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Chapter 3 : Bacteriophages at the Poles

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Abstract:

This chapter explores the data collected on the importance of bacteriophages to the ecology of the earth's polar regions. It examines the numbers of phage-like particles that have been observed in the ecosystems and their importance in regulating bacterial numbers and the food chain of the extreme oligotrophic environments. To understand the potential impact of bacteriophages on polar ecosystems, it is first necessary to understand the different life choices of phages and how environmental factors are known to affect them. Perhaps not surprisingly, these data suggest that bacteriophages are an important shunt in carbon cycling in the Antarctic regions as well as in the Arctic. Unlike many other studies, the authors conclude that neither bacteriovores nor bacteriophages are important regulators of bacterial numbers but that numbers are regulated by algae blooms and other factors that affect bacterial growth. Pseudolysogeny was first defined by Baess in 1971. In his review, pseudolysogeny was identified as a phage-host interaction in which the phage, following infection of the host, elicits an unstable, nonproductive response. Thus any study that enumerates total virus-like particles (VLPs) must be tempered with the understanding that not all will be infective. The data obtained in this study support the hypothesis that bacteriophages are of quantifiable significance in the carbon-flow cycle of Antarctic oligotrophic lakes. Few researchers have investigated bacteriophages in both the Arctic and Antarctic in the same study. Phylogenetic analysis of their data revealed five previously uncharacterized subgroups of T4-like bacteriophages in many environments, including the Arctic samples.

Citation: Miller R. 2012. Bacteriophages at the Poles, p 62-78. In Miller R, Whyte L (ed), Polar Microbiology: Life in a Deep Freeze. ASM Press, Washington, DC. doi: 10.1128/9781555817183.ch3

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FIGURE 1

The lytic and lysogenic life cycles of bacteriophages. (A) The lytic life cycle, which leads to the production of progeny phages. (B) The temperate life cycle, in which a prophage is established in the host cell, producing a bacterium referred to as a lysogen. The prophage is not transcribed (indicated by the X's), but replicates with the host cell's genome and is partitioned into its daughter cells. Some prophages are integrated into the host genome, while other types are carried as plasmids. Note: The host genome is not illustrated in this figure. (Reprinted from , , with permission from ASM Press.)

Citation: Miller R. 2012. Bacteriophages at the Poles, p 62-78. In Miller R, Whyte L (ed), Polar Microbiology: Life in a Deep Freeze. ASM Press, Washington, DC. doi: 10.1128/9781555817183.ch3
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1. Abedon, S. T. (ed.). 2008. Bacteriophage Ecology: Population Growth, Evolution, and Impact of Bacterial Viruses. Cambridge University Press, Cambridge, United Kingdom.
2. Ackerman, H. W.,, and M. S. DuBow. 1987. Viruses of Prokaryotes: General Properties of Bacteriophages. CRC Press, Boca Raton, FL.
3. Alonso, J. C.,, G. Luder,, A. C. Stiege,, S. Chai,, R. Weise,, and T. A. Trautner. 1997. The complete nucleotide sequence and functional organization of Bacillus subtilis bacteriophage SPP1. Gene 204: 201 212.
4. Angly, G. E.,, B. Felts,, M. Breitbart,, P. Salamon,, R. A. Edwards,, C. Carlson,, A. M. Chan,, M. Haynes,, S. Kelley,, H. Liu,, J. M. Mahaffy,, J. E. Mueller,, J. Nulton,, R. Olson,, R. Parsons,, S. Rayhawk,, C. A. Suttle,, and F. Rohwer. 2006. The marine viromes of four oceanic regions. PLoS Biol. 4: 2121 2131.
5. Ashelford, K. E.,, M. J. Day,, and J. C. Fry. 2003. Elevated abundance of bacteriophage infecting bacteria in soil. Appl. Environ. Microbiol. 69: 285 289.
6. Ashelford, K. E.,, J. C. Fry,, M. J. Bailey,, A. R. Jeffries,, and M. J. Day. 1999. Characterization of six bacteriophages of Serratia liquefaciens CP6 isolated from the sugar beet phytosphere. Appl. Environ. Microbiol. 65: 1959 1965.
