Home LiteratureArticle Details
PMID: 10704475 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Virioplankton: viruses in aquatic ecosystems.

Microbiology and molecular biology reviews : MMBR ·Vol. 64 ·No. 1 ·2000-03-00 ·Pages 69-114

Wommack KE, Colwell RR

Abstract

The discovery that viruses may be the most abundant organisms in natural waters, surpassing the number of bacteria by an order of magnitude, has inspired a resurgence of interest in viruses in the aquatic environment. Surprisingly little was known of the interaction of viruses and their hosts in nature. In the decade since the reports of extraordinarily large virus populations were published, enumeration of viruses in aquatic environments has demonstrated that the virioplankton are dynamic components of the plankton, changing dramatically in number with geographical location and season. The evidence to date suggests that virioplankton communities are composed principally of bacteriophages and, to a lesser extent, eukaryotic algal viruses. The influence of viral infection and lysis on bacterial and phytoplankton host communities was measurable after new methods were developed and prior knowledge of bacteriophage biology was incorporated into concepts of parasite and host community interactions. The new methods have yielded data showing that viral infection can have a significant impact on bacteria and unicellular algae populations and supporting the hypothesis that viruses play a significant role in microbial food webs. Besides predation limiting bacteria and phytoplankton populations, the specific nature of virus-host interaction raises the intriguing possibility that viral infection influences the structure and diversity of aquatic microbial communities. Novel applications of molecular genetic techniques have provided good evidence that viral infection can significantly influence the composition and diversity of aquatic microbial communities.

MeSH Terms
Animals Bacteria/virology Bacteriophages/physiology Chlorophyll/metabolism Chlorophyll A Ecosystem Gene Transfer Techniques Models, Biological Plankton/virology Virus Physiological Phenomena Virus Replication Water Microbiology
Chemicals
Chlorophyll Chlorophyll A
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Wommack K E
Center of Marine Biotechnology, Baltimore, Maryland 21202, USA.
Colwell R R
References (197)
197 references, click to expand
  1. Coevolution of bacteria and phage: are there endless cycles of bacterial defenses and phage counterdefenses?
    J Theor Biol. 1984 Jun 7;108(3):319-25 PMID: 6748694
  2. Concentration of viruses from large volumes of tap water using pleated membrane filters.
    Appl Environ Microbiol. 1976 Feb;31(2):221-6 PMID: 187115
  3. Application of DNA probes to analysis of bacteriophage distribution patterns in the environment.
    Appl Environ Microbiol. 1992 Jun;58(6):2046-52 PMID: 1622283
  4. Diversity dynamics of marine bacteria studied by immunofluorescent staining on membrane filters.
    Appl Environ Microbiol. 1982 Jan;43(1):169-76 PMID: 16345920
  5. A role for bacteriophages in the evolution and transfer of bacterial virulence determinants.
    Mol Microbiol. 1995 Oct;18(2):201-8 PMID: 8709840
  6. Archaea in coastal marine environments.
    Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5685-9 PMID: 1608980
  7. High abundance of viruses found in aquatic environments.
    Nature. 1989 Aug 10;340(6233):467-8 PMID: 2755508
  8. Role of sediment in the persistence of enteroviruses in the estuarine environment.
    Appl Environ Microbiol. 1978 Apr;35(4):685-9 PMID: 206204
  9. Persistence of enteroviruses in lake water.
    Appl Microbiol. 1974 Nov;28(5):895-6 PMID: 4374125
  10. Environmental virology: from detection of virus in sewage and water by isolation to identification by molecular biology--a trip of over 50 years.
    Annu Rev Microbiol. 1995;49:461-87 PMID: 8561468
  11. Photoreactivity of UV-b damage in bacteriophage phi X174 DNA.
    Photochem Photobiol. 1981 May;33(5):769-71 PMID: 6455675
  12. Ecology of bacteriophages infecting activated sludge bacteria.
    Appl Environ Microbiol. 1991 Aug;57(8):2147-51 PMID: 1768086
  13. Report on a pseudolysogenic mycobacterium and a review of the literature concerning pseudolysogeny.
    Acta Pathol Microbiol Scand B Microbiol Immunol. 1971;79(3):428-34 PMID: 5283061
  14. Induction and partial purification of bacteriophages from Desulfovibrio vulgaris (Hildenborough) and Desulfovibrio desulfuricans ATCC 13541.
