Viruses as Winners in the Game of Life

Annual Review of Virology

Volumn 3, Issue , 2016, Pages 197-214

  Cobián Güemes, Ana Georgina ^a   Youle, Merry ^b   Cantú, Vito Adrian ^c   Felts, Ben ^a   Nulton, James ^a   Rohwer, Forest ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b Rainbow Rock   (United States)

^c SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

Biogeography; Metagenomics; Phage abundance; Phage diversity; Phage ecology; Viruses

Indexed keywords

CONTIG; FRESH WATER; SEA WATER;

ARTICLE; BACTERIOPHAGE; BIOINFORMATICS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENOTYPE; MARINE ENVIRONMENT; METAGENOME; METAGENOMICS; NONHUMAN; PRIORITY JOURNAL; PROKARYOTIC CELL; PROPHAGE; SEDIMENT; SOIL MICROFLORA; VIRUS; VIRUS GENE; VIRUS GENOME; VIRUS LIKE AGENT; CLASSIFICATION; DNA VIRUS; GENETICS; META ANALYSIS; MICROBIOLOGY; RNA VIRUS; VIROLOGY;

BACTERIOPHAGES; DNA VIRUSES; GENOME, VIRAL; GEOLOGIC SEDIMENTS; METAGENOME; RNA VIRUSES; SOIL MICROBIOLOGY;

EID: 84992034884     PISSN: 2327056X     EISSN: 23270578     Source Type: Journal    
DOI: 10.1146/annurev-virology-100114-054952     Document Type: Article

References (89)

