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Genome sequence of a novel deep-sea vent epsilonproteobacterial phage provides new insight into the co-evolution of Epsilonproteobacteria and their phages

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Abstract

Epsilonproteobacteria are among the predominant primary producers in deep-sea hydrothermal vent ecosystems. However, phages infecting deep-sea vent Epsilonproteobacteria have never been isolated and characterized. Here, we successfully isolated a novel temperate phage, NrS-1, that infected a deep-sea vent chemolithoautotrophic isolate of Epsilonproteobacteria, Nitratiruptor sp. SB155-2, and its entire genome sequence was obtained and analyzed. The NrS-1 genome is linear, circularly permuted, and terminally redundant. The NrS-1 genome is 37,159 bp in length and contains 51 coding sequences. Five major structural proteins including major capsid protein and tape measure protein were identified by SDS-PAGE and mass spectrometry analysis. NrS-1 belongs to the family Siphoviridae, but its sequence and genomic organization are distinct from those of any other previously known Siphoviridae phages. Homologues of genes encoded in the NrS-1 genome were widely distributed among the genomes of diverse Epsilonproteobacteria. The distribution patterns had little relation to the evolutionary traits and ecological and physiological differentiation of the host epsilonproteobacterial species. The widespread occurrence of phage genes in diverse Epsilonproteobacteria supports early co-evolution between temperate phages and Epsilonproteobacteria prior to the divergence of their habitats and physiological adaptation.

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References

  • Aggeler R, Coons J, Taylor SW, Ghosh SS, Garcia JJ, Capaldi RA, Marusich MF (2002) A functionally active human F1F0 ATPase can be purified by immunocapture from heart tissue and fibroblast cell lines. Subunit structure and activity studies. J Biol Chem 277:33906–33912

    Article  PubMed  CAS  Google Scholar 

  • Anderson I, Sikorski J, Zeytun A, Nolan M, Lapidus A, Lucas S, Hammon N, Deshpande S, Cheng JF, Tapia R, Han C, Goodwin L, Pitluck S, Liolios K, Pagani I, Ivanova N, Huntemann M, Mavromatis K, Ovchinikova G, Pati A, Chen A, Palaniappan K, Land M, Hauser L, Brambilla EM, Ngatchou-Djao OD, Rohde M, Tindall BJ, Goker M, Detter JC, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Klenk HP, Kyrpides NC (2011a) Complete genome sequence of Nitratifractor salsuginis type strain (E9I37-1). Stand Genomic Sci 4:322–330

    Article  PubMed  CAS  Google Scholar 

  • Anderson RE, Brazelton WJ, Baross JA (2011b) Using CRISPRs as a metagenomic tool to identify microbial hosts of a diffuse flow hydrothermal vent viral assemblage. FEMS Microbiol Ecol 77:120–133

    Article  PubMed  CAS  Google Scholar 

  • Besemer J, Lomsadze A, Borodovsky M (2001) GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 29:2607–2618

    Article  PubMed  CAS  Google Scholar 

  • Brazelton WJ, Schrenk MO, Kelley DS, Baross JA (2006) Methane- and sulfur-metabolizing microbial communities dominate the Lost City hydrothermal field ecosystem. Appl Environ Microbiol 72:6257–6270

    Article  PubMed  CAS  Google Scholar 

  • Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile ε-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4:458–468

    Article  PubMed  CAS  Google Scholar 

  • Campbell BJ, Smith JL, Hanson TE, Klotz MG, Stein LY, Lee CK, Wu D, Robinson JM, Khouri HM, Eisen JA, Cary SC (2009) Adaptations to submarine hydrothermal environments exemplified by the genome of Nautilia profundicola. PLoS Genet 5:e1000362

