Extremophiles

, Volume 17, Issue 1, pp 99–114 | Cite as

Genomic analysis of cold-active Colwelliaphage 9A and psychrophilic phage–host interactions

Original Paper

Abstract

The 104 kb genome of cold-active bacteriophage 9A, which replicates in the marine psychrophilic gamma-proteobacterium Colwellia psychrerythraea strain 34H (between −12 and 8 °C), was sequenced and analyzed to investigate elements of molecular adaptation to low temperature and phage–host interactions in the cold. Most characterized ORFs indicated closest similarity to gamma-proteobacteria and their phages, though no single module provided definitive phylogenetic grouping. A subset of primary structural features linked to psychrophily suggested that the majority of annotated phage proteins were not psychrophilic; those that were, primarily serve phage-specific functions and may also contribute to 9A’s restricted temperature range for replication as compared to host. Comparative analyses suggest ribonucleotide reductase genes were acquired laterally from host. Neither restriction modification nor the CRISPR-Cas system appeared to be the predominant phage defense mechanism of Cp34H or other cold-adapted bacteria; we hypothesize that psychrophilic hosts rely more on the use of extracellular polymeric material to block cell surface receptors recognized by phages. The relative dearth of evidence for genome-specific defenses, genetic transfer events or auxiliary metabolic genes suggest that the 9A-Cp34H system may be less tightly coupled than are other genomically characterized marine phage–host systems, with possible implications for phage specificity under different environmental conditions.

Keywords

Bacteriophage Psychrophilic Colwellia Siphoviridae Genome Lateral gene transfer Phage-defense strategies EPS 

Abbreviations

9A

Colwelliaphage 9A

11b

Flavobacteriophage 11b

AMG

Auxiliary metabolic gene

CDS

Coding sequence corresponding to sequence of amino acids in predicted protein including start and stop codons

ch

Conserved hypothetical protein

Cp34H

Colwellia psychrerythraea strain 34H

CRISPR

Clustered regularly interspaced short palindromic repeat

EPS

Extracellular polymeric substances

LGT

Lateral gene transfer

MPSP

Marine Phage Sequencing Project

MT

Methyltransferase

nr

NCBI Genbank non-redundant database

nrd

Ribonucleotide reductase

ORF

Open reading frame

ORFan

ORF with no known homolog

PHS

Phage–host system

pp

Predicted protein

RE

Restriction enzyme

RM

Restriction-modification system

SD

Standard deviation

Supplementary material

792_2012_497_MOESM1_ESM.pdf (297 kb)
Fig. S1. Colwelliaphage 9A ORF protein characters compared to mean character value for all 9A ORFs. Each subfigure shows deviation from 9A genome character mean as fraction of that mean for each ORF. Modules separated with vertical lines. * indicates ORF contained no Glutamic Acid (E) residues, but was graphed as though it contained 1. Only ORFs with a minimum of two protein characters values scored as psychrophilic, or one character scored as strongly psychrophilic are shown. Note varying scale of x-axes. See text for definition of character values binned as psychrophilic and strongly psychrophilic and Table S1 for gene abbreviations (PDF 297 kb)
792_2012_497_MOESM2_ESM.pdf (1.1 mb)
Table S1 (PDF 1113 kb)
792_2012_497_MOESM3_ESM.pdf (133 kb)
Table S2 (PDF 133 kb)
792_2012_497_MOESM4_ESM.pdf (59 kb)
Table S3 (PDF 60 kb)
792_2012_497_MOESM5_ESM.pdf (92 kb)
Table S4 (PDF 92 kb)

