Factors affecting virus dynamics and microbial host-virus interactions in marine environments

FEMS Microbiology Ecology

Volumn 89, Issue 3, 2014, Pages 495-515

  Mojica, Kristina D A ^a   Brussaard, Corina P D ^a,b  

^a ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Heterotrophic prokaryotes; Marine microorganisms; Marine viruses; Phytoplankton; Virus host interactions

Indexed keywords

SEA WATER;

ENVIRONMENTAL ASPECTS AND RELATED PHENOMENA; GROWTH, DEVELOPMENT AND AGING; ORGANISMAL INTERACTION; SALINITY; TEMPERATURE; ULTRAVIOLET RADIATION; VIRAL PHENOMENA AND FUNCTIONS; VIROLOGY; VIRUS;

ECOLOGICAL AND ENVIRONMENTAL PROCESSES; MICROBIAL INTERACTIONS; SALINITY; SEAWATER; TEMPERATURE; ULTRAVIOLET RAYS; VIRUS PHYSIOLOGICAL PHENOMENA; VIRUSES;

PROKARYOTA;

EID: 84906809090     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12343     Document Type: Review

References (179)

1. Abedon ST (2012) Spatial vulnerability: bacterial arrangements, microcolonies, and biofilms as responses to low rather than high phage densities. Viruses 4: 663-687.
2. Anderson RE, Brazelton WJ & Baross JA (2011) Is the genetic landscape of the deep subsurface biosphere affected by viruses? Front Microbiol 2: 219.
3. Baudoux A & Brussaard CPD (2005) Characterization on different viruses infecting the marine harmful algal bloom species Phaeocystis globosa. Virology 341: 80-90.
4. Baudoux AC & Brussaard CPD (2008) Influence of irradiance on virus-algal host interactions. J Phycol 44: 902-908.
5. Bettarel Y, Dolan JR, Hornak K et al. (2002) Strong, weak, and missing links in a microbial community of the NW Mediterranean Sea. FEMS Microbiol Ecol 42: 451-462.
6. Bettarel Y, Bouvier T, Bouvier C et al. (2011) Ecological traits of planktonic viruses and prokaryotes along a full-salinity gradient. FEMS Microbiol Ecol 76: 360-372.
7. Bolnick DI, Amarasekare P, Araujo MS et al. (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26: 183-192.
8. Bongiorni L, Armeni M, Corinaldesi C, Dell'Anno A, Pusceddu A & Danovaro R (2007) Viruses, prokaryotes and biochemical composition of organic matter in different types of mucilage aggregates. Aquat Microb Ecol 49: 15-23.
9. Booth CR, Morrow JH, Coohill TP et al. (1997) Impacts of solar UVR on aquatic microorganisms. Photochem Photobiol 65: 252-253.
10. Borriss M, Helmke E, Hanschke R & Schweder T (2003) Isolation and characterization of marine psychrophilic phage-host systems from Artic sea ice. Extremophiles 7: 377-384.
11. Borsheim KY (1993) Native marine bacteriophages. FEMS Microbiol Ecol 102: 141-159.
12. Bowman JP, Gosink JJ, McCammon SA et al. (1998) Colwellia demingiae sp. nov., Colwellia hornerae sp. nov., Colwellia rossensis sp. nov. and Colwellia psychrotropica sp. nov.: psychrophilic Antarctic species with the ability to synthesize docosahexaenoic acid (22: 6 omega 3). Int J Syst Bacteriol 48: 1171-1180.
13. Bratbak G, Egge JK & Heldal M (1993) Viral mortality of the marine alga Emiliania-huxleyi (Haptophyceae) and termination of algal blooms. Mar Ecol Prog Ser 93: 39-48.
14. Bratbak G, Jacobsen A, Heldal M, Nagasaki K & Thingstad F (1998) Virus production in Phaeocystis pouchetii and its relation to host cell growth and nutrition. Aquat Microb Ecol 16: 1-9.
15. Brown AD (1964) Aspects of bacterial response to ionic environment. Bacteriol Rev 28: 296-329.
16. Brown CM, Campbell DA & Lawrence JE (2007) Resource dynamics during infection of Micromonas pusilla by virus MpV-Sp1. Environ Microbiol 9: 2720-2727.
17. Brussaard CPD, Kempers RS, Kop AJ, Riegman R & Heldal M (1996) Virus-like particles in a summer bloom of Emiliania huxleyi in the North Sea. Aquat Microb Ecol 10: 105-113.
