Skip to main content
Virologica Sinica logoLink to Virologica Sinica
. 2013 Sep 28;28(5):253–259. doi: 10.1007/s12250-013-3370-1

Freshwater cyanophages

Han Xia 1, Tianxian Li 1, Fei Deng 1, Zhihong Hu 1,
PMCID: PMC8208336  PMID: 24132756

Abstract

Cyanophages are double-stranded DNA viruses that infect cyanobacteria, and they can be found in both freshwater and marine environments. They have a complex pattern of host ranges and play important roles in controlling cyanobacteria population. Unlike marine cyanophages, for which there have been a number of recent investigations, very little attention has been paid to freshwater cyanophages. This review summarizes the taxonomy and morphology, host range, distribution, seasonal dynamics, and complete genomes of freshwater cyanophages, as well as diagnostic markers that can be used to identify them.

Keywords: Cyanophage, Freshwater, Morphology, Cyanobacteria

References

  1. Adolph K W, Haselkorn R H. Isolation and characterization of a virus infecting the blue — green algaNostoc muscorum. Virology. 1971;46:200–208. doi: 10.1016/0042-6822(71)90023-7. [DOI] [PubMed] [Google Scholar]
  2. Adolph K W, Haselkorn R. Isolation and characterization of a virus infecting a blue-green alga of the genusSynechococcus. Virology. 1973;54:230–236. doi: 10.1016/0042-6822(73)90132-3. [DOI] [PubMed] [Google Scholar]
  3. Baker A C, Goddard V J, Davy J, Schroeder D C, Adams D G, Wilson W H. Identification of a Diagnostic Marker To Detect Freshwater Cyanophages ofFilamentousCyanobacteria. Appl Environ Microbiol. 2006;72:5713–5719. doi: 10.1128/AEM.00270-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Currier T C, Wolk C P. Characteristics of Anabaena variabilis influencing plaque formation by cyanophage N-1. J Bacteriol. 1979;139:88–92. doi: 10.1128/jb.139.1.88-92.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Deng L, Hayes P K. Evidence for cyanophages active against bloom-forming freshwater cyanobacteria. Freshw Biol. 2008;53:1240–1252. doi: 10.1111/j.1365-2427.2007.01947.x. [DOI] [Google Scholar]
  6. Dreher T W, Brown N, Bozarth C S, Schwartz A D, Riscoe E, Thrash C, Bennett S E, Tzeng S C, Maier C S. A freshwater cyanophage whose genome indicates close relationships to photosynthetic marine cyanomyophages. Environ Microbiol. 2011;13:1858–1874. doi: 10.1111/j.1462-2920.2011.02502.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fox J A, Booth S J, Martin E L. Cyanophage SM-2: a new blue-green algal virus. Virology. 1976;73:557–560. doi: 10.1016/0042-6822(76)90420-7. [DOI] [PubMed] [Google Scholar]
  8. Fuhrman J A. Marine viruses and their biogeochemical and ecological effects. Nature. 1999;399:541–548. doi: 10.1038/21119. [DOI] [PubMed] [Google Scholar]
  9. Gao E B, Yuan X P, Li R, Zhang Q Y. Isolation of a novel cyanophage infectious to the filamentous cyanobacterium planktothrix agardhii(cyanophyceae) from Lake Donghu, China. Aquat Microb Ecol. 2009;54:153–162. doi: 10.3354/ame01266. [DOI] [Google Scholar]
  10. Gao E B, Gui J F, Zhang Q Y. A Novel Cyanophage with Cyanobacterial Non-bleaching Protein A Gene in the Genome. J Virol. 2012;86:236–245. doi: 10.1128/JVI.06282-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hambly E, Tetart F, Desplats C, Wilson W H, Krisch H M, Mann N H. A conserved genetic module that encodes the major virion components in both the coliphage T4 and the marine cyanophage S-PM2. Proc Natl Acad Sci USA. 2001;98:11411–11416. doi: 10.1073/pnas.191174498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hu N T, Theil T, Giddings T H, Wolk C P. NewAnabaena and Nostoccyanophages from sewage settling ponds. Virology. 1981;114:236–246. doi: 10.1016/0042-6822(81)90269-5. [DOI] [PubMed] [Google Scholar]
  13. Khudyakov I Y, Kirnos M D, Alexandrushkina N I, Vanyushin B F. Cyanophage S-2L contains DNA with 2,6-diaminopurine substituted for adenine. Virology. 1978;88:8–18. doi: 10.1016/0042-6822(78)90104-6. [DOI] [PubMed] [Google Scholar]