References

  1. Ackermann H-W (2001) Frequency of morphological phage descriptions in the year 2000. Arch Virol 146(5):843–857PubMedCrossRefGoogle Scholar
  2. Allen MA, Lauro FM, Williams TJ, Burg D, Siddiqui KS, De Francisci D, Chong KW, Pilak O, Chew HH, De Maere MZ, Ting L, Katrib M, Ng C, Sowers KR, Galperin MY, Anderson IJ, Ivanova N, Dalin E, Martinez M, Lapidus A, Hauser L, Land M, Thomas T, Cavicchioli R (2009) The genome sequence of the psychrophilic archaeon, Methanococcoides burtonii: the role of genome evolution in cold adaptation. ISME J 3(9):1012–1035PubMedCrossRefGoogle Scholar
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410PubMedGoogle Scholar
  4. Alvarez M, Zeelen JP, Mainfroid V, Rentier-Delrue F, Martial JA, Wyns L, Wierenga RK, Maes D (1998) Triose-phosphate isomerase (TIM) of the psychrophilic bacterium Vibrio marinus. Kinetic and structural properties. J Biol Chem 273(4):2199–2206PubMedCrossRefGoogle Scholar
  5. Anderson RE, Brazelton WJ, Baross JA (2011) Using CRISPRs as a metagenomic tool to identify microbial hosts of a diffuse flow hydrothermal vent viral assemblage. FEMS Microbiol Ecol 77(1):120–133PubMedCrossRefGoogle Scholar
  6. Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, Carlson C, Chan AM, Haynes M, Kelley S, Liu H, Mahaffy JM, Mueller JE, Nulton J, Olson R, Parsons R, Rayhawk S, Suttle CA, Rohwer F (2006) The marine viromes of four oceanic regions. PLoS Biol 4(11):2121–2131CrossRefGoogle Scholar
  7. Aoyama A, Hayashi M (1985) Effects of genome size on bacteriophage phi X174 DNA packaging in vitro. J Biol Chem 260(20):11033–11038PubMedGoogle Scholar
  8. Ayala-del-Río HL, Chain PS, Grzymski JJ, Ponder MA, Ivanova N, Bergholz PW, Di Bartolo G, Hauser L, Land M, Bakermans C, Rodrigues D, Klappenbach J, Zarka D, Larimer F, Richardson P, Murray A, Thomashow M, Tiedje JM (2010) The genome sequence of Psychrobacter arcticus 273-4, a psychroactive Siberian permafrost bacterium, reveals mechanisms for adaptation to low-temperature growth. Appl Environ Microbiol 76(7):2304–2312PubMedCrossRefGoogle Scholar
  9. Bakermans C (2012) Psychrophiles: life in the cold. In: Anitori R (ed) Extremophiles: microbiology and biotechnology. Caister Academic Press, Norwich, pp 53–76Google Scholar
  10. Bergholz PW, Bakermans C, Tiedje JM (2009) Psychrobacter arcticus 273-4 uses resource efficiency and molecular motion adaptations for subzero temperature growth. J Bacteriol 191(7):2340–2352PubMedCrossRefGoogle Scholar
  11. Bolotin A, Quinquis B, Sorokin A, Ehrlich SD (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151(8):2551–2561PubMedCrossRefGoogle Scholar
  12. Borriss M, Helmke E, Hanschke R, Schweder T (2003) Isolation and characterization of marine psychrophilic phage–host systems from Arctic sea ice. Extremophiles 7:377–384PubMedCrossRefGoogle Scholar
  13. Borriss M, Lombardot T, Glöckner FO, Becher D, Albrecht D, Schweder T (2007) Genome and proteome characterization of the psychrophilic Flavobacterium bacteriophage 11b. Extremophiles 11(1):95–104PubMedCrossRefGoogle Scholar
  14. Bowman JP, Gosink JJ, McCammon SA, Lewis TE, Nichols DS, Nichols PD, Skerratt JH, Staley JT, McMeekin TA (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:ω63). Int J Syst Bacteriol 48(4):1171–1180CrossRefGoogle Scholar
  15. Breitbart M, Thompson LR, Suttle CA, Sullivan MB (2007) Exploring the vast diversity of marine viruses. Oceanography 20(2):135–139CrossRefGoogle Scholar
  16. Carver TJ, Rutherford KM, Berriman M, Rajandream M-A, Barrell BG, Parkhill J (2005) ACT: the Artemis comparison tool. Bioinformatics 21:3422–3423PubMedCrossRefGoogle Scholar
  17. Chopin M-C, Chopin A, Bidnenko E (2005) Phage abortive infection in lactococci: variations on a theme. Curr Opin Microbiol 8(4):473–479Google Scholar
  18. Cock PJA, Antao T, Chang JT, Chapman BA, Cox CJ, Dalke A, Friedberg I, Hamelryck T, Kauff F, Wilczynski B, de Hoon MJL (2009) Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25:1422–1423PubMedCrossRefGoogle Scholar