7. Baess, I. 1971. Report on a pseudolysogenic mycobacterium and a review of the literature concerning pseudolysogeny. Acta Pathol. Microbiol. Scand. 79: 428 434.
8. Bailey, S.,, M. R. Clokie,, A. Millard,, and N. H. Mann. 2004. Cyanophage infection and photoinhibition in marine cyanobacteria. Res. Microbiol. 155: 720 725.
9. Barksdale, L.,, and S. B. Ardon. 1974. Persisting bacteriophage infections, lysogeny, and phage conversions. Annu. Rev. Microbiol. 28: 265 299.
10. Bergh, Ø.,, K. Y. Børsheim,, G. Bratbak,, and M. Heldal. 1989. High abundance of viruses found in aquatic environments. Nature 340: 467 468.
11. Borriss, M.,, E. Helmke,, R. Hanschke,, and T. Schweder. 2003. Isolation and characterization of marine psychrophilic phage-host systems from Arctic sea ice. Extremophiles 7: 377 384.
12. Borriss, M.,, T. Lombardot,, F. O. Glöckner,, D. Becher,, D. Albrecht,, and T. Schweder. 2007. Genome and proteome characterization of the psychrophilic Flavobacterium bacteriophage 11b. Extremophiles 11: 95 104.
13. Bratbak, G.,, J. K. Egge,, and M. Heldal. 1993. Viral mortality of the marine alga Emiliania huxleyi (Haptophycaea) and termination of algal blooms. Mar. Ecol. Prog. Ser. 93: 39 48.
14. Bratbak, G.,, O. H. Huslund,, M. Heldal,, A. Naess,, and T. Roeggen. 1992. Giant marine viruses? Mar. Ecol. Prog. Ser. 85: 201 202.
15. Bull, J. J.,, J. Millstein,, J. Orcutt,, and H. A. Wichman. 2006. Evolutionary feedback mediated through population density, illustrated with viruses in chemostats. Am. Nat. 167: E39 E51.
16. Canchaya, C.,, C. Proux,, G. Fournous,, A. Bruttin,, and H. Brüssow. 2003. Prophage genomics. Microbiol. Mol. Biol. Rev. 67: 238 276.
17. Cavenagh, M. M.,, and R. V. Miller. 1986. Specialized transduction of Pseudomonas aeruginosa PAO by bacteriophage D3. J. Bacteriol. 165: 448 452.
18. Chénard, C.,, and C. A. Suttle. 2008. Phylogenetic diversity of sequences of cyanophage photosynthetic gene phbA in marine and freshwaters. Appl. Environ. Microbiol. 74: 5317 5324.
19. Clokie, M. R.,, H. Shan,, S. Bailey,, Y. Jia,, H. M. Krisch,, S. West,, and N. H. Mann. 2006. Transcription of “photosynthetic” T4-type phage during infection of a marine cyanobacterium. Environ. Microbiol. 8: 827 835.
20. Dodds, J. A., and A. Cole. 1980. Microscopy and biology of Uronema gigas, a filamentous eukaryotic green algae, and its associated tailed virus-like particle. Virology 100: 156 165.
21. Edlin, G.,, L. Lin,, and R. Kudrna. 1975. λ-lysogens of E. coli reproduce more rapidly than non-lysogens. Nature 255: 735 737.
22. Evans, C.,, I. Pearce,, and C. P. Brussaard. 2009. Viral-mediated lysis of microbes and carbon release in the sub-Antarctic and Polar Frontal zones of the Australian Southern Ocean. Environ. Microbiol. 11: 2924 2934.
23. Farrah, S. R., 1987. Ecology of phage in freshwater environments, p. 125 136. In S. M. Goyal,, C. P. Gerba,, and G. Bitton (ed.), Phage Ecology. John Wiley and Sons, New York, NY.
24. Filée, J.,, F. Tétart,, C. A. Suttle,, and H. M. Krisch. 2005. Marine T4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere. Proc. Natl. Acad. Sci. USA 102: 12471 12476.