18. Brussaard CPD, Noordeloos AAM, Sandaa RA, Heldal M & Bratbak G (2004) Discovery of a dsRNA virus infecting the marine photosynthetic protist Micromonas pusilla. Virology 319: 280-291.
19. Brussaard CPD, Kuipers B & Veldhuis MJW (2005a) A mesocosm study of Phaeocystis globosa population dynamics - I. Regulatory role of viruses in bloom control. Harmful Algae 4: 859-874.
20. Brussaard CPD, Mari X, Van Bleijswijk JDL & Veldhuis MJW (2005b) A mesocosm study of Phaeocystis globosa (Prymnesiophyceae) population dynamics II. Significance for the microbial community. Harmful Algae 4: 875-893.
21. Brussaard CPD, Bratbak G, Baudoux AC & Ruardij P (2007) Phaeocystis and its interaction with viruses. Biogeochemistry 83: 201-215.
22. Cattaneo R, Rouviere C, Rassoulzadegan F & Weinbauer MG (2010) Association of marine viral and bacterial communities with reference black carbon particles under experimental conditions: an analysis with scanning electron, epifluorescence and confocal laser scanning microscopy. FEMS Microbiol Ecol 74: 382-396.
23. Chen PK, Citarella RV, Salazar O & Colwell RR (1966) Properties of two marine bacteriophages. J Bacteriol 91: 1136-1139.
24. Chretinennot-Dinet M-J, Giraud-Guille M-M, Vaulot D, Putaux J-L, Saito Y & Chanzy H (1997) The chitinous nature of filaments ejected by Phaeocystis (Prymnesiophyceae). J Phycol 33: 666-672.
25. Clasen JL & Elser JJ (2007) The effect of host Chlorella NC64A carbon: phosphorus ratio on the production of Paramecium bursaria Chlorella Virus-1. Freshw Biol 52: 112-122.
26. Cliver DO & Herrmann JE (1972) Proteolytic and microbial inactivation of enteroviruses. Water Res 6: 797-805.
27. Clokie MRJ & Mann NH (2006) Marine cyanophages and light. Environ Microbiol 8: 2074-2082.
28. Clokie MRJ, Millard AD, Mehta JY & Mann NH (2006) Virus isolation studies suggest short-term variations in abundance in natural cyanophage populations of the Indian Ocean. J Mar Biol Assoc UK 86: 499-505.
29. Cochran PK & Paul JH (1998) Seasonal abundance of lysogenic bacteria in a subtropical estuary. Appl Environ Microbiol 64: 2308-2312.
30. Cochran PK, Kellogg CA & Paul JH (1998) Prophage induction of indigenous marine lysogenic bacteria by environmental pollutants. Mar Ecol Prog Ser 164: 125-133.
31. Cordova A, Deserno M, Gelbart WM & Ben-Shaul A (2003) Osmotic shock and the strength of viral capsids. Biophys J 85: 70-74.
32. Corinaldesi C, Dell'Anno A, Magagnini M & Danovaro R (2010) Viral decay and viral production rates in continental-shelf and deep-sea sediments of the Mediterranean Sea. FEMS Microbiol Ecol 72: 208-218.
33. Cotner JB & Biddanda BA (2002) Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5: 105-121.
34. Cottrell MT & Suttle CA (1995) Dynamics of a lytic virus infecting the photosynthetic marine picoflagellate Micromonas pusilla. Limnol Oceanogr 40: 730-739.
35. Cseke C & Farkas GL (1979) Effect of light on the attachment of cyanophage AS-1 to Anacystis nidulans. J Bacteriol 137: 667-669.
36. Danovaro R, Armeni M, Corinaldesi C & Mei ML (2003) Viruses and marine pollution. Mar Pollut Bull 46: 301-304.
37. Danovaro R, Bongiorni L, Corinaldesi C et al. (2008) Sunscreens cause coral bleaching by promoting viral infections. Environ Health Perspect 116: 441-447.
38. Dashman T & Stotzky G (1984) Adsorption and binding of peptides on homoionic montmorillonite and kaolinite. Soil Biol Biochem 16: 51-55.
39. Daughney CJ, Chatellier X, Chan A, Kenward P, Fortin D, Suttle CA & Fowle DA (2004) Adsorption and precipitation of iron from seawater on a marine bacteriophage (PWH3A-P1). Mar Chem 91: 101-115.
40. Delisle AL & Levin RE (1972a) Characteristics of three phages infectious for psychrophilic fishery isolates of Pseudomonas putrefaciens. Antonie Van Leeuwenhoek 38: 1-8.