  19. Collins RE (2009) Identification of an inter-order lateral gene transfer event enabling the catabolism of common compatible solutes by Colwellia psychrerythraea 34H. In: Collins RE (ed) Microbial evolution in sea ice: communities to genes. PhD Dissertation. University of Washington, Seattle, pp 147–177Google Scholar
  20. Collins RE, Deming JW (2011) Abundant dissolved genetic material in Arctic sea ice Part II: viral dynamics during autumn freeze-up. Polar Biol 43(12):1831–1841CrossRefGoogle Scholar
  21. Deming JW (2010) Sea ice bacteria and viruses. In: Thomas DN, Dieckman GS (eds) Sea ice—an introduction to its physics, chemistry, biology and geology, 2nd edn. Blackwell Science Ltd, Oxford, pp 247–82Google Scholar
  22. Deming JW, Eicken H (2007) Life in ice. In: Sullivan WT, Baross JA (eds) Planets and life: the emerging science of astrobiology. Cambridge University Press, Cambridge, pp 292–312Google Scholar
  23. Ewert M, Deming JW (2011) Selective retention in saline ice of extracellular polysaccharides produced by the cold-adapted marine bacterium Colwellia psychrerythraea strain 34H. Ann Glaciol 52(57):111–117CrossRefGoogle Scholar
  24. Fuhrman JA, Noble RT (1995) Viruses and protists cause similar bacterial mortality in coastal seawater. Limnol Oceanogr 40(7):1236–1242CrossRefGoogle Scholar
  25. Grissa I, Vergnaud G, Pourcel C (2007a) CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35:W52–W57PubMedCrossRefGoogle Scholar
  26. Grissa I, Vergnaud G, Pourcel C (2007b) The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 8:172–181PubMedCrossRefGoogle Scholar
  27. Hambly E, Suttle CA (2005) The viriosphere, diversity, and genetic exchange within phage communities. Curr Opin Microbiol 8(4):444–450PubMedCrossRefGoogle Scholar
  28. Hammad AM (1998) Evaluation of alginate-encapsulated Azotobacter chroococcum as a phage-resistant and an effective inoculum. J Basic Microbiol 38(1):9–16CrossRefGoogle Scholar
  29. Hanlon GW, Denyer SP, Olliff CJ, Ibrahim LJ (2001) Reduction in exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 67(6):2746–2753PubMedCrossRefGoogle Scholar
  30. Hatfull GF (2008) Bacteriophage genomics. Curr Opin Microbiol 11(5):447–453PubMedCrossRefGoogle Scholar
  31. Hendrix RW, Smith MCM, Burns RN, Ford ME, Hatfull GF (1999) Evolutionary relationships among diverse bacteriophages and prophages: all the world’s a phage. Proc Natl Acad Sci 96(5):2192–2197PubMedCrossRefGoogle Scholar
  32. Henn MR, Sullivan MB, Stange-Thomann N, Osburne MS, Berlin AM, Kelly L, Yandava C, Kodira C, Zeng Q, Weiand M, Sparrow T, Saif S, Giannoukos G, Nusbaum C, Young SK, Birren BW, Chisholm SW (2010) Analysis of high-throughput sequencing and annotation strategies for phage genomes. PLoS One 5(2):1–12CrossRefGoogle Scholar
  33. Huang S, Zhang Y, Chen F, Jiao N (2011) Complete genome sequence of a marine roseophage provides evidence into the evolution of gene transfer agents in alphaproteobacteria. Virol J 8:124–129PubMedCrossRefGoogle Scholar
  34. Hughes KA, Sutherland IW, Clark J, Jones MV (1998) Bacteriophage and associated polysaccharide depolymerases—novel tools for study of bacterial biofilms. J Appl Microbiol 85(3):583–590PubMedCrossRefGoogle Scholar
  35. Hulo C, de Castro E, Masson P, Bougueleret L, Bairoch A, Xenarios I, Le Mercier P (2010) ViralZone: a knowledge resource to understand virus diversity. Nucleic Acids Res 39:D576–D582PubMedCrossRefGoogle Scholar
  36. Huston AL, Methe B, Deming JW (2004) Purification, characterization, and sequencing of an extracellular cold-active aminopeptidase produced by marine psychrophile Colwellia psychrerythraea strain 34H. Appl Environ Microbiol 70(6):3321–3328PubMedCrossRefGoogle Scholar
  37. Jain R, Rivera MC, Lake JA (1999) Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci 96(7):3801–3806PubMedCrossRefGoogle Scholar
  38. Jiang SC, Paul JH (1998) Gene transfer by transduction in the marine environment. Appl Environ Microbiol 64(8):2780–2787PubMedGoogle Scholar
  39. Jorgensen BB, Boetius A (2007) Feast and famine—microbial life in the deep-sea bed. Nat Rev Microbiol 5(10):770–781PubMedCrossRefGoogle Scholar
  40. Jumars PA, Deming JW, Hill PS, Karp-Boss L, Yager PL, Dade WB (1993) Physical constraints on marine osmotrophy in an optimal foraging context. Mar Microb Food Webs 7(2):121–159Google Scholar
