Detection of Bacteriophages: Sequence-Based Systems

  • Siân V. Owen
  • Blanca M. Perez-Sepulveda
  • Evelien M. AdriaenssensEmail author
Living reference work entry


The invention of sequencing technologies has fundamentally changed molecular biology, including the way we look at bacteriophages. In addition to investigating bacteriophage plaques, electron micrographs, or the phenotypes of different mutants, we are now able to explore the entire genetic potential encoded in their genomes. As of July 2018, over 6,000 complete phage genome sequences were published in public databases, with over 28,000 partial sequences available.

In this chapter, we give an overview of the latest technologies that can be used to determine phage genome sequences, ranging from short-read platforms which generally give multiple gigabases of sequence data to long-read technologies which have the potential to sequence a bacteriophage genome in one single read. We then look at applications of sequencing technologies in detecting bacteriophages, from a single gene, over entire genomes, to the community level.


  1. Abedon ST (2017) Information phage therapy research should report. Pharmaceuticals 10:1–17. Scholar
  2. Ackermann H-W (2011) Bacteriophage taxonomy. Microbiol Aust 32:90–94Google Scholar
  3. Adams RLP, Burdon RH (1985) The function of DNA methylation in bacteria and phage. In: Molecular biology of DNA methylation. Springer, New York, pp 73–87CrossRefGoogle Scholar
  4. Adriaenssens E, Brister JR (2017) How to name and classify your phage: an informal guide. Viruses 9:70. Scholar
  5. Adriaenssens EM, Cowan DA (2014) Using signature genes as tools to assess environmental viral ecology and diversity. Appl Environ Microbiol 80:4470–4480. Scholar
  6. Adriaenssens EM, Ackermann H-W, Anany H et al (2012) A suggested new bacteriophage genus: “Viunalikevirus”. Arch Virol 157:2035–2046. Scholar
  7. Adriaenssens EM, Kramer R, Van Goethem MW et al (2017) Environmental drivers of viral community composition in Antarctic soils identified by viromics. Microbiome 5:83. Scholar
  8. Adriaenssens EM, Wittmann J, Kuhn JH et al (2018) Taxonomy of prokaryotic viruses: 2017 update from the ICTV Bacterial and Archaeal Viruses Subcommittee. Arch Virol 163:1125–1129. Scholar
  9. Aguirre de Cárcer D, López-Bueno A, Pearce DA, Alcamí A (2015) Biodiversity and distribution of polar freshwater DNA viruses. Sci Adv 1:e1400127. Scholar
  10. Akhter S, Aziz RK, Edwards RA (2012) PhiSpy: a novel algorithm for finding prophages in bacterial genomes that combines similarity- and composition-based strategies. Nucleic Acids Res 40:e126. Scholar
  11. Alavidze Z, Aminov R, Betts A et al (2016) Silk route to the acceptance and re-implementation of bacteriophage therapy. Biotechnol J 11:595–600. Scholar
  12. Arndt D, Grant JR, Marcu A et al (2016) PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44:W16–W21. Scholar
  13. Baker AC, Goddard VJ, Davy J et al (2006) Identification of a diagnostic marker to detect freshwater cyanophages of filamentous cyanobacteria. Appl Environ Microbiol 72:5713–5719. Scholar
  14. Barrett T, Clark K, Gevorgyan R et al (2012) BioProject and BioSample databases at NCBI: facilitating capture and organization of metadata. Nucleic Acids Res 40:57–63. Scholar
  15. Baym M, Kryazhimskiy S, Lieberman TD et al (2015) Inexpensive multiplexed library preparation for megabase-sized genomes. PLoS One 10:e0128036. Scholar
  16. Bellas CM, Anesio AM (2013) High diversity and potential origins of T4-type bacteriophages on the surface of Arctic glaciers. Extremophiles 17:861–870. Scholar
  17. Benson DA, Cavanaugh M, Clark K et al (2013) GenBank. Nucleic Acids Res 41:36–42. Scholar
  18. Bolduc B, Shaughnessy DP, Wolf YI et al (2012) Identification of novel positive-strand RNA viruses by metagenomic analysis of archaea-dominated Yellowstone hot springs. J Virol 86:5562–5573. Scholar
  19. Bose M, Barber RD (2006) Prophage Finder: a prophage loci prediction tool for prokaryotic genome sequences. In Silico Biol 6:223–227PubMedGoogle Scholar