    J Gen Microbiol. 1991 Jul;137(7):1545-9 PMID: 1683398
  15. Prophage F116: evidence for extrachromosomal location in Pseudomonas aeruginosa strain PAO.
    J Virol. 1977 Jun;22(3):844-7 PMID: 406425
  16. Inactivation of polioviruses and coxsackieviruses in surface water.
    Appl Environ Microbiol. 1977 Feb;33(2):334-40 PMID: 192146
  17. Persisting bacteriophage infections, lysogeny, and phage conversions.
    Annu Rev Microbiol. 1974;28(0):265-99 PMID: 4215366
  18. Isolation and characterization of AS-1, a phycovirus infecting the blue-green algae, Anacystis nidulans and Synechococcus cedrorum.
    Virology. 1972 Jan;47(1):105-13 PMID: 4110125
  19. Calibrating estimates of phage-induced mortality in marine bacteria: Ultrastructural studies of marine bacteriophage development from one-step growth experiments.
    Microb Ecol. 1993 Mar;25(2):161-82 PMID: 24189813
  20. Gene transfer by transduction in the marine environment.
    Appl Environ Microbiol. 1998 Aug;64(8):2780-7 PMID: 9687430
  21. 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. 1998 Jun;64(6):2051-60 PMID: 9603813
  22. Virus persistence in groundwater.
    Appl Environ Microbiol. 1985 Apr;49(4):778-81 PMID: 4004211
  23. Natural variability and diurnal fluctuations within the bacteriophage population of the rumen.
    Appl Environ Microbiol. 1996 Mar;62(3):994-7 PMID: 8975626
  24. Evolutionary relationships among large double-stranded DNA viruses that infect microalgae and other organisms as inferred from DNA polymerase genes.
    Virology. 1996 May 1;219(1):170-8 PMID: 8623526
  25. Studies on the nature of the virus inactivating capacity of sea water.
    Arch Gesamte Virusforsch. 1965;17(3):409-13 PMID: 4286821
  26. Bacteriophages active against Bacteroides fragilis in sewage-polluted waters.
    Appl Environ Microbiol. 1987 Jul;53(7):1632-7 PMID: 3662510
  27. Viruses and viruslike particles of eukaryotic algae.
    Microbiol Rev. 1991 Dec;55(4):586-620 PMID: 1779928
  28. Genetic diversity in marine algal virus communities as revealed by sequence analysis of DNA polymerase genes.
    Appl Environ Microbiol. 1996 Aug;62(8):2869-74 PMID: 8702280
  29. Algal virus: isolation.
    Science. 1963 May 10;140(3567):679-80 PMID: 13976026
  30. Production of extracellular nucleic acids by genetically altered bacteria in aquatic-environment microcosms.
    Appl Environ Microbiol. 1989 Aug;55(8):1865-9 PMID: 2506807
  31. Frequency of generalized transducing phages in natural isolates of the Salmonella typhimurium complex.
    Appl Environ Microbiol. 1995 Apr;61(4):1637-40 PMID: 7747978
  32. An evaluation of factors affecting the survival of Escherichia coli in sea water. IV. Bacteriophages.
    Appl Microbiol. 1960 Jul;8:254-6 PMID: 13807797
  33. Significance of Lysogeny in the Marine Environment: Studies with Isolates and a Model of Lysogenic Phage Production
    Microb Ecol. 1998 May;35(3):235-43 PMID: 9569281
  34. THE QUESTION OF THE EXISTENCE OF SPECIFIC MARINE BACTERIA.
    Bacteriol Rev. 1965 Mar;29:9-24 PMID: 14295987
  35. Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems.
    Appl Environ Microbiol. 1985 Mar;49(3):599-607 PMID: 3994368
  36. Hybridization analysis of chesapeake bay virioplankton
    Appl Environ Microbiol. 1999 Jan;65(1):241-50 PMID: 9872785
  37. Population dynamics of chesapeake bay virioplankton: total-community analysis by pulsed-field gel electrophoresis
    Appl Environ Microbiol. 1999 Jan;65(1):231-40 PMID: 9872784
  38. Significance of viral lysis and flagellate grazing as factors controlling bacterioplankton production in a eutrophic lake.
    Appl Environ Microbiol. 1998 Feb;64(2):431-8 PMID: 16349497
  39. Ecological relationship between Vibrio parahaemolyticus and agar-digesting vibrios as evidenced by bacteriophage susceptibility patterns.