25. Frye, J. G.,, S. Porwollik,, F. Blackmer,, P. Cheng,, and M. McClelland. 2005. Host gene expression changes and DNA amplification during temperate phage induction. J. Bacteriol. 187: 1485 1492.
26. Fuhrman, J., 1992. Bacterioplankton roles in cycling of organic matter: the microbial food web, p. 361 383. In P. G. Falkowski, and A. D. Woodhead (ed.), Primary Productivity and Biogeochemical Cycles in the Sea. Plenum Press, New York, NY.
27. Gowing, M. M.,, D. L. Garrison,, A. H. Gibson,, J. M. Rupp,, M. O. Jeffries,, and C. H. Fritsen. 2004. Bacterial and viral abundance in Ross Sea summer pack ice communities. Mar. Ecol. Prog. Ser. 279: 3 12.
28. Gowing, M. M.,, B. E. Riggs,, D. L. Garrison,, A. H. Gibson,, and M. O. Jeffries. 2002. Large viruses in Ross Sea late autumn pack ice habitats. Mar. Ecol. Prog. Ser. 241: 1 11.
29. Guixa-Boixereu, N.,, J. I. Calderón-Paz,, J. Heldal,, G. Bratbak,, and C. Pedrnós-Alió. 1996. Viral lysis and bacterivory as prokaryotic loss factors along a salinity gradient. Aquat. Microb. Ecol. 11: 215 227.
30. Guixa-Boixereu, N.,, D. Vaqué,, J. M. Gasol,, J. Sánchez-Cámara,, and C. Pedrós-Alió. 2002. Viral distribution and activity in Antarctic waters. Deep Sea Res. Part 2 Top. Stud. Oceanogr. 49: 827 845.
31. Hendrix, R. W.,, M. C. M. Smith,, R. N. Burns,, M. E. Ford,, and G. F. Hatfull. 1999. Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage. Proc. Natl. Acad. Sci. USA 96: 2192 2197.
32. Hewson, I.,, J. M. O’Neill,, J. A. Fuhrman,, and W. C. Dennison. 2001. Virus-like particle distribution and abundance in sediments and overlying waters along eutrophication gradients in two subtropical estuaries. Limnol. Oceanogr. 47: 1734 1746.
33. Hofer, J. S.,, and R. Sommaruga. 2001. Seasonal dynamics of viruses in an alpine lake: importance of filamentous forms. Aquat. Microb. Ecol. 26: 1 11.
34. Holmes, R. K.,, and L. Barksdale. 1970. Comparative studies with tox + and tox - corynebacteriophages. J. Virol. 5: 783 794.
35. Hyman, P.,, and S. T. Abedon,. 2008. Phage ecology of bacterial pathogenesis, p. 353 385. In S. T. Abedon (ed.), Bacteriophage Ecology: Population Growth, Evolution, and Impact of Bacterial Viruses. Cambridge University Press, Cambridge, United Kingdom.
36. Ivánovics, G.,, V. Gaál,, E. Nagy,, B. Prágai,, and M. Simon Jr. 1976. Studies on negacinogeny in Bacillus cereus. II. Bacillus cereus isolates characterized by prophage-controlled production of megacin A (phospholipase A). Acta Microbiol. Acad. Sci. Hung. 23: 283 291.
37. Karaolis, D. K. R.,, S. Somara,, D. R. Maneval Jr.,, J. A. Johnson,, and J. B. Kaper. 1999. A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. Nature 199: 375 379.
38. Koch, A. L. 1971. The adaptive responses of Escherichia coli to a feast and famine existence. Adv. Microb. Physiol. 6: 147 217.
39. Koch, A. L., 1979. Microbial growth in low concentrations of nutrients, p. 261 279. In M. Shilo (ed.), Strategies of Microbial Life in Extreme Environments (Berlin: Dahlem Konferenzen). Verlag Chemie, Weinheim, Germany.
40. Kokjohn, T. A.,, G. S. Sayler,, and R. V. Miller. 1991. Attachment and replication of Pseudomonas aeruginosa bacteriophages under conditions simulating aquatic environments. J. Gen. Microbiol. 137: 661 666.