  20. Bossi L, Fuentes JA, Mora G, Figueroa-Bossi N (2003) Prophage contribution to bacterial population dynamics. J Bacteriol 185:6467–6471CrossRefGoogle Scholar
  21. Breitbart M, Salamon P, Andresen B et al (2002) Genomic analysis of uncultured marine viral communities. Proc Natl Acad Sci U S A 99:14250–14255. Scholar
  22. Breitbart M, Hewson I, Felts B et al (2003) Metagenomic analyses of an uncultured viral community from human feces. J Bacteriol 185:6220–6223. Scholar
  23. Breitbart M, Miyake JH, Rohwer F (2004) Global distribution of nearly identical phage-encoded DNA sequences. FEMS Microbiol Lett 236:249–256. Scholar
  24. Brister JR, Ako-Adjei D, Bao Y, Blinkova O (2015) NCBI viral genomes resource. Nucleic Acids Res 43:D571–D577. Scholar
  25. Brum JR, Ignacio-Espinoza JC, Roux S et al (2015) Patterns and ecological drivers of ocean viral communities. Science (80-) 348:1261498. Scholar
  26. Brüssow H, Canchaya C, Hardt WD (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560–602. Scholar
  27. Butina TV, Belykh OI, Maksimenko SY, Belikov SI (2010) Phylogenetic diversity of T4-like bacteriophages in Lake Baikal, East Siberia. FEMS Microbiol Lett 309:122–129. Scholar
  28. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. Scholar
  29. Casjens S (2003) Prophages and bacterial genomics: what have we learned so far? Mol Microbiol 49:277–300CrossRefGoogle Scholar
  30. Castro-Wallace SL, Chiu CY, John KK et al (2017) Nanopore DNA sequencing and genome assembly on the International Space Station. Sci Rep 7:18022. Scholar
  31. Chan Y-WW, Millard AD, Wheatley PJ et al (2015) Genomic and proteomic characterization of two novel siphovirus infecting the sedentary facultative epibiont cyanobacterium Acaryochloris marina. Environ Microbiol 17:4239–4252. Scholar
  32. Chen F, Wang K, Huang S et al (2009) Diverse and dynamic populations of cyanobacterial podoviruses in the Chesapeake Bay unveiled through DNA polymerase gene sequences. Environ Microbiol 11:2884–2892. Scholar
  33. Chow C-ET, Fuhrman JA (2012) Seasonality and monthly dynamics of marine myovirus communities. Environ Microbiol 14:2171–2183. Scholar
  34. 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. Scholar
  35. Comeau AM, Krisch HM (2008) The capsid of the T4 phage superfamily: the evolution, diversity, and structure of some of the most prevalent proteins in the biosphere. Mol Biol Evol 25:1321–1332. Scholar
  36. Cowley LA, Beckett SJ, Chase-Topping M et al (2015) Analysis of whole genome sequencing for the Escherichia coli O157:H7 typing phages. BMC Genomics 16:271. Scholar
  37. Culley AI, Steward GF (2007) New genera of RNA viruses in subtropical seawater, inferred from polymerase gene sequences. Appl Environ Microbiol 73:5937–5344. Scholar
  38. Culley AI, Lang AS, Suttle CA (2003) High diversity of unknown picorna-like viruses in the sea. Nature 424:1054–1057. Scholar
  39. Dekel-Bird NP, Avrani S, Sabehi G et al (2013) Diversity and evolutionary relationships of T7-like podoviruses infecting marine cyanobacteria. Environ Microbiol 15:1476–1491. Scholar
  40. Dunn JJ, Studier FW, Gottesman M (1983) Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements. J Mol Biol 166:477–535. Scholar
  41. Dutilh BE, Schmieder R, Nulton J et al (2012) Reference-independent comparative metagenomics using cross-assembly: CrAss. Bioinformatics 28:3225–3231. Scholar
  42. Dutilh BE, Cassman N, McNair K et al (2014) A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat Commun 5:4498. Scholar
  43. Dwivedi B, Schmieder R, Goldsmith DB et al (2012) PhiSiGns: an online tool to identify signature genes in phages and design PCR primers for examining phage diversity. BMC Bioinform 13:37. Scholar
  44. Fierer N, Breitbart M, Nulton J et al (2007) Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, archaea, fungi, and viruses in soil. Appl Environ Microbiol 73:7059–7066. Scholar
  45. Filée J, Tétart F, Suttle CA, Krisch HM (2005) Marine T4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere. Proc Natl Acad Sci U S A 102:12471–12476. Scholar