    Appl Environ Microbiol. 1978 Sep;36(3):500-5 PMID: 727782
  40. Enumeration of marine viruses in culture and natural samples by flow cytometry
    Appl Environ Microbiol. 1999 Jan;65(1):45-52 PMID: 9872758
  41. INDIGENOUS MARINE BACTERIOPHAGES.
    J Bacteriol. 1960 Apr;79(4):614 PMID: 16561855
  42. Rapid concentration of bacteriophages from aquatic habitats.
    J Appl Bacteriol. 1977 Jun;42(3):417-21 PMID: 407206
  43. Genetic Diversity of Algal Viruses Which Lyse the Photosynthetic Picoflagellate Micromonas pusilla (Prasinophyceae).
    Appl Environ Microbiol. 1995 Aug;61(8):3088-91 PMID: 16535105
  44. Concentration of bacteriophages from natural waters.
    J Appl Bacteriol. 1979 Feb;46(1):103-16 PMID: 374327
  45. Effects of Suspended Particulates on the Frequency of Transduction among Pseudomonas aeruginosa in a Freshwater Environment.
    Appl Environ Microbiol. 1995 Apr;61(4):1214-9 PMID: 16534986
  46. Transduction of a freshwater microbial community by a new Pseudomonas aeruginosa generalized transducing phage, UT1.
    Mol Ecol. 1994 Apr;3(2):121-6 PMID: 8019688
  47. Phenotypic alterations associated with the bacteriophage carrier state of Shigella dysenteriae.
    J Gen Microbiol. 1961 Mar;24:355-67 PMID: 13761818
  48. Host-virus interactions in Escherichia coli: effect of stationary phase on viral release from MS2-infected bacteria.
    J Virol. 1972 Jul;10(1):162-5 PMID: 4557207
  49. Viruses in Antarctic lakes.
    Limnol Oceanogr. 1998 Nov;43(7):1754-61 PMID: 11543124
  50. Increased reproductive fitness of Escherichia coli lambda lysogens.
    J Virol. 1977 Feb;21(2):554-9 PMID: 319255
  51. The effect of host-cell starvation on virus-induced lysis by MS2 bacteriophage.
    J Gen Virol. 1976 Jun;31(3):323-30 PMID: 778338
  52. Phage typing and phage induction in carrier and invasive Staphylococcus epidermidis isolates.
    J Hosp Infect. 1991 Aug;18(4):293-9 PMID: 1682367
  53. Occurrence of virus-like particles in the Dead Sea.
    Extremophiles. 1997 Aug;1(3):143-9 PMID: 9680320
  54. Mechanisms and rates of decay of marine viruses in seawater.
    Appl Environ Microbiol. 1992 Nov;58(11):3721-9 PMID: 16348812
  55. Bacteriophage infection and multiplication occur in Pseudomonas aeruginosa starved for 5 years.
    Can J Microbiol. 1997 Dec;43(12):1157-63 PMID: 9476352
  56. Rifampicin-resistant mutant supporting bacteriophage growth on stationary phase Achromobacter cells.
    J Gen Virol. 1977 Apr;35(1):117-23 PMID: 859010
  57. The state of the microbes: A summary of a symposium honoring Lawrence Pomeroy.
    Microb Ecol. 1994 Sep;28(2):113-6 PMID: 24186436
  58. Restriction endonucleases in the analysis and restructuring of dna molecules.
    Annu Rev Biochem. 1975;44:273-93 PMID: 166604
  59. THE GROWTH OF BACTERIOPHAGE.
    J Gen Physiol. 1939 Jan 20;22(3):365-84 PMID: 19873108
  60. An unstable intermediate carrying information from genes to ribosomes for protein synthesis.
    Nature. 1961 May 13;190:576-581 PMID: 20446365
  61. Coliphage and indigenous phage in Mamala Bay, Oahu, Hawaii.
    Appl Environ Microbiol. 1997 Jan;63(1):133-8 PMID: 9065272
  62. Isolation of Virus Capable of Lysing the Brown Tide Microalga, Aureococcus anophagefferens.
    Science. 1994 Nov 4;266(5186):805-7 PMID: 17730401
  63. The isolation of bacteriophages from the environment.
    J Appl Bacteriol. 1982 Aug;53(1):1-17 PMID: 6757237
  64. Virucidal action of sea water.
    Am J Epidemiol. 1967 Jan;85(1):1-8 PMID: 4289331
  65. Resistance to co-occurring phages enables marine synechococcus communities to coexist with cyanophages abundant in seawater.
    Appl Environ Microbiol. 1993 Oct;59(10):3393-9 PMID: 16349072
  66. Microbial ecology. Archaea, Archaea, everywhere.
    Nature. 1994 Oct 20;371(6499):657-8 PMID: 7935810
  67. Particle counter determination of bacterial biomass in seawater.
    Appl Environ Microbiol. 1987 Feb;53(2):274-7 PMID: 16347275
  68. The significance of viruses to mortality in aquatic microbial communities.
    Microb Ecol. 1994 Sep;28(2):237-43 PMID: 24186450
  69. Archaebacterial viruses.
    Adv Virus Res. 1988;34:143-88 PMID: 3137792
  70. A 26-kDa outer membrane protein, OmpK, common to Vibrio species is the receptor for a broad-host-range vibriophage, KVP40.