41. Laybourn-Parry, J.,, J. S. Hofer,, and R. Sommaruga. 2001. Viruses in the plankton of freshwater and saline Antarctic lakes. Freshw. Biol. 46: 1279 1287.
42. Laybourn-Parry, J.,, W. A. Marshall,, and N. J. Madan. 2007. Viral dynamics and patterns of lysogeny in saline Antarctic lakes. Polar Biol. 30: 351 358.
43. Lenski, R. E. 1988. Dynamics of interactions between bacteria and virulent bacteriophage. Adv. Microb. Ecol. 10: 99 108.
44. Lin, L.,, R. Bitner,, and G. Edlin. 1977. Increased reproductive fitness of Escherichia coli lambda lysogens. J. Virol. 21: 554 559.
45. Lindell, D.,, J. D. Jaffe,, Z. I. Johnson,, G. M. Church,, and S. W. Chisholm. 2005. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438: 86 89.
46. Lindell, D.,, M. B. Sullivan,, Z. I. Johnson,, A. C. Tolonen,, F. Rohwer,, and S. W. Chisholm. 2004. Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc. Natl. Acad. Sci. USA 101: 11013 11018.
47. López-Bueno, A.,, J. Tamames,, D. Velázquez,, A. Moya,, A. Quesada,, and A. Alcamí. 2009. High diversity of the viral community from an Antarctic lake. Science 326: 858 861.
48. Madan, N. J.,, W. A. Marshall,, and J. Laybourn-Parry. 2005. Virus and microbial loop dynamics over an annual cycle in three contrasting Antarctic lakes. Freshw. Biol. 50: 1291 1300.
49. Mahenthiralingam, E., 2004. Gene associations in bacterial pathogenesis: pathogenicity islands and genomic deletions, p. 249 274. In R. V. Miller, and M. J. Day (ed.), Microbial Evolution: Gene Establishment, Survival, and Exchange. ASM Press, Washington, DC.
50. Mann, N. H.,, A. Cook,, A. Millard,, S. Bailey,, and M. Clokie. 2003. Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424: 741.
51. Marchant, J.,, A. Davidson,, S. Wright,, and J. Glazebrook. 2000. The distribution and abundance of viruses in the Southern Ocean during spring. Antarct. Sci. 12: 414 417.
52. Martinez-Molina, E.,, and J. Olivares. 1979. Antibiotic production by Pseudomonas reptilivora as a phage conversion. Can. J. Microbiol. 25: 1108 1110.
53. Maurice, C. F.,, T. Bouvier,, J. Comte,, F. Guillemette,, and P. A. del Giorgio. 2010. Seasonal variations of phage life strategies and bacterial physiological states in three northern temperate lakes. Environ. Microbiol. 12: 628 641.
54. Middelboe, M. 2000. Bacterial growth rate and marine virus-host dynamics. Microb. Ecol. 40: 114 124.
55. Middelboe, M.,, T. G. Nielsen,, and P. K. Bjørnsen. 2002. Viral and bacterial production in the North Water; in situ measurements, batch-culture experiments and characterization and distribution of a virus-host system. Deep Sea Res. Part 2 Top. Stud. Oceanogr. 49: 5063 5079.
56. Miller, E. S.,, J. F. Heidelberg,, J. A. Eisen,, W. C. Nelson,, A. S. Durkin,, A. Ciecko,, T. V. Feldblyum,, O. White,, I. T. Paulsen,, W. C. Nierman,, J. Lee,, B. Szczypinski,, and C. M. Fraser. 2003. Complete genome sequence of the broad-host-range vibriophage KVP40: comparative genomics of a T4-related bacteriophage. J. Bacteriol. 185: 5220 5233.
57. Miller, R. V. 1998a. Bacterial gene swapping in nature. Sci. Am. 278: 66 71.
58. Miller, R. V., 1998b. Methods for enumeration and characterization of bacteriophages from environmental samples, p. 218 235. In R. Burlage (ed.), Techniques in Microbial Ecology. Oxford University Press, Oxford, United Kingdom.