    Article  PubMed  Google Scholar 

  • Casas V, Rohwer F (2007) Phage metagenomics. Methods Enzymol 421:259–268

    Article  PubMed  CAS  Google Scholar 

  • Casjens SR, Gilcrease EB, Winn-Stapley DA, Schicklmaier P, Schmieger H, Pedulla ML, Ford ME, Houtz JM, Hatfull GF, Hendrix RW (2005) The generalized transducing Salmonella bacteriophage ES18: complete genome sequence and DNA packaging strategy. J Bacteriol 187:1091–1104

    Article  PubMed  CAS  Google Scholar 

  • Christensen SK, Mikkelsen M, Pedersen K, Gerdes K (2001) RelE, a global inhibitor of translation, is activated during nutritional stress. Proc Natl Acad Sci USA 98:14328–14333

    Article  PubMed  CAS  Google Scholar 

  • Clark CG, Ng LK (2008) Sequence variability of Campylobacter temperate bacteriophages. BMC Microbiol 8:49

    Article  PubMed  Google Scholar 

  • Clokie MRJ, Mann NH (2006) Marine cyanophages and light. Environ Microbiol 8:2074–2082

    Article  PubMed  CAS  Google Scholar 

  • Clokie MRJ, Millard AD, Mann NH (2010) T4 genes in the marine ecosystem: studies of the T4-like cyanophages and their role in marine ecology. Virol J 7:291

    Article  PubMed  Google Scholar 

  • Corre E, Reysenbach AL, Prieur D (2001) ε-Proteobacterial diversity from a deep-sea hydrothermal vent on the Mid-Atlantic Ridge. FEMS Microbiol Lett 205:329–335

    PubMed  CAS  Google Scholar 

  • Delcher AL, Harmon D, Kasif S, White O, Salzberg SL (1999) Improved microbial gene identification with GLIMMER. Nucleic Acids Res 27:4636–4641

    Article  PubMed  CAS  Google Scholar 

  • Dhillon TS, Poon AP, Chan D, Clark AJ (1998) General transducing phages like Salmonella phage P22 isolated using a smooth strain of Escherichia coli as host. FEMS Microbiol Lett 161:129–133

    Article  PubMed  CAS  Google Scholar 

  • Ducret A, Van Oostveen I, Eng JK, Yates JR 3rd, Aebersold R (1998) High throughput protein characterization by automated reverse-phase chromatography/electrospray tandem mass spectrometry. Protein Sci 7:706–719

    Article  PubMed  CAS  Google Scholar 

  • Fouts DE (2006) Phage_Finder: automated identification and classification of prophage regions in complete bacterial genome sequences. Nucleic Acids Res 34:5839–5851

    Article  PubMed  CAS  Google Scholar 

  • Fouts DE, Mongodin EF, Mandrell RE, Miller WG, Rasko DA, Ravel J, Brinkac LM, DeBoy RT, Parker CT, Daugherty SC, Dodson RJ, Durkin AS, Madupu R, Sullivan SA, Shetty JU, Ayodeji MA, Shvartsbeyn A, Schatz MC, Badger JH, Fraser CM, Nelson KE (2005) Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol 3:72–85

    Article  CAS  Google Scholar 

  • Gerdes K, Christensen SK, Lobner-Olesen A (2005) Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 3:371–382

    Article  PubMed  CAS  Google Scholar 

  • Geslin C, Le Romancer M, Gaillard M, Erauso G, Prieur D (2003a) Observation of virus-like particles in high temperature enrichment cultures from deep-sea hydrothermal vents. Res Microbiol 154:303–307

    Article  PubMed  Google Scholar 

  • Geslin C, Le Romancer M, Erauso G, Gaillard M, Perrot G, Prieur D (2003b) PAV1, the first virus-like particle isolated from a hyperthermophilic euryarchaeote, “Pyrococcus abyssi”. J Bacteriol 185:3888–3894