1. Staley JT, Konopka A. 1985. Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu. Rev. Microbiol. 39:321-46
2. Hobbie JE, Daley RJ, Jasper S. 1977. Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl. Environ. Microbiol. 33:1225-28
3. Torrella F, Morita RY. 1979. Evidence by electron micrographs for a high incidence of bacteriophage particles in the waters of Yaquina Bay, Oregon: ecological and taxonomical implications. Appl. Environ. Microbiol. 37:774-78
4. Bergh \O, Børsheim KY, Bratbak G, Heldal M. 1989. High abundance of viruses found in aquatic environments. Nature 340:467-68
5. Anesio AM, Mindl B, Laybourn-Parry J, Hodson AJ, Sattler B. 2007. Viral dynamics in cryoconite holes on a high Arctic glacier (Svalbard). J. Geophys. Res. 112:G04S31
6. Bolduc B, Wirth JF, Mazurie A, Young MJ. 2015. Viral assemblage composition in Yellowstone acidic hot springs assessed by network analysis. ISME J. 9:2162-77
7. Ortmann AC, Suttle CA. 2005. High abundances of viruses in a deep-sea hydrothermal vent system indicates viral mediated microbial mortality. Deep-Sea Res. I 52:1515-27
8. Engelhardt T, Kallmeyer J, Cypionka H, Engelen B. 2014. High virus-to-cell ratios indicate ongoing production of viruses in deep subsurface sediments. ISME J. 8:1503-9
9. WhitmanWB, Coleman DC, WiebeWJ. 1998. Prokaryotes: the unseen majority. PNAS 95:6578-83
10. Williamson KE, Radosevich M, Wommack KE. 2005. Abundance and diversity of viruses in six Delaware soils. Appl. Environ. Microbiol. 71:3119
11. Kallmeyer J, Pockalny R, Adhikari RR, Smith DC, D'Hondt S. 2012. Global distribution of microbial abundance and biomass in subseafloor sediment. PNAS 109:16213-16
12. DeLong EF. 2003. Oceans of Archaea. ASM News 69:503-11
13. Rocke E, PachiadakiMG, Cobban A, Kujawinski EB, Edgcomb VP. 2015. Protist community grazing on prokaryotic prey in deep ocean water masses. PLOS ONE 10:e012450
14. Danovaro R, Serresi M. 2000. Viral density and virus-to-bacterium ratio in deep-sea sediments of the Eastern Mediterranean. Appl. Environ. Microbiol. 66:1857
15. Wommack KE, Colwell RR. 2000. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64:69-114
16. Mokili JL, Rohwer F, Dutilh BE. 2012. Metagenomics and future perspectives in virus discovery. Curr. Opin. Virol. 2:63-77
17. Kimura M. 1962. On the probability of fixation of mutant genes in a population. Genetics 47:713
18. Barr JJ, Auro R, Furlan M, Whiteson KL, Erb ML, et al. 2013. Bacteriophage adhering to mucus provide a non-host-derived immunity. PNAS 110:10771-76
19. Kim MS, Park EJ, Roh SW, Bae JW. 2011. Diversity and abundance of single-stranded DNA viruses in human feces. Appl. Environ. Microbiol. 77:8062-70
20. Sender R, Fuchs S, Milo R. 2016. Revised estimates for the number of human and bacteria cells in the body. bioRxiv 036103. doi: 10.1101/036103
21. Haynes M, Rohwer F. 2011. The human virome. In Metagenomics of the Human Body, ed. KE Nelson, pp. 63-77. New York: Springer
22. Tuma RS, BeaudetMP, Jin X, Jones LJ, Cheung CY, et al. 1999. Characterization of SYBR Gold nucleic acid gel stain: a dye optimized for usewith 300-nm ultraviolet transilluminators. Anal. Biochem. 268:278-88
23. Lang AS, Zhaxybayeva O, Beatty JT. 2012. Gene transfer agents: phage-like elements of genetic exchange. Nat. Rev. Microbiol. 10:472-82
24. Jover LF, Effler TC, Buchan A, Wilhelm SW, Weitz JS. 2014. The elemental composition of virus particles: implications for marine biogeochemical cycles. Nat. Rev. Microbiol. 12:519-28
25. Fuhrman JA. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399:541-48
26. Weinbauer MG. 2004. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28:127-81
27. Weitz JS, Stock CA, Wilhelm SW, Bourouiba L, Coleman ML, et al. 2015. A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes. ISME J. 9:1352-64
28. Proctor LM, Fuhrman JA. 1990. Viral mortality of marine bacteria and cyanobacteria. Nature 343:60-62
29. Suttle CA. 2005. Viruses in the sea. Nature 437:356-61
30. Suttle CA. 2007. Marine viruses-major players in the global ecosystem. Nat. Rev. Microbiol. 5:801-12
31. Thingstad TF. 2000. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol. Oceanogr. 45:1320-28
32. Thingstad TF, Pree B, Giske J, Vage S. 2015. What difference does it make if viruses are strain-, rather than species-specific? Front. Microbiol. 6:320
33. Sandaa RA, Gómez-Consarnau L, Pinhassi J, Riemann L, Malits A, et al. 2009. Viral control of bacterial biodiversity-evidence from a nutrient-enriched marine mesocosm experiment. Environ. Microbiol. 11:2585-97