  14. Khudyakov I Y, Matveev A V. New cyanophages S-4L and S-5L lysing Synechococcus elongatus. Microbiol. 1982;51:102–106. [Google Scholar]
  15. Kirons M D, Khudyakov I Y, Alexandrushkina N I, Vanyushin B F. 2-Aminoadenine is an adenine substituting for a base in S-2L cyanophage DNA. Nature. 1977;270:369–370. doi: 10.1038/270369a0. [DOI] [PubMed] [Google Scholar]
  16. Liu X Y, Kong S L, Shi M, Fu L W, Gao Y, An C C. Genomic analysis of freshwater cyanophage Pf-WMP3 infecting yanobacteriumPhormidium foveolarum: the conserved elements for a phage. Microb Ecol. 2008;56:671–680. doi: 10.1007/s00248-008-9386-7. [DOI] [PubMed] [Google Scholar]
  17. Liu X Y, Shi M, Kong S L, Gao Y, An C C. Cyanophage Pf-WMP4, a T7-like phage infecting the freshwater cyanobacteriumPhormidium foveolarum: complete genome sequence and DNA translocation. Virology. 2007;366:28–39. doi: 10.1016/j.virol.2007.04.019. [DOI] [PubMed] [Google Scholar]
  18. Majumdar A K, Singh S P. A phage typing scheme forSalmonella bareilly. Indian Vet. J. 1973;50:1161–1166. [Google Scholar]
  19. Martin E L, Tyler A K. Encyclopedia of Virology, vol. 1. 2nd edition. London, UK: Allan Granoff and Robert G. Webster, Editors. Academic Press; 1999. Cyanophages; pp. 324–332. [Google Scholar]
  20. Middelboe M, Jacquet S, Weinbauer M. Viruses in freshwater ecosystems: an introduction to the exploration of viruses in new aquatic habitats. Freshwater Biol. 2008;53:1069–1075. doi: 10.1111/j.1365-2427.2008.02014.x. [DOI] [Google Scholar]
  21. Padan E, Shilo M. Distribution of cyanophages in natural habitats. Verh Internat Verein Limnol. 1969;17:747–751. [Google Scholar]
  22. Padan E, Shilo M. Cyanophages-viruses attacking blue-green algae. Bacteriol Rev. 1973;37:343–370. doi: 10.1128/br.37.3.343-370.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Padhy R N, Singh P K. Lysogeny in the blue green algaNostoc muscorum. Arch Microbiol. 1978;117:265–268. doi: 10.1007/BF00738545. [DOI] [Google Scholar]
  24. Safferman R S. Phycoviruses. In: Carr NG, Whitton BA, editors. The biology of blue-green algae. Oxford: Blackwell Scientific Publications; 1973. pp. 214–237. [Google Scholar]
  25. Safferman R S, Diener T O, Desjardins P R, Morris M E. Isolation and characterization of AS-1, a phycovirus infecting the blue-green algae, Anacystis nidulans and Synechococcus cedorum. Virology. 1972;47:105–113. doi: 10.1016/0042-6822(72)90243-7. [DOI] [PubMed] [Google Scholar]
  26. Safferman R S, Morris M E. Algal virus: Isolation. Science. 1963;140:679–680. doi: 10.1126/science.140.3567.679. [DOI] [PubMed] [Google Scholar]
  27. Safferman R S, Schneider I R, Steere R L, Morris M E, Diener T O. Phycovirus SM-1: a virus infecting unicellular blue-green algae. Virology. 1969;37:386–395. doi: 10.1016/0042-6822(69)90222-0. [DOI] [PubMed] [Google Scholar]
  28. Schneider I R, Diener T O, Safferman R S. Blue-green algal virus LPP-1: purification and partial characterization. Science. 1964;144:1127–1130. doi: 10.1126/science.144.3622.1127. [DOI] [PubMed] [Google Scholar]
  29. Shane M S. Distribution of blue-green algal viruses in various types of natural waters. Water Res. 1971;5:711–716. doi: 10.1016/0043-1354(71)90093-5. [DOI] [Google Scholar]
  30. Sherman L A, Haselkorn R. LPP-1 infection of the blue-green algaPlectonema boryanum. J Virol. 1970;6:820–833. doi: 10.1128/jvi.6.6.820-833.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Short C M, Suttle C A. Nearly identical bacteriophage structural gene sequences are widely distributed in both marine and freshwater environments. Appl Environ Microbiol. 2005;71:480–486. doi: 10.1128/AEM.71.1.480-486.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Singh P, Singh S S, Srivastava A, Singh A, Mishra A K. Structural, functional and molecular basis of cyanophage-cyanobacterial interactions and its significance. Afr J Biotechnol. 2012;11:2591–2608. [Google Scholar]