  41. Krembs C, Eicken H, Deming JW (2011) Exopolymer alteration of physical properties of sea ice and implications for ice habitability and biogeochemistry in a warmer Arctic. Proc Natl Acad Sci 108(9):3653–3658PubMedCrossRefGoogle Scholar
  42. Kwan T, Liu J, DuBow M, Gros P, Pelletier J (2005) The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc Natl Acad Sci 102(14):5174–5179PubMedCrossRefGoogle Scholar
  43. Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8(5):317–327PubMedCrossRefGoogle Scholar
  44. Liebner S, Wagner D (2007) Abundance, distribution and potential activity of methane oxidizing bacteria in permafrost soils from the Lena Delta, Siberia. Environ Microbiol 9:107–117PubMedCrossRefGoogle Scholar
  45. Lohr JE, Chen F, Hill RT (2005) Genomic analysis of bacteriophage PhiJL001: insights into its interaction with a sponge-associated alpha-proteobacterium. Appl Environ Microbiol 71(3):1598–1609PubMedCrossRefGoogle Scholar
  46. Mann NH, Clokie MRJ, Millard A, Cook A, Wilson WH, Wheatley PJ, Letarov A, Krisch HM (2005) The genome of S-PM2, a “photosynthetic” T4-type bacteriophage that infects marine Synechococcus strains. J Bacteriol 187(9):3188–3200PubMedCrossRefGoogle Scholar
  47. Marx JG, Carpenter SD, Deming JW (2009) Production of cryoprotectant extracellular polysaccharide substances (EPS) by the marine psychrophilic bacterium Colwellia psychrerythraea strain 34H under extreme conditions. Can J Microbiol 55(1):63–72PubMedCrossRefGoogle Scholar
  48. McInerney MJ, Rohlin L, Mouttaki H, Kim U, Krupp RS, Rios-Hernandez L, Sieber J, Struchtemeyer CG, Bhattacharyya A, Campbell JW, Robert P, Gunsalus RP (2007) The genome of Syntrophus aciditrophicus: life at the thermodynamic limit of microbial growth. Proc Natl Acad Sci 104(18):7600–7605PubMedCrossRefGoogle Scholar
  49. Methé BA, Nelson KE, Deming JW, Momen B, Melamud E, Zhang X, Moult J, Madupu R, Nelson WC, Dodson RJ, Brinkac LM, Daugherty SC, Durkin AS, DeBoy RT, Kolonay JF, Sullivan SA, Zhou L, Davidsen TM, Wu M, Huston AL, Lewis M, Weaver B, Weidman JF, Khouri H, Utterback TR, Feldblyum TV, Fraser CM (2005) The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc Natl Acad Sci 102(31):10913–10918PubMedCrossRefGoogle Scholar
  50. Metpally R, Reddy B (2009) Comparative proteome analysis of psychrophilic versus mesophilic bacterial species: insights into the molecular basis of cold adaptation of proteins. BMC Genomics 10(11):1–10Google Scholar
  51. Naito T, Kusano K, Kobayashi I (1995) Selfish behavior of restriction-modification systems. Science 267(5199):897–899PubMedCrossRefGoogle Scholar
  52. Notredame C, Higgins DG, Heringa J (2000) T-coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302(1):205–217PubMedCrossRefGoogle Scholar
  53. Olsen RH, Metcalf ES (1968) Conversion of mesophilic to psychrophilic bacteria. Science 162(3859):1288–1289PubMedCrossRefGoogle Scholar
  54. Paul JH, Williamson SJ, Long A, Authement RN, John D, Segall AM, Rohwer FL, Androlewicz M, Patterson S (2005) Complete genome sequence of ϕHSIC, a pseudotemperate marine phage of Listonella pelagia. Appl Environ Microbiol 71(6):3311–3320PubMedCrossRefGoogle Scholar
  55. Pomeroy LR, Wiebe WJ (2001) Temperature and substrates as interactive limiting factor for marine heterotrophic bacteria. Aquat Microb Ecol 23:187–204CrossRefGoogle Scholar
  56. Rivkina E, Laurinavichius K, McGrath J, Tiedje J, Shcherbakova V, Gilichinsky D (2004) Microbial life in permafrost. Adv Space Res 33(8):1215–1221PubMedCrossRefGoogle Scholar
  57. Roberts RJ, Vincze T, Posfai J, Macelis D (2010) REBASE—a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res 38:D234–D236PubMedCrossRefGoogle Scholar
  58. Rodrigues DF, Tiedje JM (2008) Coping with our cold planet. Appl Environ Microbiol 74(6):1677–1686PubMedCrossRefGoogle Scholar
  59. Rohwer F, Thurber RV (2009) Viruses manipulate the marine environment. Nature 459(7244):207–212PubMedCrossRefGoogle Scholar
  60. Rosario K, Breitbart M (2011) Exploring the viral world through metagenomics. Curr Opin Virol 1(4):289–297PubMedCrossRefGoogle Scholar