59. Miller, R. V. 2001. Environmental bacteriophage-host interactions: factors contributing to natural transduction. Antonie van Leeuwenhoek 79: 141 147.
60. Miller, R. V., 2004. Bacteriophage-mediated transduction: an engine for change and evolution, p. 144 157. In R. V. Miller, and M. J. Day (ed.), Microbial Evolution: Gene Establishment, Survival, and Exchange. ASM Press, Washington, DC.
61. Miller, R. V., 2006. Marine phages, p. 535 544. In R. Calendar (ed.), The Bacteriophages, 2nd ed. Oxford University Press, New York, NY.
62. Miller, R. V.,, and M. J. Day (ed.). 2004a. Microbial Evolution: Gene Establishment, Survival, and Exchange. ASM Press, Washington, DC.
63. Miller, R. V.,, and M. J. Day,. 2004b. Horizontal gene transfer and the real world, p. 173 177. In R. V. Miller, and M. J. Day (ed.), Microbial Evolution: Gene Establishment, Survival, and Exchange. ASM Press, Washington, DC.
64. Miller, R. V.,, and M. J. Day,. 2008. Contribution of lysogeny, pseudolysogeny, and starvation to phage ecology, p. 114 143. In S. T. Abedon (ed.), Bacteriophage Ecology: Population Growth, Evolution, and Impact of Bacterial Viruses. Cambridge University Press, Cambridge, United Kingdom.
65. Miller, R. V.,, and S. Ripp,. 1998. The importance of pseudolysogeny to in situ bacteriophage-host interactions, p. 179 191. In M. Syvanen, and C. I. Kado (ed.), Horizontal Gene Transfer. Chapman & Hall, London, United Kingdom.
66. Miller, R. V.,, and S. A. Ripp,. 2002. Pseudolysogeny: a bacteriophage strategy for increasing longevity in situ, p. 81 91. In M. Syvanen, and C. I. Kado (ed.), Horizontal Gene Transfer, 2nd ed. Academic Press, San Diego, CA.
67. Miller, R. V.,, S. Ripp,, J. Replicon,, O. A. Ogunseitan,, and T. A. Kokjohn,. 1992 Virus-mediated gene transfer in freshwater environments, p. 50 62. In M. J. Gauthier (ed.), Gene Transfers and Environment. Springer, Berlin, Germany.
68. Miller, R. V.,, and G. S. Sayler,. 1992. Bacteriophage-host interactions in aquatic systems, p. 176 193. In E. M. Wellington, and J. D. van Elsas (ed.), Genetic Interactions among Microorganisms in the Natural Environment. Pergamon Press, Oxford, United Kingdom.
69. Moebus, K., 1987. Ecology of marine bacteriophages, p. 136 156. In S. M. Goyal,, C. P. Gerba,, and G. Bitton (ed.), Phage Ecology. John Wiley and Sons, New York, NY.
70. Moebus, K. 1996. Marine bacteriophage reproduction under nutrient-limited growth of host bacteria. I. Investigations with six phages. Mar. Ecol. Prog. Ser. 144: 1 12.
71. Morita, R. Y. (ed.). 1997. Bacteria in Oligotrophic Environments: Starvation-Survival Lifestyle. Chapman & Hall, New York, NY.
72. Noble, R. T.,, and J. A. Fuhrman. 1997. Virus decay and its causes in coastal waters. Appl. Environ. Microbiol. 63: 77 83.
73. Ogunseitan, O. A.,, G. S. Sayler,, and R. V. Miller. 1990. Dynamic interactions of Pseudomonas aeruginosa and bacteriophages in lake water. Microb. Ecol. 19: 171 185.
74. Ortmann, A. C.,, J. E. Lawrence,, and C. A. Suttle. 2002. Lysogeny and lytic viral production during a bloom of cyanobacterium Synechococcus spp. Microb. Ecol. 43: 225 231.
75. Payet, J. P.,, and C. A. Suttle. 2008. Physical and biological correlates of virus dynamics in the southern Beaufort Sea and Amundsen Gulf. J. Mar. Syst. 74: 933 945.