41. Delisle AL & Levin RE (1972b) Effect of temperature on an obligately psychrophilic phage-host system of Pseudomonas putrefaciens. Antonie Van Leeuwenhoek 38: 9-15.
42. Dutz J & Koski M (2006) Trophic significance of solitary cells of the prymnesiophyte Phaeocystis globosa depends on cell type. Limnol Oceanogr 51: 1230-1238.
43. Enriquez R, Frosner GG, Hochsteinmintzel V, Riedemann S & Reinhardt G (1992) Accumulation and persistence of hepatitis-A virus in mussels. J Med Virol 37: 174-179.
44. Evans C & Wilson WH (2008) Preferential grazing of Oxyrrhis marina on virus-infected Emiliania huxleyi. Limnol Oceanogr 53: 2035-2040.
45. Evans C, Malin G, Wilson WH & Liss PS (2006) Infectious titers of Emiliania huxleyi virus 86 are reduced by exposure to millimolar dimethyl sulfide and acrylic acid. Limnol Oceanogr 51: 2468-2471.
46. Evans C, Kadner SV, Darroch LJ, Wilson WH, Liss PS & Malin G (2007) The relative significance of viral lysis and microzooplankton grazing as pathways of dimethylsulfoniopropionate (DMSP) cleavage: an Emiliania huxleyi culture study. Limnol Oceanogr 52: 1036-1045.
47. Evilevitch A, Fang LT, Yoffe AM et al. (2008) Effects of salt concentrations and bending energy on the extent of ejection of phage genomes. Biophys J 94: 1110-1120.
48. Farmer JJ III & Janda JM (2005) Vibrionaceae. Bergey's Manual of Systematic Baceriology: The Proteobacteria, Vol. 2 (Brenner DJ, Krieg NR & Staley JR, eds), pp. 491-494. Springer-Verlag, New York, NY.
49. Faust C, Stallknecht D & Swayne D (2009) Filter-feeding bivalves can remove avian influenza viruses from water and reduce infectivity. Proc Biol Sci 276: 3727-3735.
50. Finiguerra MB, Escribano DF & Taylor GT (2011) Light-independent mechanisms of virion inactivation in coastal marine systems. Hydrobiologia 665: 51-66.
51. Frada M, Probert I, Allen MJ, Wilson WH & de Vargas C (2008) The "Cheshire Cat" escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection. P Natl Acad Sci USA 105: 15944-15949.
52. Furuta M, Schrader JO, Schrader HS et al. (1997) Chlorella virus PBCV-1 encodes a homolog of the bacteriophage T4 UV damage repair gene denV. Appl Environ Microbiol 63: 1551-1556.
53. Garza DR & Suttle CA (1998) The effect of cyanophages on the mortality of Synechococcus spp. and selection for UV resistant viral communities. Microb Ecol 36: 281-292.
54. Goldsmith DB, Crosti G, Dwivedi B et al. (2011) Development of phoH as a novel signature gene for assessing marine phage diversity. Appl Environ Microbiol 77: 7730-7739.
55. Gonzalez JM & Suttle CA (1993) Grazing by marine nanoflagellates on viruses and virus-sized particles - ingestion and digestion. Mar Ecol-Prog Ser 94: 1-10.
56. Graneli E & Turner JT (2007) Ecology of Harmful Algae. Springer, Berlin.
57. Hadas E, Marie D, Shpigel M & Ilan M (2006) Virus predation by sponges is a new nutrient-flow pathway in coral reef food webs. Limnol Oceanogr 51: 1548-1550.
58. Hardies SC, Hwang YJ, Hwang CY, Jang GI & Cho BC (2013) Morphology, physiological characteristics, and complete sequence of marine bacteriophage phi RIO-1 infecting Pseudoalteromonas marina. J Virol 87: 9189-9198.
59. Hewson I & Fuhrman JA (2003) Viriobenthos production and virioplankton sorptive scavenging by suspended sediment particles in coastal and pelagic waters. Microbial Ecol 46: 337-347.
60. Hickey DA & Singer GAC (2004) Genomic and proteomic adaptations to growth at high temperature. Genome Biol 5: 117.
61. Hidaka T & Ichida K (1976) Properties of a marine RNA-containing bacteriophage. Mem Fac Fish Kagoshima Univ 25: 77-89.
62. Hofmann GE, Smith JE, Johnson KS, Send U & Levin LA (2011) High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS One 6: e28983.
63. Hotze EM, Badireddy AR, Chellam S & Wiesner MR (2009) Mechanisms of bacteriophage inactivation via singlet oxygen generation in UV illuminated fullerol suspensions. Environ Sci Technol 43: 6639-6645.