    FEMS Microbiol Lett. 1995 Jan 1;125(1):101-5 PMID: 7867914
  71. Marine ammonia- and nitrite-oxidizing bacteria: serological diversity determined by immunofluorescence in culture and in the environment.
    Appl Environ Microbiol. 1985 Aug;50(2):194-201 PMID: 16346845
  72. Effects of sunlight on bacteriophage viability and structure.
    Appl Environ Microbiol. 1996 Apr;62(4):1336-41 PMID: 8919794
  73. Dynamic interactions ofPseudomonas aeruginosa and bacteriophages in lake water.
    Microb Ecol. 1990 Mar;19(2):171-85 PMID: 24196310
  74. Significance of bacteriophages for controlling bacterioplankton growth in a mesotrophic lake.
    Appl Environ Microbiol. 1995 Jan;61(1):333-40 PMID: 16534914
  75. Survival strategies of bacteria in the natural environment.
    Microbiol Rev. 1987 Sep;51(3):365-79 PMID: 3312987
  76. A shared strategy for virulence.
    Science. 1996 May 31;272(5266):1261-3 PMID: 8650535
  77. Use of nuclepore filters for counting bacteria by fluorescence microscopy.
    Appl Environ Microbiol. 1977 May;33(5):1225-8 PMID: 327932
  78. Seasonal variations of virus abundance and viral control of the bacterial production in a backwater system of the danube river.
    Appl Environ Microbiol. 1995 Oct;61(10):3734-40 PMID: 16535153
  79. Enumeration and biomass estimation of planktonic bacteria and viruses by transmission electron microscopy.
    Appl Environ Microbiol. 1990 Feb;56(2):352-6 PMID: 2306088
  80. Characterization of Pseudomonas aeruginosa bacteriophage UNL-1, a bacterial virus with a novel UV-A-inducible DNA damage reactivation phenotype.
    Appl Environ Microbiol. 1999 Jun;65(6):2606-13 PMID: 10347050
  81. Cloning and sequence analysis of Vibrio parahaemolyticus ompK gene encoding a 26-kDa outer membrane protein, OmpK, that serves as receptor for a broad-host-range vibriophage, KVP40.
    FEMS Microbiol Lett. 1995 Dec 15;134(2-3):245-9 PMID: 8586275
  82. Lambda lysogens of E. coli reproduce more rapidly than non-lysogens.
    Nature. 1975 Jun 26;255(5511):735-7 PMID: 1094307
  83. Characterization of marine temperate phage-host systems isolated from Mamala Bay, Oahu, Hawaii.
    Appl Environ Microbiol. 1998 Feb;64(2):535-42 PMID: 9464390
  84. Presence of lysogenic phage in the outbreak strains of Vibrio cholerae O139.
    J Med Microbiol. 1995 Jun;42(6):399-403 PMID: 7791203
  85. Estimation of ruminal bacteriophage numbers by pulsed-field gel electrophoresis and laser densitometry.
    Appl Environ Microbiol. 1993 Jul;59(7):2299-303 PMID: 8357262
  86. Nested PCR with three highly degenerate primers for amplification and identification of DNA from related organisms.
    Biotechniques. 1995 Apr;18(4):609-12 PMID: 7598890
  87. Physiology and ecology of bacteriophages of the marine bacterium Beneckea natriegens: salinity.
    Appl Environ Microbiol. 1976 Mar;31(3):415-22 PMID: 938035
  88. Fluorescently Labeled Virus Probes Show that Natural Virus Populations Can Control the Structure of Marine Microbial Communities.
    Appl Environ Microbiol. 1995 Oct;61(10):3623-7 PMID: 16535146
  89. Seasonal and Diel Variability in Dissolved DNA and in Microbial Biomass and Activity in a Subtropical Estuary.
    Appl Environ Microbiol. 1988 Mar;54(3):718-727 PMID: 16347583
  90. Bacteriophage diversity in the North Sea.
    Appl Environ Microbiol. 1998 Nov;64(11):4128-33 PMID: 9797256
  91. Bacterial genome sequence bagged.
    Science. 1995 Jul 28;269(5223):468-70 PMID: 7624767
  92. Isolation and preliminary characterization of bacteriophages for Bacillus subtilis.
    J Bacteriol. 1961 Jul;82:135-41 PMID: 13743075
  93. Mechanism of DNA chain growth. I. Possible discontinuity and unusual secondary structure of newly synthesized chains.