  33. Sode K, Oozeki M, Asakawa K, Burgess J G, Matsunaga T. Isolation of a marine cyanophage infecting the marine unicellular cyanobacterium, Synechoccus sp. NKBG 042902. J Mar Biotechnol. 1994;1:189–192. [Google Scholar]
  34. Sullivan M B, Waterbury J B, Chisholm S W. Cyanophages infecting the oceanic cyanobacteriumProchlorococcus. Nature. 2003;424:1047–1051. doi: 10.1038/nature01929. [DOI] [PubMed] [Google Scholar]
  35. Suttle C A. Cyanophages and their role in the ecology of cyanobacteria. In: Whitton BA, Potts M, editors. The ecology of cyanobacteria. Their diversity in time and space. Dordrecht: Kluwer Academic Publishers; 2000. pp. 563–589. [Google Scholar]
  36. Suttle C A. Viruses in the sea. Nature. 2005;437:356–461. doi: 10.1038/nature04160. [DOI] [PubMed] [Google Scholar]
  37. Suttle C A, Chan A M, Feng F, Garza D R. Cyanophages and sunlight: a paradox. In: Guerrero R, Pedros-Alio C, editors. Trends in microbial ecology. Barcelona, Spain: Spanish Society for Microbiology; 1993. pp. 303–307. [Google Scholar]
  38. Takashima Y, Yoshida T, Yoshida M, Shirai Y, Tomaru Y, Takao Y, Hiroishi S, Nagasaki K. Development and application of quantitative detection of cyanophages phylogenetically related to cyanophage Ma-LMM01 InfectingMicrocystis aeruginosain fresh Water. Microbes Environ. 2007;22:207–213. doi: 10.1264/jsme2.22.207. [DOI] [Google Scholar]
  39. Tucker S, Pollard P. Identification of cyanophage Ma-LBP and infection of the cyanobacteriumMicrocystis aeruginosafrom an Australian subtropical lake by the virus. Appl Environ Microbiol. 2005;71:629–635. doi: 10.1128/AEM.71.2.629-635.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wilhelm S W, Carberry M J, Eldridge M L, Poorvin L, Saxton M A. Marine and freshwater cyanophages in a Laurentian Great Lake: evidence from infectivity assays and molecular analyses of g20 genes. Appl Environ Microb. 2006;72:4957–4963. doi: 10.1128/AEM.00349-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wilhelm S W, Matteson A R. Freshwater and marine virioplankton: a brief overview of commonalities and differences. Freshwater Biol. 2008;53:1076–1089. doi: 10.1111/j.1365-2427.2008.01980.x. [DOI] [Google Scholar]
  42. WHO . Guidelines for safe recreational water environments. 2009. [Google Scholar]
  43. Yoshida M, Yoshida T, Kashima A, Takashima Y, Hosoda N, Nagasaki K, Hiroishi S. Ecological dynamics of the toxic bloom-forming cyanobacteriumMicrocystis aeruginosaand its cyanophages in freshwater. Appl Environ Microbiol. 2008;74:3269–3273. doi: 10.1128/AEM.02240-07. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yoshida T, Takashima Y, Tomaru Y, Shirai Y, Takao Y, Hiroishi S, Nagasaki K. Isolation and Characterization of a Cyanophage Infecting the Toxic Cyanobacterium Microcystis aeruginosa. Appl Environ Microbiol. 2006;72:1239–1247. doi: 10.1128/AEM.72.2.1239-1247.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Yoshida T, Nagasaki K, Takashima Y, Shirai Y, Tomaru Y, Takao Y, Sakamoto S, Hiroishi S, Ogata H. Ma-LMM01 infecting toxicMicrocystis aeruginosailluminates diverse cyanophage genome strategies. J Bacteriol. 2008;190:1762–1772. doi: 10.1128/JB.01534-07. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Zhao Y J, Chen K, Shi Z L, Guo Y X, Zhu H Y, Zhang J H, Liu Y D. Isolation and identification of the first cyanophage in China. Pro Nat Sci. 2002;12:923–927. [Google Scholar]
  47. Zhou Y R, Lin J, Li N, Hu Z H, Deng F. Characterization and genomic analysis of a plaque purified strain of cyanophage PP. 2013. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Virologica Sinica are provided here courtesy of Wuhan Institute of Virology, Chinese Academy of Sciences

RESOURCES