    Article  PubMed  CAS  Google Scholar 

  • Geslin C, Gaillard M, Flament D, Rouault K, Le Romancer M, Prieur D, Erauso G (2007) Analysis of the first genome of a hyperthermophilic marine virus-like particle, PAV1, isolated from Pyrococcus abyssi. J Bacteriol 189:4510–4519

    Article  PubMed  CAS  Google Scholar 

  • Gorlas A, Koonin EV, Bienvenu N, Prieur D, Geslin C (2012) TPV1, the first virus isolated from the hyperthermophilic genus Thermococcus. Environ Microbiol 14:503–516

    Article  PubMed  CAS  Google Scholar 

  • Gross M, Marianovsky I, Glaser G (2006) MazG - a regulator of programmed cell death in Escherichia coli. Mol Microbiol 59:590–601

    Article  PubMed  CAS  Google Scholar 

  • Groth AC, Calos MP (2004) Phage integrases: biology and applications. J Mol Biol 335:667–678

    Article  PubMed  CAS  Google Scholar 

  • Hirokawa T, Boon-Chieng S, Mitaku S (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378–379

    Article  PubMed  CAS  Google Scholar 

  • Jardine PJ, Anderson DL (2006) DNA packaging in double-stranded DNA phages. In: Calendar R (ed) The bacteriophages. Oxford University Press, Oxford, pp 49–65

    Google Scholar 

  • Jeanthon C (2000) Molecular ecology of hydrothermal vent microbial communities. Antonie Van Leeuwenhoek 77:117–133

    Article  PubMed  CAS  Google Scholar 

  • Juniper SK, Bird DF, Summit M, Vong MP, Baker ET (1998) Bacterial and viral abundances in hydrothermal event plumes over northern Gorda Ridge. Deep-Sea Res Part II Top Stud Oceanogr 45:2739–2749

    Article  Google Scholar 

  • Katsura I (1987) Determination of bacteriophage λ tail length by a protein ruler. Nature 327:73–75

    Article  PubMed  CAS  Google Scholar 

  • King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (2011) Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, San Diego

    Google Scholar 

  • Kodama Y, Watanabe K (2004) Sulfuricurvum kujiense gen. nov., sp. nov., a facultatively anaerobic, chemolithoautotrophic, sulfur-oxidizing bacterium isolated from an underground crude-oil storage cavity. Int J Syst Evol Microbiol 54:2297–2300

    Article  PubMed  CAS  Google Scholar 

  • Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580

    Article  PubMed  CAS  Google Scholar 

  • Lehours P, Vale FF, Bjursell MK, Melefors O, Advani R, Glavas S, Guegueniat J, Gontier E, Lacomme S, Matos AA, Menard A, Megraud F, Engstrand L, Andersson AF (2011) Genome sequencing reveals a phage in Helicobacter pylori. mBio 2:e00239–00211

    Google Scholar 

  • Li GY, Zhang Y, Inouye M, Ikura M (2009) Inhibitory mechanism of Escherichia coli RelE-RelB toxin-antitoxin module involves a helix displacement near an mRNA interferase active site. J Biol Chem 284:14628–14636

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Zhang X (2008) Deep-sea thermophilic Geobacillus bacteriophage GVE2 transcriptional profile and proteomic characterization of virions. Appl Microbiol Biotechnol 80:697–707

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Wu S, Song Q, Zhang X, Xie L (2006) Two novel bacteriophages of thermophilic bacteria isolated from deep-sea hydrothermal fields. Curr Microbiol 53:163–166

    Article  PubMed  CAS  Google Scholar 

  • Lobocka MB, Rose DJ, Plunkett G III, Rusin M, Samojedny A, Lehnherr H, Yarmolinsky MB, Blattner FR (2004) Genome of bacteriophage P1. J Bacteriol 186:7032–7068

    Article  PubMed  CAS  Google Scholar 

  • Lu LD, Sun Q, Fan XY, Zhong Y, Yao YF, Zhao GP (2010) Mycobacterial MazG is a novel NTP pyrophosphohydrolase involved in oxidative stress response. J Biol Chem 285:28076–28085