64. Jacobsen A, Larsen A, Martinez-Martinez J, Verity PG & Frischer ME (2007) Susceptibility of colonies and colonial cells of Phaeocystis pouchetii (Haptophyta) to viral infection. Aquat Microb Ecol 48: 105-112.
65. Jacquet S & Bratbak G (2003) Effects of ultraviolet radiation on marine virus-phytoplankton interactions. FEMS Microbiol Ecol 44: 279-289.
66. Jacquet S, Heldal M, Iglesias-Rodriguez D, Larsen A, Wilson W & Bratbak G (2002) Flow cytometric analysis of an Emiliana huxleyi bloom terminated by viral infection. Aquat Microb Ecol 27: 111-124.
67. Jia Y, Shan JY, Millard A, Clokie MRJ & Mann NH (2010) Light-dependent adsorption of photosynthetic cyanophages to Synechococcus sp WH7803. FEMS Microbiol Lett 310: 120-126.
68. Jian H, Xiao X & Wang F (2013) Role of filamentous phage SW1 in regulating the lateral flagella of Shewanella piezotolerans Strain WP3 at low temperatures. Appl Environ Microbiol 79: 7101-7109.
69. Jiang SC & Paul JH (1998) Significance of lysogeny in the marine environment: studies with isolates and a model of lysogenic phage production. Microb Ecol 35: 235-243.
70. Johnson RM (1968) Characteristics of a marine vibrio-bacteriophage system. J Ariz Acad Sci 5: 28-33.
71. Juneau P, Lawrence JE, Suttle CA & Harrison PJ (2003) Effects of viral infection on photosynthetic processes in the bloom-forming alga Heterosigma akashiwo. Aquat Microb Ecol 31: 9-17.
72. Kapuscinski RB & Mitchell R (1980) Processes controlling virus inactivation in coastal waters. Water Res 14: 363-371.
73. Kellogg CA & Paul JH (2002) Degree of ultraviolet radiation damage and repair capabilities are related to G+C content in marine vibriophages. Aquat Microb Ecol 27: 13-20.
74. Kelly L, Ding H, Huang KH, Osburne MS & Chisholm SW (2013) Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent. ISME J 7: 1827-1841.
75. Keynan A, Nealson K, Sideropo H & Hastings JW (1974) Marine transducing bacteriophage attacking a luminous bacterium. J Virol 14: 333-340.
76. Kimura M, Jia Z, Nakayama N & Asakawa S (2008) Ecology of viruses in soils: past, present and future perspectives. Soil Sci Plant Nutr 54: 1-32.
77. Kukkaro P & Bamford DH (2009) Virus-host interactions in environments with a wide range of ionic strengths. Environ Microbiol Rep 1: 71-77.
78. Lawrence JE & Suttle CA (2004) Effect of viral infection on sinking rates of Heterosigma akashiwo and its implications for bloom termination. Aquat Microb Ecol 37: 1-7.
79. Levisohn R, Moreland J & Nealson KH (1987) Isolation and characterization of a generalized transducing phage for the marine luminous bacterium Vibrio fischeri MJ-1. J Gen Microbiol 133: 1577-1582.
80. Lindell D, Jaffe JD, Johnson ZI, Church GM & Chisholm SW (2005) Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438: 86-89.
81. Lipson SM & Stotzky G (1984) Effects of proteins on reovirus adsorption to clay minerals. Appl Environ Microbiol 48: 525-530.
82. Liu B, Wu SJ, Song Q, Zhang XB & Xie LH (2006) Two novel bacteriophages of thermophilic bacteria isolated from deep-sea hydrothermal fields. Curr Microbiol 53: 163-166.
83. Lytle CD & Sagripanti JL (2005) Predicted inactivation of viruses of relevance to biodefense by solar radiation. J Virol 79: 14244-14252.
84. 2 pressure and phosphate limitation favor Micromonas pusilla through stimulated growth and reduced viral impact. Appl Environ Microbiol 80: 3119-3127.
85. Middelboe M (2000) Bacterial growth rate and marine virus-host dynamics. Microb Ecol 40: 114-124.
86. Mitchell R & Jannasch HW (1969) Processes controlling virus inactivation in seawater. Environ Sci Technol 3: 941-943.
87. Moebus K (1996) Marine bacteriophage reproduction under nutrient-limited growth of host bacteria. I. Investigations with six phage-host systems. Mar Ecol Prog Ser 144: 1-12.