76. Pearce, I.,, A. T. Davidson,, E. M. Bell,, and S. Wright. 2007. Seasonal changes in the concentration and metabolic activity of bacteria and viruses at an Antarctic coastal site. Aquat. Microb. Ecol. 47: 11 23.
77. Proctor, L. M.,, A. Okubo,, and J. A. Fuhrman. 1993. Calibrating estimates of phage-induced mortality in marine bacteria: ultrastructural studies of marine bacteriophage development from one-step growth experiments. Microb. Ecol. 25: 161 182.
78. Ptashne, M. 2004. A Genetic Switch: Phage Lambda Revisited, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
79. Replicon, J.,, A. Frankfater,, and R. V. Miller. 1995. A continuous culture model to examine factors that affect transduction among Pseudomonas aeruginosa strains in freshwater environments. Appl. Environ. Microbiol. 61: 3359 3366.
80. Ripp, S.,, and R. V. Miller. 1997. The role of pseudolysogeny in bacteriophage-host interactions in a natural freshwater environment. Microbiology 143: 2065 2070.
81. Ripp, S.,, and R. V. Miller. 1998. Dynamics of pseudolysogenic response in slowly growing cells of Pseudomonas aeruginosa. Microbiology 144: 2225 2232.
82. Rocha, E. P. C.,, A. Danchin,, and A. Viari. 2001. The evolutionary role of restriction and modification systems as revealed by comparative genome analysis. Genome Res. 11: 946 958.
83. Rohwer, F.,, A. Segall,, G. Steward,, V. Seguritan,, M. Breitbart,, F. Wolven,, and F. Azam. 2000. The complete genomic sequence of marine phage Roseophage SIO1 shares homology with nonmarine phages. Limnol. Oceanogr. 45: 408 418.
84. Säwström, C.,, M. A. Anesio,, W. Granéli,, and J. Laybourn-Parry. 2007a. Seasonal viral loop dynamics in two large ultraoligotrophic Antarctic freshwater lakes. Microb. Ecol. 53: 1 11.
85. Säwström, C.,, J. Laybourn-Parry,, W. Granéli,, and A. M. Anesio. 2007b. Heterotrophic bacterial and viral dynamics in Arctic freshwaters: results from a field study and nutrient-temperature manipulation experiments. Polar Biol. 30: 1407 1415.
86. Säwström, C.,, W. Granéli,, J. Laybourn-Parry,, and A. M. Anesio. 2007c. High viral infection rates in Antarctic and Arctic bacterioplankton. Environ. Microbiol. 9: 250 255.
87. Säwström, C.,, P. Mumford,, W. Marshall,, A. Hodson,, and J. Laybourn-Parry. 2002. The microbial communities and primary productivity of cryoconite holes in an Arctic glacier (Svalbard 79°N). Polar Biol. 25: 591 596.
88. Säwström, C.,, I. Pearce,, A. T. Davidson,, P. Rosén,, and J. Laybourn-Parry. 2008. Influence of environmental conditions, bacterial activity and viability on the viral component in 10 Antarctic lakes. FEMS Microbiol. Ecol. 63: 12 22.
89. Saye, D. J.,, and R. V. Miller,. 1989. The aquatic environment: consideration of horizontal gene transmission in a diversified habitat, p. 223 259. In S. B. Levy, and R. V. Miller (ed.), Gene Transfer in the Environment. McGraw-Hill, New York, NY.
90. Saye, D. J.,, O. Ogunseitan,, G. S. Sayler,, and R. V. Miller. 1987. Potential for transduction of plasmids in a natural freshwater environment: effect of plasmid donor concentration and a natural microbial community on transduction in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 53: 987 995.
91. Schrader, H. S.,, J. O. Schrader,, J. J. Walker,, N. B. Bruggeman,, J. M. Vanderloop,, J. J. Shaffer,, and T. A. Kokjohn,. 1997a. Effects of host starvation on bacteriophage dynamics, p. 368 385. In R. Y. Morita (ed.), Bacteria in Oligotrophic Environments: Starvation-Survival Lifestyle. Chapman & Hall, New York, NY.