    Article  PubMed  CAS  Google Scholar 

  • Luo CH, Chiou PY, Yang CY, Lin NT (2012) Genome, integration, and transduction of a novel temperate phage of Helicobacter pylori. J Virol 86:8781–8792

    Article  PubMed  CAS  Google Scholar 

  • Mann NH, Clokie MR, 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 187:3188–3200

    Article  PubMed  CAS  Google Scholar 

  • Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39:D225–D229

    Article  PubMed  CAS  Google Scholar 

  • Miller WG, Parker CT, Rubenfield M, Mendz GL, Wosten MM, Ussery DW, Stolz JF, Binnewies TT, Hallin PF, Wang G, Malek JA, Rogosin A, Stanker LH, Mandrell RE (2007) The complete genome sequence and analysis of the epsilonproteobacterium Arcobacter butzleri. PLoS ONE 2:e1358

    Article  PubMed  Google Scholar 

  • Miller WG, Wang GL, Binnewies TT, Parker CT (2008) The complete genome sequence and analysis of the human pathogen Campylobacter lari. Foodborne Pathog Dis 5:371–386

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa S, Takai K (2008) Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. FEMS Microbiol Ecol 65:1–14

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa S, Takaki Y (2009) Nonpathogenic Epsilonproteobacteria. Encyclopedia of Life Sciences. Wiley, New York

  • Nakagawa S, Takai K, Inagaki F, Hirayama H, Nunoura T, Horikoshi K, Sako Y (2005) Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. Environ Microbiol 7:1619–1632

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa S, Takaki Y, Shimamura S, Reysenbach AL, Takai K, Horikoshi K (2007) Deep-sea vent ε-proteobacterial genomes provide insights into emergence of pathogens. Proc Natl Acad Sci USA 104:12146–12150

    Article  PubMed  CAS  Google Scholar 

  • Ndjonka D, Bell CE (2006) Structure of a hyper-cleavable monomeric fragment of phage λ repressor containing the cleavage site region. J Mol Biol 362:479–489

    Article  PubMed  CAS  Google Scholar 

  • Nercessian O, Reysenbach AL, Prieur D, Jeanthon C (2003) Archaeal diversity associated with in situ samplers deployed on hydrothermal vents on the East Pacific Rise (13°N). Environ Microbiol 5:492–502

    Article  PubMed  Google Scholar 

  • Nunoura T, Oida H, Nakaseama M, Kosaka A, Ohkubo SB, Kikuchi T, Kazama H, Hosoi-Tanabe S, Nakamura K, Kinoshita M, Hirayama H, Inagaki F, Tsunogai U, Ishibashi J, Takai K (2010) Archaeal diversity and distribution along thermal and geochemical gradients in hydrothermal sediments at the Yonaguni Knoll IV hydrothermal field in the Southern Okinawa Trough. Appl Environ Microbiol 76:1198–1211

    Article  PubMed  CAS  Google Scholar 

  • Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304

    Article  PubMed  CAS  Google Scholar 

  • Odaert B, Saida F, Aliprandi P, Durand S, Crechet JB, Guerois R, Laalami S, Uzan M, Bontems F (2007) Structural and functional studies of RegB, a new member of a family of sequence-specific ribonucleases involved in mRNA inactivation on the ribosome. J Biol Chem 282:2019–2028

    Article  PubMed  CAS  Google Scholar 

  • Ortmann AC, Suttle CA (2005) High abundances of viruses in a deep-sea hydrothermal vent system indicates viral mediated microbial mortality. Deep-Sea Res Part I Oceanogr Res Pap 52:1515–1527

    Article  Google Scholar 

  • Pabo CO, Sauer RT, Sturtevant JM, Ptashne M (1979) The lambda repressor contains two domains. Proc Natl Acad Sci USA 76:1608–1612