88. Monier A, Welsh RM, Gentemann C, Weinstock G, Eisen JA & Worden AZ (2011) Phosphate transporters in marine phytoplankton and their viruses: cross-domain commonalities in viral-host gene exchanges. Environ Microbiol 14: 162-176.
89. Motegi C & Nagata T (2007) Enhancement of viral production by addition of nitrogen or nitrogen plus carbon in subtropical surface waters of the South Pacific. Aquat Microb Ecol 48: 27-34.
90. Murray AG & Jackson GA (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.
91. Nagasaki K & Yamaguchi M (1998) Effect of temperature on the algicidal activity and the stability of HaV (Heterosigma akashiwo virus). Aquat Microb Ecol 15: 211-216.
92. Nagasaki K, Shirai Y, Tomaru Y, Nishida K & Pietrokovski S (2005) Algal viruses with distinct intraspecies host specificities include identical intein elements. Appl Environ Microbiol 71: 3599-3607.
93. Noble RT & Fuhrman JA (1997) Virus decay and its causes in coastal waters. Appl Environ Microbiol 63: 77-83.
94. Orgata H, Ray J, Toyoda K, Sandaa R-A, Nagasaki K, Bratbak G & Claverie J-M (2011) Two new subfamilies of DNA mismatch repair proteins (MutS) specifically abundant in the marine environment. ISME J 5: 1143-1151.
95. Parada V, Herndl GJ & Weinbauer MG (2006) Viral burst size of heterotrophic prokaryotes in aquatic systems. J Mar Biol Assoc UK 86: 613-621.
96. Passow U (2002) Transparent exopolymer particles (TEP) in aquatic environments. Prog Oceanogr 55: 287-333.
97. Paul JH, Cochran PK & Jiang SC (1999) Lysogeny and transduction in the marine environment. Microbial Biosystems: New Frontiers (Bell CR, Brylinsky M & Johnson-Green P, eds), pp. 557-565. Atlantic Canada Society for Microbial Ecology, Halifax, Canada.
98. Payet JP & Suttle CA (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.
99. Paytan A & McLaughlin K (2007) The oceanic phosphorus cycle. Chem Rev 107: 563-576.
100. Pernthaler J (2005) Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol 3: 537-546.
101. Porter K, Kukkaro P, Bamford JKH, Bath C, Kivela HM, Dyall-Smith ML & Bamford DH (2005) SHI: a novel, spherical halovirus isolated from an Australian hypersaline lake. Virology 335: 22-33.
102. Proctor LM & Fuhrman JA (1991) Roles of viral infection in organic particle flux. Mar Ecol Prog Ser 69: 133-142.
103. Proctor LM, Okubo A & Fuhrman JA (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.
104. Rao VC, Metcalf TG & Melnick JL (1986) Human viruses in sediments, sludges, and soils. Bull World Health Organ 64: 1-13.
105. Rousseau V, Chretiennot-Dinet MJ, Jacobsen A, Verity P & Whipple S (2007) The life cycle of Phaeocystis: state of knowledge and presumptive role in ecology. Biogeochemistry 83: 29-47.
106. Ruardij P, Veldhuis MJW & Brussaard CPD (2005) Modeling the bloom dynamics of the polymorphic phytoplankter Phaeocystis globosa: impact of grazers and viruses. Harmful Algae 4: 941-963.
107. Santini S, Jeudy S, Bartoli J et al. (2013) Genome of Phaeocystis globosa virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes. P Natl Acad Sci USA 110: 10800-10805.
108. Santos F, Yarza P, Parro V, Meseguer I, Rossello-Mora R & Anton J (2012) Culture-independent approaches for studying viruses from hypersaline environments. Appl Environ Microbiol 78: 1635-1643.
109. Selinger RLB, Wang Z, Gelbart WM & Ben-Shaul A (1991) Statistical-thermodynamic approach to fracture. Phys Rev A 43: 4396-4400.
110. Shaffer JJ, Jacobsen LM, Schrader JO, Lee KW, Martin EL & Kokjohn TA (1999) Characterization of Pseudomonas aeruginosa bacteriophage UNL-1, a bacterial virus with a novel UV-A-inducible DNA damage reactivation phenotype. Appl Environ Microbiol 65: 2606-2613.
111. Sheik AR, Brussaard CPD, Lavik G, Foster RA, Musat N, Adam B & Kuypers MMM (2012) Viral infection of Phaeocystis globosa impedes release of chitinous star-like structures: quantification using single cell approaches. Environ Microbiol 15: 1441-1451.
112. Sheik AR, Brussaard CPD, Lavik G, et al. (2014) Responses of the coastal bacterial community to viral infection of the algae Phaeocystis globosa. ISME J 8: 212-225.