92. Schrader, H. S.,, J. O. Schrader,, J. J. Walker,, T. A. Wolf,, K. W. Nickerson,, and T. A. Kokjohn. 1997b. Bacteriophage infection and multiplication occur in Pseudomonas aeruginosa starved for 5 years. Can. J. Microbiol. 43: 1157 1163.
93. Short, C. M.,, and C. A. Suttle. 2005. Nearly identical bacteriophage structural gene sequences are widely distributed in both marine and freshwater environments. Appl. Environ. Microbiol. 71: 480 486.
94. Smith, E.,, A. C. Wolters,, H. Lee,, J. T. Trevors,, and J. D. van Elsas. 1996. Interactions between a genetically marked Pseudomonas fluorescens strain and bacteriophage ϕR2f in soil: effects of nutrients, alginate encapsulation, and the wheat rhizosphere. Microb. Ecol. 31: 125 140.
95. Steward, G. F.,, D. C. Smith,, and F. Azam. 1996. Abundance and production of bacteria and viruses in the Bering and Chukchi Seas. Mar. Ecol. Prog. Ser. 131: 287 300.
96. Sullivan, M. B.,, M. L. Coleman,, P. Weigele,, R. Rohwer,, and S. W. Chisholm. 2005. Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol. 3: e144.
97. Thingstad, T. F.,, G. Bratbak,, and M. Heldal,. 2008. Aqauatic phage ecology, p. 251 280. In S. T. Abedon (ed.), Bacteriophage Ecology: Population Growth, Evolution, and Impact of Bacterial Viruses. Cambridge University Press, Cambridge, United Kingdom.
98. Wells, L. E.,, and J. W. Deming. 2006a. Significance of bacterivory and viral lysis in bottom waters of Franklin Bay, Canadian Arctic, during winter. Aquat. Microb. Ecol. 43: 209 221.
99. Wells, L. E.,, and J. W. Deming. 2006b. Modelled and measured dynamics of viruses in Arctic winter sea-ice brines. Environ. Microbiol. 8: 1115 1121.
100. Wichels, A.,, S. S. Biel,, H. R. Gederblom,, T. Brinkhoff,, G. Muyzer,, and C. Schütt. 1998. Bacteriophage diversity in the North Sea. Appl. Environ. Microbiol. 64: 4128 4133.
101. Williams, S.,, A. Mortimer,, and L. Manchester,. 1987. Ecology of soil bacteriophages, p. 136 156. In S. M. Goyal,, C. P. Gerba,, and G. Bitton (ed.), Phage Ecology. John Wiley and Sons, New York, NY.
102. Williamson, K. E.,, M. Radosevich,, D. W. Smith,, and K. E. Wommack. 2007. Incidence of lysogeny within temperate and extreme soil environments. Environ. Microbiol. 9: 2563 2574.
103. Wilson, W. H.,, N. G. Carr,, and N. H. Mann. 1996. The effect of phosphate status on the kinetics of cyanophage infection in the oceanic cyanobacterium Synechococcus sp. WH7803. J. Phycol. 32: 506 516.
104. Wilson, W. H.,, D. Lane,, D. A. Pearce,, and J. C. Ellis-Evans. 2000. Transmission electron microscope analysis of virus-like particles in the freshwater lakes of Signy Island, Antarctica. Polar Biol. 23: 657 660.
105. Wilson, W. H.,, S. Turner,, and N. H. Mann. 1998. Population dynamics of phytoplankton and viruses in a phosphate-limited mesocosm and their effect on DMSP and DMS production. Estuar. Coast. Shelf Sci. 46: 49 59.
106. Winter, C.,, G. J. Herndl,, and M. G. Weinbauer. 2004. Diel cycles in viral infection of bacterioplankton in the North Sea. Aquat. Microb. Ecol. 35: 207 216.
107. Wommack, K. E.,, and R. R. Colwell. 2000. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64: 69 114.
108. Zeidner, G.,, J. P. Bielawski,, M. Shmoish,, D. J. Scanlan,, G. Sabehi,, and O. Beja. 2005. Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environ. Microbiol. 7: 1505 1513.

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