    Article  PubMed  CAS  Google Scholar 

  • Parker CT, Quinones B, Miller WG, Horn ST, Mandrell RE (2006) Comparative genomic analysis of Campylobacter jejuni strains reveals diversity due to genomic elements similar to those present in C. jejuni strain RM1221. J Clin Microbiol 44:4125–4135

    Article  PubMed  CAS  Google Scholar 

  • Pedersen K, Zavialov AV, Pavlov MY, Elf J, Gerdes K, Ehrenberg M (2003) The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell 112:131–140

    Article  PubMed  CAS  Google Scholar 

  • Pei J, Grishin NV (2007) PROMALS: towards accurate multiple sequence alignments of distantly related proteins. Bioinformatics 23:802–808

    Article  PubMed  CAS  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

    Article  PubMed  CAS  Google Scholar 

  • Piazzolla D, Cali S, Spoldi E, Forti F, Sala C, Magnoni F, Deho G, Ghisotti D (2006) Expression of phage P4 integrase is regulated negatively by both Int and Vis. J Gen Virol 87:2423–2431

    Article  PubMed  CAS  Google Scholar 

  • Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD (2012) The Pfam protein families database. Nucleic Acids Res 40:D290–D301

    Article  PubMed  CAS  Google Scholar 

  • Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R (2005) InterProScan: protein domains identifier. Nucleic Acids Res 33:W116–W120

    Article  PubMed  CAS  Google Scholar 

  • Rao VB, Feiss M (2008) The bacteriophage DNA packaging motor. Annu Rev Genet 42:647–681

    Article  PubMed  CAS  Google Scholar 

  • Rohwer F, Edwards R (2002) The Phage Proteomic Tree: a genome-based taxonomy for phage. J Bacteriol 184:4529–4535

    Article  PubMed  CAS  Google Scholar 

  • Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:W686–W689

    Article  PubMed  CAS  Google Scholar 

  • Schrenk MO, Kelley DS, Delaney JR, Baross JA (2003) Incidence and diversity of microorganisms within the walls of an active deep-sea sulfide chimney. Appl Environ Microbiol 69:3580–3592

    Article  PubMed  CAS  Google Scholar 

  • Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW (2005) Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3:e144

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sullivan MB, Huang KH, Ignacio-Espinoza JC, Berlin AM, Kelly L, Weigele PR, DeFrancesco AS, Kern SE, Thompson LR, Young S, Yandava C, Fu R, Krastins B, Chase M, Sarracino D, Osburne MS, Henn MR, Chisholm SW (2010) Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ Microbiol 12:3035–3056

    Article  PubMed  CAS  Google Scholar 

  • Takai K, Inagaki F, Nakagawa S, Hirayama H, Nunoura T, Sako Y, Nealson KH, Horikoshi K (2003) Isolation and phylogenetic diversity of members of previously uncultivated ε-Proteobacteria in deep-sea hydrothermal fields. FEMS Microbiol Lett 218:167–174

    PubMed  CAS  Google Scholar 

  • Takai K, Nakagawa S, Reysenbach A, Hoek J (2006) Microbial ecology of mid-ocean ridges and back-arc basins. In: Christie DM, Fisher CR, Lee SM, Givens S (eds) Back-arc spreading systems: geological, biological, chemical, and physical interactions geophysical monograph series. American Geophysical Union, Washington, DC, pp 185–213

  • Takashima Y, Yoshida T, Yoshida M, Shirai Y, Tomaru Y, Takao Y, Hiroishi S, Nagasaki K (2007) Development and application of quantitative detection of cyanophages phylogenetically related to cyanophage Ma-LMM01 infecting Microcystis aeruginosa in fresh water. Microbes Environ 22:207–213

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Vander Byl C, Kropinski AM (2000) Sequence of the genome of Salmonella bacteriophage P22. J Bacteriol 182:6472–6481