    Proc Natl Acad Sci U S A. 1968 Feb;59(2):598-605 PMID: 4967086
  94. F-specific RNA bacteriophages are adequate model organisms for enteric viruses in fresh water.
    Appl Environ Microbiol. 1993 Sep;59(9):2956-62 PMID: 8215367
  95. Phycovirus SM-1: a virus infecting unicellular blue-green algae.
    Virology. 1969 Mar;37(3):386-95 PMID: 5777559
  96. Use of modified diatomaceous earth for removal and recovery of viruses in water.
    Appl Environ Microbiol. 1991 Sep;57(9):2502-6 PMID: 1768124
  97. The stationary phase of the bacterial life cycle.
    Annu Rev Microbiol. 1993;47:855-74 PMID: 8257118
  98. 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. 1987 May;53(5):987-95 PMID: 3111371
  99. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd.
    Science. 1995 Jul 28;269(5223):496-512 PMID: 7542800
  100. Characteristics of PR5, a lipid-containing plasmid-dependent phage.
    Can J Microbiol. 1978 Jul;24(7):875-82 PMID: 98225
  101. Prevalence of broad-host-range lytic bacteriophages of Sphaerotilus natans, Escherichia coli, and Pseudomonas aeruginosa.
    Appl Environ Microbiol. 1998 Feb;64(2):575-80 PMID: 9464396
  102. Deoxyribonucleic acid repair in bacteriophage.
    Microbiol Rev. 1981 Mar;45(1):72-98 PMID: 6261109
  103. Microbial diversity: the importance of exploration and conservation.
    J Ind Microbiol Biotechnol. 1997 May;18(5):302-7 PMID: 9218360
  104. DNA restriction and modification mechanisms in bacteria.
    Annu Rev Microbiol. 1971;25:153-76 PMID: 4949033
  105. Changes in bacterial and eukaryotic community structure after mass lysis of filamentous cyanobacteria associated with viruses.
    Appl Environ Microbiol. 1999 Feb;65(2):795-801 PMID: 9925618
  106. Concentration of viruses and dissolved DNA from aquatic environments by vortex flow filtration.
    Appl Environ Microbiol. 1991 Aug;57(8):2197-204 PMID: 1768090
  107. [Induction of the production of bacteriophages in lysogenic bacteria].
    Ann Inst Pasteur (Paris). 1950 Dec;79(6):815-59 PMID: 14811113
  108. Bacterioplankton: a sink for carbon in a coastal marine plankton community.
    Science. 1986 May 16;232(4752):865-7 PMID: 17755970
  109. Direct electron microscopy study on the morphological diversity of bacteriophage populations in lake plusssee.
    Appl Environ Microbiol. 1993 Oct;59(10):3378-84 PMID: 16349070
  110. Microbial gene transfer: an ecological perspective.
    J Mol Microbiol Biotechnol. 1999 Aug;1(1):45-50 PMID: 10941783
  111. Genetic transfer and bacterial taxonomy.
    Bacteriol Rev. 1970 Mar;34(1):40-81 PMID: 4909647
  112. Phage growth characteristics on stationary phase Achromobacter cells.
    J Gen Virol. 1978 Nov;41(2):265-72 PMID: 722281
  113. Minimum bacterial density for bacteriophage replication: implications for significance of bacteriophages in natural ecosystems.
    Appl Environ Microbiol. 1985 Jan;49(1):19-23 PMID: 3156556
  114. Viral contribution to dissolved DNA in the marine environment as determined by differential centrifugation and kingdom probing.
    Appl Environ Microbiol. 1995 Jan;61(1):317-25 PMID: 16534913
  115. Characterization of phage phi O139, a Vibrio cholerae O139 temperate bacteriophage with cohesive DNA termini.
    FEMS Microbiol Lett. 1995 Aug 15;131(1):69-74 PMID: 7557312
  116. Chlorella virus PBCV-1 encodes a homolog of the bacteriophage T4 UV damage repair gene denV.
    Appl Environ Microbiol. 1997 Apr;63(4):1551-6 PMID: 9097450
  117. Genesis of the novel epidemic Vibrio cholerae O139 strain: evidence for horizontal transfer of genes involved in polysaccharide synthesis.