  61. Russell NJ, Harrisson P, Johnston IA, Jaenicke R, Zuber M, Franks F, Wynn-Williams D (1990) Cold adaptation of microorganisms. Philos Trans R Soc B 326(1237):595–611CrossRefGoogle Scholar
  62. Sano E, Carlson S, Wegley L, Rohwer F (2004) Movement of viruses between biomes. Appl Environ Microbiol 70(10):5842–5846PubMedCrossRefGoogle Scholar
  63. Stern A, Sorek R (2011) The phage–host arms race: shaping the evolution of microbes. BioEssays 33(1):43–51PubMedCrossRefGoogle Scholar
  64. Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW (2005) Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3(5):790–806CrossRefGoogle Scholar
  65. Sullivan MB, Krastins B, Hughes JL, Kelly L, Chase M, Sarracino D, Chisholm SW (2009) The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial “mobilome”. Environ Microbiol 11(11):2935–2951PubMedCrossRefGoogle Scholar
  66. Suttle CA (1994) The significance of viruses to mortality in aquatic microbial communities. Microb Ecol 28(2):237–243CrossRefGoogle Scholar
  67. Suttle CA (2007) Marine viruses—major players in the global ecosystem. Nat Rev Microbiol 5(10):801–812PubMedCrossRefGoogle Scholar
  68. Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28(1):33–36PubMedCrossRefGoogle Scholar
  69. Thomas DN, Dieckmann GS (2002) Antarctic sea ice—a habitat for extremophiles. Science 295(5555):641–644PubMedCrossRefGoogle Scholar
  70. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680PubMedCrossRefGoogle Scholar
  71. Thompson LR, Zeng Q, Kelly L, Huang KH, Singer AU, Stubbe J, Chisholm SW (2011) Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc Natl Acad Sci 108(39):E757–E764PubMedCrossRefGoogle Scholar
  72. Ting L, Williams TJ, Cowley MJ, Lauro FM, Guilhaus M, Raftery MJ, Cavicchioli R (2010) Cold adaptation in the marine bacterium, Sphingopyxis alaskensis, assessed using quantitative proteomics. Environ Microbiol 12(10):2658–2676PubMedGoogle Scholar
  73. Tock MR, Dryden DTF (2005) The biology of restriction and anti-restriction. Curr Opin Microbiol 8(4):466–472PubMedCrossRefGoogle Scholar
  74. Van Valen L (1973) A new evolutionary law. Evolut Theor 1(1):1–3Google Scholar
  75. Wan X-F, Zhou J, Xu D (2006) CodonO: a new informatics method for measuring synonymous codon usage bias within and across genomes. Int J Gen Syst 35(1):109–125CrossRefGoogle Scholar
  76. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25(9):1189–1191PubMedCrossRefGoogle Scholar
  77. Weinbauer MG, Rassoulzadegan F (2004) Are viruses driving microbial diversification and diversity? Environ Microbiol 6(1):1–11PubMedCrossRefGoogle Scholar
  78. Wells LE (2006) Lysogeny among psychrophilic Colwellia. In: Wells LW (ed) Viral adaptations to life in the cold. PhD Dissertation. University of Washington, Seattle, pp 269–92Google Scholar
  79. Wells LE (2008) Cold-active viruses. In: Margesin R, Schinner F, Marx JC, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, London, pp 157–173CrossRefGoogle Scholar
  80. Wells LE, Deming JW (2006a) Significance of bacterivory and viral lysis in bottom waters of Franklin Bay, Canadian Arctic, during winter. Aquat Microb Ecol 43(3):209–221CrossRefGoogle Scholar
  81. Wells LE, Deming JW (2006b) Characterization of a cold-active bacteriophage on two psychrophilic marine hosts. Aquat Microb Ecol 45(1):15–29CrossRefGoogle Scholar
  82. Wells LE, Deming JW (2006c) Effects of temperature, salinity and clay particles on inactivation and decay of cold-active marine Bacteriophage 9A. Aquat Microb Ecol 45(1):31–39CrossRefGoogle Scholar
  83. Wells LE, Deming JW (2006d) Modeled and measured dynamics of viruses in Arctic winter sea-ice brines. Environ Microbiol 8(6):1115–1121PubMedCrossRefGoogle Scholar
  84. Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531–552PubMedGoogle Scholar
  85. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Bio Rev 64(1):69–114CrossRefGoogle Scholar

Copyright information

© Springer Japan 2012

Authors and Affiliations

  1. 1.School of Oceanography and Astrobiology ProgramUniversity of WashingtonSeattleUSA

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