113. Shirai Y, Tomaru Y, Takao Y, Suzuki H, Nagumo T & 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.
114. Simon M, Grossart HP, Schweitzer B & Ploug H (2002) Microbial Ecol of organic aggregates in aquatic ecosystems. Aquat Microb Ecol 28: 175-211.
115. Sorensen G (2009) The role of the virus-phytoplankton system in marine biogeochemical cycling: possible impacts of climate change. Plymouth Stud Sci 2: 289-302.
116. Steinke M, Wolfe GV & Kirst GO (1998) Partial characterisation of dimethylsulfoniopropionate (DMSP) lyase isozymes in 6 strains of Emiliania huxleyi. Mar Ecol Prog Ser 175: 215-225.
117. Sullivan MB, Coleman ML, Weigele P, Rohwer F & Chisholm SW (2005) Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3: 790-806.
118. 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: 1344-1357.
119. Sullivan MB, Huang KH, Ignacio-Espinoza JC et al. (2010) Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ Microbiol 12: 3035-3056.
120. Suttle CA (2000) Viral infection of cyanobacteria and eukaryotic algae. Viral Ecology (Hurst CJ, ed), pp. 247-296. Academic Press, San Diego, CA.
121. Suttle CA (2007) Marine viruses - major players in the global ecosystem. Nat Rev 5: 801-812.
122. Suttle CA & Chan AM (1993) Marine cyanophages infecting oceanic and coastal strains of Synechococcus - abundance, morphology, cross-infectivity and growth-characteristics. Mar Ecol Prog Ser 92: 99-109.
123. Suttle CA & Chan AM (1994) Dynamics and distribution of cyanophages and their effect on marine Synechococcus spp. Appl Environ Microbiol 60: 3167-3174.
124. Suttle CA & Chen F (1992) Mechanisms and rates of decay of marine viruses in seawater. Appl Environ Microbiol 58: 3721-3729.
125. Tang X, Chao J, Chen D, Shao K & Gao G (2012) Organic-aggregate-attached bacteria in aquatic ecosystems: abundance, diversity, community dynamics and function. Oceanography (Marcelli PM, ed), InTech, ISBN: 978-953-51-0301-1, Available from: http://www.intechopen.com/books/oceanography/organic-aggregate-attached-bacteria-in-aquatic-ecosystems-abundance-diversity-community-dynamics-and (accessed 17 November 2013)
126. Templeton MR, Andrews RC & Hofmann R (2005) Inactivation of particle-associated viral surrogates by ultraviolet light. Water Res 39: 3487-3500.
127. Thyrhaug R, Larsen A, Brussaard CPD & Bratbak G (2002) Cell cycle dependent virus production in marine phytoplankton. J Phycol 38: 338-343.
128. Thyrhaug R, Larsen A, Thingstad TF & Bratbak G (2003) Stable coexistence in marine algal host-virus systems. Mar Ecol-Prog Ser 254: 27-35.
129. Tomaru Y, Katanozaka N, Nishida K, Shirai Y, Tarutani K, Yamaguchi M & Nagasaki K (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.
130. Tomaru Y, Tanabe H, Yamanaka S & Nagasaki K (2005) Effects of temperature and light on stability of microalgal viruses, HaV, HcV, and HcRNAV. Plankton Biol Ecol 52: 1-6.
131. Tomaru Y, Shirai Y, Suzuki H, Nagumo T & Nagasaki K (2008) Isolation and characterization of a new single-stranded DNA virus infecting the cosmopolitan marine diatom Chaetoceros debilis. Aquat Microb Ecol 50: 103-112.
132. Tomaru Y, Mizumoto H, Takao Y & Nagasaki K (2009a) Co-occurrence of DNA- and RNA-viruses infecting the bloom-forming dinoflagellate Heterocapsa circularisquama, on the Japan coast. Plankton Benthos Res 4: 129-134.
133. Tomaru Y, Takao Y, Suzuki H, Nagumo T & Nagasaki K (2009b) Isolation and characterization of a single-stranded RNA virus infecting the bloom-forming diatom Chaetoceros socialis. Appl Environ Microbiol 75: 2375-2381.
134. Tomaru Y, Fujii N, Oda S, Toyoda K & Nagasaki K (2011a) Dynamics of diatom viruses on the western coast of Japan. Aquat Microb Ecol 63: 223-230.
135. Tomaru Y, Takao Y, Suzuki H, Nagumo T, Koike K & Nagasaki K (2011b) Isolation and characterization of a single-stranded DNA virus infecting Chaetoceros lorenzianus Grunow. Appl Environ Microbiol 77: 5285-5293.