    EMBO J. 1995 Jan 16;14(2):209-16 PMID: 7835331
  118. Effect of particulates on virus survival in seawater.
    J Water Pollut Control Fed. 1975 Jan;47(1):93-103 PMID: 1121053
  119. Fluorometric determination of DNA in aquatic microorganisms by use of hoechst 33258.
    Appl Environ Microbiol. 1982 Jun;43(6):1393-9 PMID: 16346035
  120. Dynamics and Distribution of Cyanophages and Their Effect on Marine Synechococcus spp.
    Appl Environ Microbiol. 1994 Sep;60(9):3167-74 PMID: 16349372
  121. Marine viruses and their biogeochemical and ecological effects.
    Nature. 1999 Jun 10;399(6736):541-8 PMID: 10376593
  122. Life after log.
    J Bacteriol. 1992 Jan;174(2):345-8 PMID: 1729229
  123. Inducible bacteriophages from ruminal bacteria.
    Appl Environ Microbiol. 1989 Jun;55(6):1630-4 PMID: 2504111
  124. Bacteriophage growth on stationary phase Achromobacter cells.
    J Gen Virol. 1976 Jul;32(1):45-50 PMID: 956787
  125. Frequency of morphological phage descriptions in 1995.
    Arch Virol. 1996;141(2):209-18 PMID: 8634015
  126. Use of ultrafiltration to isolate viruses from seawater which are pathogens of marine phytoplankton.
    Appl Environ Microbiol. 1991 Mar;57(3):721-6 PMID: 16348439
  127. A Continuous Culture Model To Examine Factors That Affect Transduction among Pseudomonas aeruginosa Strains in Freshwater Environments.
    Appl Environ Microbiol. 1995 Sep;61(9):3359-66 PMID: 16535123
  128. Lytic viruses infecting a Chlorella-like alga.
    Virology. 1985 Jan 15;140(1):135-43 PMID: 2981448
  129. Dynamics of extracellular DNA in the marine environment.
    Appl Environ Microbiol. 1987 Jan;53(1):170-9 PMID: 3827244
  130. Phage transfer: a new player turns up in cholera infection.
    Science. 1996 Jun 28;272(5270):1869-70 PMID: 8658152
  131. Structure of a marine bacteriophage as revealed by the negative-staining technique.
    J Bacteriol. 1966 Feb;91(2):819-22 PMID: 5883122
  132. Fine structure and host-virus relationship of a marine bacterium and its bacteriophage.
    J Bacteriol. 1966 Nov;92(5):1535-54 PMID: 5924277
  133. Seasonal abundance of lysogenic bacteria in a subtropical estuary
    Appl Environ Microbiol. 1998 Jun;64(6):2308-12 PMID: 9603858
  134. Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton.
    Appl Environ Microbiol. 1996 Jun;62(6):1991-7 PMID: 16535334
  135. Characterizing aquatic bacteria according to population, cell size, and apparent DNA content by flow cytometry.
    Cytometry. 1989 Jan;10(1):70-6 PMID: 2465113
  136. Basic characterization of a lipid-containing bacteriophage specific for plasmids of the P, N, and W compatibility groups.