34. Paul JH. 1999. Microbial gene transfer: an ecological perspective. J. Mol. Microbiol. Biotechnol. 1:45-50
35. Frank JA, Lorimer D, Youle M, Witte P, Craig T, et al. 2013. Structure and function of a cyanophageencoded peptide deformylase. ISME J. 7:1150-60
36. Lindell D, Sullivan MB, Johnson ZI, Tolonen AC, Rohwer F, Chisholm SW. 2004. Transfer of photosynthesis genes to and from Prochlorococcus viruses. PNAS 101:11013-18
37. Sullivan MB, Lindell D, Lee JA, Thompson LR, Bielawski JP, Chisholm SW. 2006. Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLOS Biol. 4:e234
38. Goldsmith DB, Crosti G, Dwivedi B, McDaniel LD, Varsani A, et al. 2011. Development of phoH as a novel signature gene for assessing marine phage diversity. Appl. Environ. Microbiol. 77:7730-39
39. Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, et al. 2008. Functional metagenomic profiling of nine biomes. Nature 452:629-32
40. Bose M, Barber RD. 2006. Prophage Finder: a prophage loci prediction tool for prokaryotic genome sequences. In Silico Biol. 6:223-27
41. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. 2011. PHAST: a fast phage search tool. Nucleic Acids Res. 39(Suppl. 2):W347-52
42. McNair K, Bailey BA, Edwards RA. 2012. PHACTS, a computational approach to classifying the lifestyle of phages. Bioinformatics 28:614-18
43. Akhter S, Aziz RK, Edwards RA. 2012. PhiSpy: a novel algorithm for finding prophages in bacterial genomes that combines similarity-and composition-based strategies. Nucleic Acids Res. 40:e126
44. Fouts DE. 2006. Phage-Finder: automated identification and classification of prophage regions in complete bacterial genome sequences. Nucleic Acids Res. 34:5839-51
45. Paul JH. 2008. Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? ISME J. 2:579-89
46. Canchaya C, Fournous G, Chibani-Chennoufi S, Dillmann ML, Brüssow H. 2003. Phage as agents of lateral gene transfer. Curr. Opin. Microbiol. 6:417-24
47. Casas V, Miyake J, Balsley H, Roark J, Telles S, et al. 2006. Widespread occurrence of phage-encoded exotoxin genes in terrestrial and aquatic environments in Southern California. FEMS Microbiol. Lett. 261:141-49
48. Breitbart M, Felts B, Kelley S, Mahaffy JM, Nulton J, et al. 2004. Diversity and population structure of a near-shore marine-sediment viral community. Proc. R. Soc. B 271:565
49. BreitbartM, Salamon P, Andresen B, Mahaffy JM, Segall AM, et al. 2002. Genomic analysis of uncultured marine viral communities. PNAS 99:14250-55
50. BreitbartM, Hewson I, Felts B, Mahaffy JM, Nulton J, et al. 2003. Metagenomic analyses of an uncultured viral community from human feces. J. Bacteriol. 185:6220-23
51. Brum JR, Hurwitz BL, Schofield O, Ducklow HW, Sullivan MB. 2015. Seasonal time bombs: dominant temperate viruses affect Southern Ocean microbial dynamics. ISME J. 10:437-49
52. Adriaenssens EM, Van Zyl L, De Maayer P, Rubagotti E, Rybicki E, et al. 2015. Metagenomic analysis of the viral community in Namib Desert hypoliths. Environ. Microbiol. 17:480-95
53. Roux S, Enault F, Ravet V, Colombet J, Bettarel Y, et al. 2016. Analysis of metagenomic data reveals common features of halophilic viral communities across continents. Environ. Microbiol. 18:889-903
54. Herskowitz I, Hagen D. 1980. The lysis-lysogeny decision of phage γ: explicit programming and responsiveness. Annu. Rev. Genet. 14:399-445
55. Knowles B, Silveira CB, Bailey BA, Barott K, Cantu VA, et al. 2016. Lytic to temperate switching of viral communities. Nature 531:466-70
56. Rohwer F, Edwards R. 2002. The phage proteomic tree: a genome-based taxonomy for phage. J. Bacteriol. 184:4529-35
57. Dwivedi B, Schmieder R, Goldsmith DB, Edwards RA, Breitbart M. 2012. PhiSiGns: an online tool to identify signature genes in phages and design PCR primers for examining phage diversity. BMC Bioinform. 13:37
58. Rohwer F. 2003. Global phage diversity. Cell 113:141
59. Chao A. 1984. Nonparametric estimation of the number of classes in a population. Scand. J. Stat. 11:265-70
60. Ignacio-Espinoza JC, Solonenko SA, Sullivan MB. 2013. The global virome: not as big as we thought? Curr. Opin. Virol. 3:566-71
61. Adriaenssens EM, Cowan DA. 2014. Using signature genes as tools to assess environmental viral ecology and diversity. Appl. Environ. Microbiol. 80:4470-80