    Article  PubMed  CAS  Google Scholar 

  • Waldor MK, Mekalanos JJ (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910–1914

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Zhang X (2008) Identification and characterization of a novel thymidylate synthase from deep-sea thermophilic bacteriophage Geobacillus virus E2. Virus Genes 37:218–224

    Article  PubMed  Google Scholar 

  • Wang Y, Zhang X (2010) Genome analysis of deep-sea thermophilic phage D6E. Appl Environ Microbiol 76:7861–7866

    Article  PubMed  CAS  Google Scholar 

  • Washburn MP, Wolters D, Yates JR 3rd (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19:242–247

    Article  PubMed  CAS  Google Scholar 

  • Wei D, Zhang X (2008) Identification and characterization of a single-stranded DNA-binding protein from thermophilic bacteriophage GVE2. Virus Genes 36:273–278

    Article  PubMed  CAS  Google Scholar 

  • Wei D, Zhang X (2010) Proteomic analysis of interactions between a deep-sea thermophilic bacteriophage and its host at high temperature. J Virol 84:2365–2373

    Article  PubMed  CAS  Google Scholar 

  • Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wommack KE, Williamson SJ, Sundbergh A, Helton RR, Glazer BT, Portune K, Cary SC (2004) An instrument for collecting discrete large-volume water samples suitable for ecological studies of microorganisms. Deep-Sea Res Part I Oceanogr Res Pap 51:1781–1792

    Google Scholar 

  • Ye T, Zhang X (2008) Characterization of a lysin from deep-sea thermophilic bacteriophage GVE2. Appl Microbiol Biotechnol 78:635–641

    Article  PubMed  CAS  Google Scholar 

  • Yoshida T, Takashima Y, Tomaru Y, Shirai Y, Takao Y, Hiroishi S, Nagasaki K (2006) Isolation and characterization of a cyanophage infecting the toxic cyanobacterium Microcystis aeruginosa. Appl Environ Microbiol 72:1239–1247

    Article  PubMed  CAS  Google Scholar 

  • Yoshida-Takashima Y, Nunoura T, Kazama H, Noguchi T, Inoue K, Akashi H, Yamanaka T, Toki T, Yamamoto M, Furushima Y, Ueno Y, Yamamoto H, Takai K (2012) Spatial distribution of viruses associated with planktonic and attached microbial communities in hydrothermal environments. Appl Environ Microbiol 78:1311–1320

    Article  PubMed  CAS  Google Scholar 

  • Young R (2002) Bacteriophage holins: deadly diversity. J Mol Microbiol Biotechnol 4:21–36

    PubMed  CAS  Google Scholar 

  • Young R, Wang IN, Roof WD (2000) Phages will out: strategies of host cell lysis. Trends Microbiol 8:120–128

    Article  PubMed  CAS  Google Scholar 

  • Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39:W347–W352

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank K. Uematsu for technical help with TEM. This study was partially supported by a Grant-in-Aid for Young Scientists (B) (No. 22770092) from the Japan Society for the Promotion of Science (JSPS).

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  1. Subsurface Geobiology Advanced Research (SUGAR) Team, Extremobiosphere Research Program, Institute of Biogeosciences, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, Kanagawa, 237-0061, Japan

    Yukari Yoshida-Takashima, Yoshihiro Takaki, Shigeru Shimamura, Takuro Nunoura & Ken Takai

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  1. Yukari Yoshida-Takashima
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  2. Yoshihiro Takaki
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Correspondence to Yukari Yoshida-Takashima.

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Communicated by L. Huang.

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Yoshida-Takashima, Y., Takaki, Y., Shimamura, S. et al. Genome sequence of a novel deep-sea vent epsilonproteobacterial phage provides new insight into the co-evolution of Epsilonproteobacteria and their phages. Extremophiles 17, 405–419 (2013). https://doi.org/10.1007/s00792-013-0529-5

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