    Can J Microbiol. 1975 Feb;21(2):152-63 PMID: 46179
  137. Co-adaptation of Escherichia coli and coliphage lambda vir in continuous culture.
    J Gen Microbiol. 1987 Feb;133(2):353-60 PMID: 3309153
  138. A marine bacteriophage.
    Nature. 1955 Apr 16;175(4459):690-1 PMID: 14370199
  139. Frequency of F116-mediated transduction of Pseudomonas aeruginosa in a freshwater environment.
    Appl Environ Microbiol. 1978 Nov;36(5):724-30 PMID: 103503
  140. The Effect of Cyanophages on the Mortality of Synechococcus spp. and Selection for UV Resistant Viral Communities.
    Microb Ecol. 1998 Nov;36(3):281-292 PMID: 9852508
  141. A broad-host-range vibriophage, KVP40, isolated from sea water.
    Microbiol Immunol. 1992;36(1):93-7 PMID: 1584076
  142. Morphological varieties and host ranges of Vibrio parahaemolyticus bacteriophages isolated from seawater.
    Appl Environ Microbiol. 1982 Aug;44(2):466-70 PMID: 7125657
  143. Lysogenic conversion by a filamentous phage encoding cholera toxin.
    Science. 1996 Jun 28;272(5270):1910-4 PMID: 8658163
  144. Fate of viruses in artificial wetlands.
    Appl Environ Microbiol. 1987 Apr;53(4):731-6 PMID: 3034155
  145. Genome data shake tree of life.
    Science. 1998 May 1;280(5364):672-4 PMID: 9599142
  146. Bacteriophage typing.
    Methods Mol Biol. 1995;46:15-26 PMID: 7550706
  147. Induction of phage formation in the lysogenic Escherichia coli K-12 by mitomycin C.
    Nature. 1959 Oct 3;184(Suppl 14):1079-80 PMID: 14429381
  148. Viruses, plasmids and other genetic elements of thermophilic and hyperthermophilic Archaea.
    FEMS Microbiol Rev. 1996 May;18(2-3):225-36 PMID: 8639330
  149. Cyanophages-viruses attacking blue-green algae.
    Bacteriol Rev. 1973 Sep;37(3):343-70 PMID: 4202147
  150. Stability of human enteroviruses in estuarine and marine waters.
    Appl Environ Microbiol. 1976 Aug;32(2):245-9 PMID: 184736
  151. Potential for transfer and establishment of engineered genetic sequences.
    Trends Ecol Evol. 1988 Apr;3(4):S23-7 PMID: 21227125
  152. Independent functions of viral protein and nucleic acid in growth of bacteriophage.
    J Gen Physiol. 1952 May;36(1):39-56 PMID: 12981234
  153. Photoreactivation compensates for UV damage and restores infectivity to natural marine virus communities.
    Appl Environ Microbiol. 1997 Jun;63(6):2200-5 PMID: 9172339
  154. FINE STRUCTURE OF A GENETIC REGION IN BACTERIOPHAGE.
    Proc Natl Acad Sci U S A. 1955 Jun 15;41(6):344-54 PMID: 16589677
  155. The transient phase between growth and nongrowth of heterotrophic bacteria, with emphasis on the marine environment.
    Annu Rev Microbiol. 1987;41:25-49 PMID: 3318670
  156. Transduction of linked chromosomal genes between Pseudomonas aeruginosa strains during incubation in situ in a freshwater habitat.
    Appl Environ Microbiol. 1990 Jan;56(1):140-5 PMID: 2106824
  157. Detection of exogenous gene sequences in dissolved DNA from aquatic environments.
    Microb Ecol. 1989 Jul;18(1):21-8 PMID: 24196018
  158. Incidence of Vibrio parahaemolyticus bacteriophages and other Vibrio bacteriophages in marine samples.
    Appl Environ Microbiol. 1978 Sep;36(3):492-9 PMID: 727781
  159. Reactivation of ultra-violet-inactivated bacteriophage by visible light.
    Nature. 1949 Jun 18;163(4155):949 PMID: 18229246
  160. Chlorella viruses isolated in China.
    Appl Environ Microbiol. 1988 Sep;54(9):2170-3 PMID: 2847652
  161. Mechanism of poliovirus inactivation by cell-free filtrates of marine bacteria.
    Can J Microbiol. 1983 Nov;29(11):1481-6 PMID: 6322946
  162. Are viruses important partners in pelagic fend webs?
    Trends Ecol Evol. 1993 Jun;8(6):209-13 PMID: 21236150
  163. Production of dissolved DNA, RNA, and protein by microbial populations in a Florida reservoir.
    Appl Environ Microbiol. 1990 Oct;56(10):2957-62 PMID: 1704697
  164. Advances in the study of marine viruses.
    Microsc Res Tech. 1997 Apr 15;37(2):136-61 PMID: 9145395
  165. The population biology of bacterial viruses: why be temperate.
    Theor Popul Biol. 1984 Aug;26(1):93-117 PMID: 6484871
  166. 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. 1979 Apr;37(4):774-8 PMID: 453841
  167. Experiments on photoreactivation of bacteriophages inactivated with ultraviolet radiation.
    J Bacteriol. 1950 Mar;59(3):329-47 PMID: 15436402
  168. Diel, seasonal, and depth-related variability of viruses and dissolved DNA in the northern Adriatic Sea.
    Microb Ecol. 1995 Jul;30(1):25-41 PMID: 24185410
  169. High abundance of Archaea in Antarctic marine picoplankton.
    Nature. 1994 Oct 20;371(6499):695-7 PMID: 7935813
  170. Genetic basis of starvation survival in nondifferentiating bacteria.
    Annu Rev Microbiol. 1989;43:293-316 PMID: 2478072
  171. Potential significance of lysogeny to bacteriophage production and bacterial mortality in coastal waters of the gulf of Mexico.