136. Tomaru Y, Toyoda K, Suzuki H, Nagumo T, Kimura K & Takao Y (2013) New single-stranded DNA virus with a unique genomic structure that infects marine diatom Chaetoceros setoensis. Sci Rep 3: doi:10.1038/srep03337
137. Torsvik T & Dundas ID (1980) Persisting phage infection in Halobacterium salinarium str. 1. J Gen Virol 47: 29-36.
138. Traving SJ, Clokie MRJ & Middelboe M (2013) Increased acidification has profound effect on the interactions between the cyanobacterium Synechococcus sp. WH7803 and its viruses. FEMS Microbiol Ecol 87: 133-141.
139. Valentine DL (2007) Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat Rev Microbiol 5: 316-323.
140. Van Etten JL, Burbank DE, Xia Y & Meints RH (1983) Growth cycle of a virus, PBCV-1, that infects Chlorella-like algae. Virology 126: 117-125.
141. Vardi A, Van Mooy BAS, Fredricks HF, Popendorf KJ, Ossolinski JE, Haramaty L & Bidle KD (2009) Viral glycosphingolipids induce lytic infection and cell death in marine phytoplankton. Science 326: 861-865.
142. Vettori C, Gallori E & Stotzky G (2000) Clay minerals protect bacteriophage PBS1 of Bacillus subtilis against inactivation and loss of transducing ability by UV radiation. Can J Microbiol 46: 770-773.
143. Wait DA & Sobsey MD (1983) Method for recovery of enteric viruses from estuarine sediments with chaotropic agents. Appl Environ Microbiol 46: 379-385.
144. Wang FP, Wang P, Chen MX & Xiao X (2004) Isolation of extremophiles with the detection and retrieval of Shewanella strains in deep-sea sediments from the west Pacific. Extremophiles 8: 165-168.
145. Wang F, Wang FP, Li Q & Xiao X (2007) A novel filamentous phage from the deep-sea bacterium Shewanella piezotolerans WP3 is induced at low temperature. J Bacteriol 189: 7151-7153.
146. Waters RE & Chan AT (1982) Micromonas pusilla virus: the virus growth cycle and associated physiological events within the host cells; host range mutation. J Gen Virol 63: 199-206.
147. Waters P & Lloyd D (1985) Salt, pH and temperature dependencies of growth and bioluminescence of three species of luminous bacteria analysed on gradient plates. J Gen Microbiol 131: 2865-2869.
148. Wei HC, Ca QY, Rahn R, Zhang XS, Wang Y & Lebwohl M (1998) DNA structural integrity and base composition affect ultraviolet light-induced oxidative DNA damage. Biochemistry 37: 6485-6490.
149. Weinbauer MG & Suttle CA (1996) Potential significance of lysogeny to bacteriophage production and bacterial mortality in coastal waters of the Gulf of Mexico. Appl Environ Microbiol 62: 4374-4380.
150. Weinbauer MG & Suttle CA (1999) Lysogeny and prophage induction in coastal and offshore bacterial communities. Aquat Microb Ecol 18: 217-225.
151. Weinbauer MG, Wilhelm SW, Suttle CA & Garza DR (1997) Photoreactivation compensates for UV damage and restores infectivity to natural marine virus communities. Appl Environ Microbiol 63: 2200-2205.
152. Weinbauer MG, Wilhelm SW, Suttle CA, Pledger RJ & Mitchell DL (1999) Sunlight-induced DNA damage and resistance in natural viral communities. Aquat Microb Ecol 17: 111-120.
153. Weinbauer MG, Brettar I & Hofle MG (2003) Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnol Oceanogr 48: 1457-1465.
154. Weinbauer MG, Bettarel Y, Cattaneo R et al. (2009) Viral ecology of organic and inorganic particles in aquatic systems: avenues for further research. Aquat Microb Ecol 57: 321-341.
155. Wells LE & Deming JW (2006a) Effects of temperature, salinity and clay particles on inactivation and decay of cold-active marine Bacteriophage 9A. Aquat Microb Ecol 45: 31-39.
156. Wells LE & Deming JW (2006b) Characterization of a cold-active bacteriophage on two psychrophilic marine hosts. Aquat Microb Ecol 45: 15-29.
157. White PA, Kalff J, Rasmussen JB & Gasol JM (1991) The effect of temperature and algal biomass on bacterial production and specific growth-rate in fresh-water and marine habitats. Microb Ecol 21: 99-118.