62. Zhong Y, Chen F, Wilhelm SW, Poorvin L, Hodson RE. 2002. Phylogenetic diversity of marine cyanophage isolates and natural virus communities as revealed by sequences of viral capsid assembly protein gene g20. Appl. Environ. Microbiol. 68:1576
63. Jameson E, Mann NH, Joint I, Sambles C, MühlingM. 2011. The diversity of cyanomyovirus populations along a north-south Atlantic Ocean transect. ISME J. 5:1713-21
64. Chow CET, Fuhrman JA. 2012. Seasonality and monthly dynamics of marine myovirus communities. Environ. Microbiol. 14:2171-83
65. Dorigo U, Jacquet S, Humbert JF. 2004. Cyanophage diversity, inferred from g20 gene analyses, in the largest natural lake in France, Lake Bourget. Appl. Environ. Microbiol. 70:1017
66. McDaniel LD, delaRosa M, Paul JH. 2006. Temperate and lytic cyanophages from the Gulf of Mexico. J. Mar. Biol. Assoc. U.K. 86:517-27
67. Comeau AM, Krisch HM. 2008. The capsid of the T4 phage superfamily: the evolution, diversity, and structure of some of the most prevalent proteins in the biosphere. Mol. Biol. Evol. 25:1321-32
68. Pagarete A, Chow CE, Johannessen T, Fuhrman J, Thingstad T, Sandaa R. 2013. Strong seasonality and interannual recurrence in marine myovirus communities. Appl. Environ. Microbiol. 79:6253-59
69. Thingstad T, Lignell R. 1997. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol. 13:19-27
70. Breitbart M, Rohwer F. 2005. Here a virus, there a virus, everywhere the same virus? Trends Microbiol. 13:278-84
71. Chenard C, Suttle C. 2008. Phylogenetic diversity of sequences of cyanophage photosynthetic gene psbA in marine and freshwaters. Appl. Environ. Microbiol. 74:5317-24
72. Huang S, Wilhelm SW, Jiao N, Chen F. 2010. Ubiquitous cyanobacterial podoviruses in the global oceans unveiled through viral DNA polymerase gene sequences. ISME J. 4:1243-51
73. Goldsmith DB, Parsons RJ, Beyene D, Salamon P, BreitbartM. 2015. Deep sequencing of the viral phoH gene reveals temporal variation, depth-specific composition, and persistent dominance of the same viral phoH genes in the Sargasso Sea. PeerJ 3:e997
74. Breitbart M, Miyake JH, Rohwer F. 2004. Global distribution of nearly identical phage encoded DNA sequences. FEMS Microbiol. Lett. 236:249-56
75. Short CM, Suttle CA. 2005. Nearly identical bacteriophage structural gene sequences are widely distributed in both marine and freshwater environments. Appl. Environ. Microbiol. 71:480-86
76. Sano E, Carlson S, Wegley L, Rohwer F. 2004. Movement of viruses between biomes. Appl. Environ. Microbiol. 70:5842
77. Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, et al. 2006. The marine viromes of four oceanic regions. PLOS Biol. 4:e368
78. Brum JR, Sullivan MB. 2015. Rising to the challenge: Accelerated pace of discovery transforms marine virology. Nat. Rev. Microbiol. 13:147-59
79. Watkins SC, KuehnleN, Ruggeri CA, MalkiK, BruderK, et al. 2015. Assessment of ametaviromic dataset generated from nearshore Lake Michigan. Mar. Freshw. Res. doi: 10.1071/MF15172
80. YouleM, HaynesM, Rohwer F. 2012. Scratching the surface of biology's dark matter. In Viruses: Essential Agents of Life, ed. GWitzany, pp. 61-81. Dordrecht, Neth.: Springer
81. Tseng CH, Chiang PW, Shiah FK, Chen YL, Liou JR, et al. 2013. Microbial and viral metagenomes of a subtropical freshwater reservoir subject to climatic disturbances. ISME J. 7:2374-86
82. Bankevich A, Nurk S, Antipov D, Gurevich AA, DvorkinM, et al. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19:455-77
83. García-L ópez R, Vázquez-Castellanos JF, Moya A. 2015. Fragmentation and coverage variation in viral metagenome assemblies, and their effect in diversity calculations. Front. Bioeng. Biotechnol. 3:141
84. Fu L, Niu B, Zhu Z, Wu S, Li W. 2012. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28:3150-52
85. Fierer N, Breitbart M, Nulton J, Salamon P, Lozupone C, et al. 2007. Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, archaea, fungi, and viruses in soil. Appl. Environ. Microbiol. 73:7059-66
86. Kim KH, Bae JW. 2011. Amplificationmethods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl. Environ. Microbiol. 77:7663-68
87. Duhaime MB, Sullivan MB. 2012. Ocean viruses: rigorously evaluating the metagenomic sample-tosequence pipeline. Virology 434:181-86
88. Duhaime MB, Deng L, Poulos BT, Sullivan MB. 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. 14:2526-37
89. United Nations. 2016. Population and Vital Statistics Report: Statistical Papers, Ser. A, Vol. LXVIII. New York: United Nations. http://unstats.un.org/unsd/demographic/products/vitstats/Sets/Series- A-2016.pdf