nature 474, 604-608 (2011).
89. Lindell, D. et al. Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449, 83-86 (2007).
90. Marston, M. F. et al. Rapid diversification of coevolving marine Synechococcus and a virus. Proc. Natl Acad. Sci. USA 109, 4544-4549 (2012).
91. Zhao, Y. et al. Abundant SAR11 viruses in the ocean. Nature 494, 357-360 (2013).
92. Kang, I., Oh, H.-M., Kang, D.&Cho, J.-C. Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans. Proc. Natl Acad. Sci. USA 110, 12343-12348 (2013).
93. Karner, M. B., Delong, E. F.&Karl, D. M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507-510 (2001).
94. Prangishvili, D., Forterre, P.&Garrett, R. A. Viruses of the Archaea: a unifying view. Nature Rev. Microbiol. 4, 837-848 (2006).
95. Geslin, C. et al. Analysis of the first genome of a hyperthermophilic marine virus-like particle, PAV1, isolated from Pyrococcus abyssi. J. Bacteriol. 189, 4510-4519 (2007).
96. DeLong, E. F. et al. Community genomics among stratified microbial assemblages in the ocean's interior. Science 311, 496-503 (2006).
97. Mizuno, C. M., Rodriguez-Valera, F., Kimes, N. E.&Ghai, R. Expanding the marine virosphere using metagenomics. PLoS Genet. 9, e1003987 (2013).
98. Rodriguez-Valera, F., Mizuno, C. M.&Ghai, R. Tales from a thousand and one phages. Bacteriophage 4, e28265 (2014).
99. Roux, S. et al. Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell-and meta-genomics. eLife http://dx.doi.org/10.7554/eLife.03125 (2014).
100. Wright, J. J., Konwar, K. M.&Hallam, S. J. Microbial ecology of expanding oxygen minimum zones. Nature Rev. Microbiol. 10, 381-394 (2012).
101. Tadmor, A. D., Ottesen, E. A., Leadbetter, J. R.&Phillips, R. Probing individual environmental bacteria for viruses by using microfluidic digital PCR. Science 333, 58-62 (2011).
102. Allers, E. et al. Single-cell and population level viral infection dynamics revealed by phageFISH, a method to visualize intracellular and free viruses. Environ. Microbiol. 15, 2306-2318 (2013).
103. Deng, L. et al. Contrasting life strategies of viruses that infect photo-and heterotrophic bacteria, as revealed by viral tagging. mBio 3, e00373-12 (2012).
104. Deng, L. et al. Viral tagging reveals discrete populations in Synechococcus viral genome sequence space. Nature 513, 242-245 (2014).
105. Flores, C. O., Meyer, J. R., Valverde, S., Farr, L.&Weitz, J. S. Statistical structure of host-phage interactions. Proc. Natl Acad. Sci. USA 108, E288-E297 (2011).
106. Flores, C. O., Valverde, S.&Weitz, J. S. Multi-scale structure and geographic drivers of cross-infection within marine bacteria and phages. ISME J. 7, 520-532 (2013).
107. Weitz, J. S. et al. Phage-bacteria infection networks. Trends Microbiol. 21, 82-91 (2013).
108. Holmfeldt, K., Howard-Varona, C., Solonenko, N.&Sullivan, M. B. Contrasting genomic patterns and infection strategies of two co-existing Bacteroidetes podovirus genera. Environ. Microbiol. 16, 2501-2513 (2014).
109. Suttle, C. A. Viruses in the sea. Nature 437, 356-361 (2005).
110. Giovannoni, S. et al. Giovannoni et al. reply. Nature 499, E4-E5 (2013).
111. Matson, P. A.&Hunter, M. D. Special feature: The relative contributions to top-down and bottom-up forces in population and community ecology. Ecology 73, 723 (1992).
112. Vage, S., Storesund, J. E.&Thingstad, T. F. SAR11 viruses and defensive host strains. Nature 499, E3-E4 (2013).
113. Rodriguez-Brito, B. et al. Viral and microbial community dynamics in four aquatic environments. ISME J. 4, 739-751 (2010).
114. Weitz, J. S.&Wilhelm, S. W. Ocean viruses and their effects on microbial communities and biogeochemical cycles. F1000 Biol. Rep. 4, 17 (2012).
115. Keller, D. P.&Hood, R. R. Modeling the seasonal autochthonous sources of dissolved organic carbon and nitrogen in the upper Chesapeake Bay. Ecol. Modell. 222, 1139-1162 (2011).
116. Keller, D. P.&Hood, R. R. Comparative simulations of dissolved organic matter cycling in idealized oceanic, coastal, and estuarine surface waters. J. Mar. Syst. 109-110, 109-128 (2013).
117. Gobler, C. J., Hutchins, D. A., Fisher, N. S., Cosper, E. M.&Sanudo-Wilhelmy, S. A. Release and bioavailability of C, N, P, Se, and Fe following viral lysis of a marine chrysophyte. Limnol. Oceanogr. 42, 1492-1504 (1997).
118. Noble, R. T.&Fuhrman, J. A. Breakdown and microbial uptake of marine viruses and other lysis products. Aquat. Microb. Ecol. 20, 1-11 (1999).
119. Reed, D. C., Algar, C. K., Huber, J. A.&Dick, G. J. Gene-centric approach to integrating environmental genomics and biogeochemical models. Proc. Natl Acad. Sci. USA 111, 1879-1884 (2014).
120. Brum, J. R., Morris, J. J., Decima, M.&Stukel, M. R. in Eco-DAS IX Symposium Proceedings (ed. Kemp, P. F.) Ch. 2 (ASLO, 2014).
121. Paul, J. H. Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? ISME J. 2, 579-589 (2008).
122. Cordero, O. X.&Polz, M. F. Explaining microbial genomic diversity in light of evolutionary ecology. Nature Rev. Microbiol. 12, 263-273 (2014).
123. Chow, C.E. T.&Fuhrman, J. A. Seasonality and monthly dynamics of marine myovirus communities. Environ. Microbiol. 14, 2171-2183 (2012).
124. Schlitzer, R. Ocean Data View, http://odv.awi.de (2011).
125. Karsenti, E. et al. A holistic approach to marine eco-systems biology. PLoS Biol. 9, e1001177 (2011).
126. Hingamp, P. et al. Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes. ISME J. 7, 1678-1695 (2013).
127. Needham, D. M. et al. Short-term observations of marine bacterial and viral communities: patterns, connections and resilience. ISME J. 7, 1274-1285 (2013).
128. Chow, C.-E. T., Kim, D. Y., Sachdeva, R., Caron, D. A.&Fuhrman, J. A. Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists. ISME J. 8, 816-829 (2014).
129. Parsons, R. J., Breitbart, M., Lomas, M. W.&Carlson, C. A. Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea. ISME J. 6, 273-284 (2011).