158. Whitehead RF, de Mora SJ & Demers S (2000) Enhanced UV radiation - a new problem for the marine environment. The Effects of UV Radiation in the Marine Environment (de Mora S, Demers S & Vernet M, eds), pp. 1-34. Cambridge University Press, Cambridge, UK.
159. Wiebe WJ & Liston J (1968) Isolation and characterization of a marine bacteriophage. Mar Biol 1: 244-249.
160. Wiebe WJ, Sheldon WM & Pomeroy LR (1992) Bacterial-growth in the cold - evidence for an enhanced substrate requirement. Appl Environ Microbiol 58: 359-364.
161. Wigginton KR, Menin L, Montoya JP & Kohn T (2010) Oxidation of virus proteins during UV254 and singlet oxygen mediated inactivation. Environ Sci Technol 44: 5437-5443.
162. Wigginton KR, Pecson BM, Sigstam T & Bosshard F (2012) Virus inactivation mechanisms: impact of disinfection on virus function and structural integrity. Environ Sci Technol 46: 12069-12078.
163. Wikner J, Vallino JJ, Steward GF, Smith DC & Azam F (1993) Nucleic-acids from the host bacterium as a major source of nucleotides for 3 marine bacteriophages. FEMS Microbiol Ecol 12: 237-248.
164. Wilcox RM & Fuhrman JA (1994) Bacterial viruses in coastal seawater: lytic rather than lysogenic production. Mar Ecol Prog Ser 114: 35-45.
165. Wilhelm SW, Weinbauer MG, Suttle CA & Jeffrey WH (1998a) The role of sunlight in the removal and repair of viruses in the sea. Limnol Oceanogr 43: 586-592.
166. Wilhelm SW, Weinbauer MG, Suttle CA, Pledger RJ & Mitchell DL (1998b) Measurements of DNA damage and photoreactivation imply that most viruses in marine surface waters are infective. Aquat Microb Ecol 14: 215-222.
167. Wilhelm SW, Jeffrey WH, Dean AL, Meador J, Pakulski JD & Mitchell DL (2003) UV radiation induced DNA damage in marine viruses along a latitudinal gradient in the southeastern Pacific Ocean. Aquat Microb Ecol 31: 1-8.
168. Williamson SJ & Paul JH (2006) Environmental factors that influence the transition from lysogenic to lytic existence in the phi HSIC/Listonella pelagia marine phage-host system. Microb Ecol 52: 217-225.
169. Williamson SJ, Houchin LA, McDaniel L & Paul JH (2002) Seasonal variation in lysogeny as depicted by prophage induction in Tampa Bay, Florida. Appl Environ Microbiol 68: 4307-4314.
170. Williamson SJ, Cary SC, Williamson KE, Helton RR, Bench SR, Winget D & Wommack KE (2008) Lysogenic virus-host interactions predominate at deep-sea diffuse-flow hydrothermal vents. ISME J 2: 1112-1121.
171. Wilson WH, Carr NG & Mann NH (1996) The effect of phosphate status on the kinetics of cyanophage infection in the oceanic cyanobacterium Synechococcus sp WH7803. J Phycol 32: 506-516.
172. Wilson WH, Turner S & Mann NH (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.
173. Winter C, Herndl GJ & Weinbauer MG (2004) Diel cycles in viral infection of bacterioplankton in the North Sea. Aquat Microb Ecol 35: 207-216.
174. Wommack KE & Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64: 69-114.
175. Wommack KE, Hill RT, Muller TA & Colwell RR (1996) Effects of sunlight on bacteriophage viability and structure. Appl Environ Microbiol 62: 1336-1341.
176. Yamaguchi M, Itakura S, Nagasaki K, Matsuyama Y, Uchida T & Imai I (1997) Effects of temperature and salinity on the growth of the red tide flagellates Heterocapsa circularisquama (Dinophyceae) and Chattonella verruculosa (Raphidophyceae). J Plankton Res 19: 1167-1174.
177. Zachary A (1976) Physiology and ecology of bacteriophages of the marine bacterium Beneckea natriegens: salinity. Appl Environ Microbiol 31: 415-422.
178. Zeng QL & Chisholm SW (2012) Marine viruses exploit their host's two-component regulatory system in response to resource limitation. Curr Biol 22: 124-128.
179. Zingone A, Chretinnot-Dinet M-J, Lange M & Medlin L (1999) Morphological and genetic characterization of Phaeocystis cordata and P. Jahnii (Prymesiophyceae), two new species from the Mediterranean Sea. J Phycol 35: 1322-1337.