    Appl Environ Microbiol. 1996 Dec;62(12):4374-80 PMID: 16535459
  172. Abundance of viruses in marine waters: assessment by epifluorescence and transmission electron microscopy.
    Appl Environ Microbiol. 1991 Sep;57(9):2731-4 PMID: 16348556
  173. Reproductive fitness of P1, P2, and Mu lysogens of Escherichia coli.
    J Virol. 1977 Feb;21(2):560-4 PMID: 319256
  174. Isolation and characterization of a Pseudomonas aeruginosa bacteriophage with a very limited host range.
    Can J Microbiol. 1989 Jun;35(6):630-5 PMID: 2504471
  175. Distribution of Viruses and Dissolved DNA along a Coastal Trophic Gradient in the Northern Adriatic Sea.
    Appl Environ Microbiol. 1993 Dec;59(12):4074-82 PMID: 16349109
  176. Immunofluorescence detection of the denitrifying strain Pseudomonas stutzeri (ATCC 14405) in seawater and intertidal sediment environments.
    Microb Ecol. 1993 May;25(3):233-46 PMID: 24189920
  177. Evidence for the existence of a restriction-modification system common to several species of the family Vibrionaceae.
    FEMS Microbiol Lett. 1992 Jul 1;73(1-2):191-4 PMID: 1521769
  178. Chesapeake bay anoxia: origin, development, and significance.
    Science. 1984 Jan 6;223(4631):22-7 PMID: 17752972
  179. Distribution of viruses in the Chesapeake Bay.
    Appl Environ Microbiol. 1992 Sep;58(9):2965-70 PMID: 1444409
  180. Host range mutants of bacteriophage Ox2 can use two different outer membrane proteins of Escherichia coli K-12 as receptors.
    J Bacteriol. 1984 Aug;159(2):579-82 PMID: 6378883
  181. Bacterioplankton secondary production estimates for coastal waters of british columbia, antarctica, and california.
    Appl Environ Microbiol. 1980 Jun;39(6):1085-95 PMID: 16345577
  182. Turnover of extracellular DNA in eutrophic and oligotrophic freshwater environments of southwest Florida.
    Appl Environ Microbiol. 1989 Jul;55(7):1823-8 PMID: 16347976
  183. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii.
    Science. 1996 Aug 23;273(5278):1058-73 PMID: 8688087
  184. Amplification of DNA polymerase gene fragments from viruses infecting microalgae.
    Appl Environ Microbiol. 1995 Apr;61(4):1274-8 PMID: 7747950
  185. Inactivation of poliovirus in digested sludge.
    Appl Environ Microbiol. 1976 Jun;31(6):921-30 PMID: 180887
  186. Extinction and viruses.
    Biosystems. 1993;31(2-3):155-9 PMID: 8155848
  187. Preformed magnesium hydroxide precipitate for second-step concentration of enteroviruses from drinking and surface waters.
    Can J Microbiol. 1982 Jul;28(7):783-7 PMID: 6293693
  188. Bacteriophage PRD1: a broad host range DSDNA tectivirus with an internal membrane.
    Adv Virus Res. 1995;45:281-319 PMID: 7793328
  189. Two generalized transducing phages in Vibrio parahaemolyticus and Vibrio alginolyticus.
    Microbiol Immunol. 1991;35(12):1073-84 PMID: 1808461
  190. Viruses and the microbial loop.
    Microb Ecol. 1994 Sep;28(2):209-21 PMID: 24186448
  191. Abundance of Virus-Sized Non-DNase-Digestible DNA (Coated DNA) in Eutrophic Seawater.
    Appl Environ Microbiol. 1993 Mar;59(3):712-7 PMID: 16348887
  192. Isolation and Molecular Characterization of Five Marine Cyanophages Propagated on Synechococcus sp. Strain WH7803.
    Appl Environ Microbiol. 1993 Nov;59(11):3736-43 PMID: 16349088
  193. Virus decay and its causes in coastal waters.
    Appl Environ Microbiol. 1997 Jan;63(1):77-83 PMID: 16535501
  194. Simplified method for dissolved DNA determination in aquatic environments.
    Appl Environ Microbiol. 1986 Oct;52(4):654-9 PMID: 16347160
  195. Viruses as partners in spring bloom microbial trophodynamics.
    Appl Environ Microbiol. 1990 May;56(5):1400-5 PMID: 16348190
  196. Distribution of viral abundance in the reef environment of Key Largo, Florida.
    Appl Environ Microbiol. 1993 Mar;59(3):718-24 PMID: 8480998
  197. Bacterial population dynamics in a meromictic lake.
    Appl Environ Microbiol. 1997 Jun;63(6):2181-8 PMID: 9172337
Article Info
Journal
Microbiology and molecular biology reviews : MMBR
Abbr.
Microbiol Mol Biol Rev
ISSN
1092-2172
Published
2000-03-00
Pages
69-114
Language
English
Region
United States
NLM ID
9706653
PMCID
PMC98987
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]