  46. Fleischmann R, Adams M, White O et al (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science (80-) 269:496–512. Scholar
  47. Fortier L-C, Sekulovic O (2013) Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4:354–365. Scholar
  48. Fouts DE (2006) Phage_Finder: automated identification and classification of prophage regions in complete bacterial genome sequences. Nucleic Acids Res 34:5839–5851. Scholar
  49. Friedman SD, Genthner FJ, Gentry J et al (2009) Gene mapping and phylogenetic analysis of the complete genome from 30 single-stranded RNA male-specific coliphages (family Leviviridae). J Virol 83:11233–11243. Scholar
  50. Fujii T, Nakayama N, Nishida M et al (2008) Novel capsid genes (g23) of T4-type bacteriophages in a Japanese paddy field. Soil Biol Biochem 40:1049–1058. Scholar
  51. Fuller NJ, Wilson WH, Joint IR, Mann NH (1998) 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 64:2051–2060PubMedPubMedCentralGoogle Scholar
  52. Garneau JR, Depardieu F, Fortier L-C et al (2017) PhageTerm: a tool for fast and accurate determination of phage termini and packaging mechanism using next-generation sequencing data. Sci Rep 7:8292. Scholar
  53. 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. Scholar
  54. Goodwin S, McPherson JD, McCombie WR (2016) Coming of age: ten years of next-generation sequencing technologies. Nat Rev Genet 17:333–351. Scholar
  55. Grazziotin AL, Koonin EV, Kristensen DM (2017) Prokaryotic Virus Orthologous Groups (pVOGs): a resource for comparative genomics and protein family annotation. Nucleic Acids Res 45:D491–D498. Scholar
  56. Hall RJ, Wang J, Todd AK et al (2014) Evaluation of rapid and simple techniques for the enrichment of viruses prior to metagenomic virus discovery. J Virol Methods 195:194–204. Scholar
  57. Hannigan GD, Meisel JS, Tyldsley AS et al (2015) The human skin double-stranded DNA virome: topographical and temporal diversity, genetic enrichment, and dynamic associations with the host microbiome. MBio 6:e01578–e01515. Scholar
  58. Hatfull GF (2015) Dark matter of the biosphere: the amazing world of bacteriophage diversity. J Virol 89:8107–8110. Scholar
  59. Hatfull GF, Hendrix RW (2011) Bacteriophages and their genomes. Curr Opin Virol 1:298–303. Scholar
  60. Henn MR, Sullivan MB, Stange-Thomann N et al (2010) Analysis of high-throughput sequencing and annotation strategies for phage genomes. PLoS One 5:e9083. Scholar
  61. Hertveldt K, Lavigne R, Pleteneva E et al (2005) Genome comparison of Pseudomonas aeruginosa large phages. J Mol Biol 354:536–545. Scholar
  62. Hopkins M, Kailasan S, Cohen A et al (2014) Diversity of environmental single-stranded DNA phages revealed by PCR amplification of the partial major capsid protein. ISME J 8:2093–2103. Scholar
  63. Huang S, Wilhelm SW, Jiao N, Chen F (2010) Ubiquitous cyanobacterial podoviruses in the global oceans unveiled through viral DNA polymerase gene sequences. ISME J 4:1243–1251. Scholar
  64. Ip CLC, Loose M, Tyson JR et al (2015) MinION analysis and reference consortium: phase 1 data release and analysis. F1000Research 4:1075. Scholar
  65. Johnson M, Zaretskaya I, Raytselis Y et al (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:W5–W9. Scholar
  66. Karsch-Mizrachi I, Nakamura Y, Cochrane G (2012) The international nucleotide sequence database collaboration. Nucleic Acids Res 40:D33–D37. Scholar
  67. Keller MW, Rambo-Martin BL, Wilson MM, et al (2018) Direct RNA sequencing of the complete Influenza A virus genome. bioRxiv.
  68. Klumpp J, Lavigne R, Loessner MJ, Ackermann H-W (2010) The SPO1-related bacteriophages. Arch Virol 155:1547–1561. Scholar
  69. Klumpp J, Fouts DE, Sozhamannan S (2012) Next generation sequencing technologies and the changing landscape of phage genomics. Bacteriophage 2:190–199. Scholar
  70. Klumpp J, Schmuki M, Sozhamannan S et al (2014) The odd one out: Bacillus ACT bacteriophage CP-51 exhibits unusual properties compared to related Spounavirinae W.Ph. and Bastille. Virology 462:299–308. Scholar
  71. Kot W, Vogensen FK, Sørensen SJ, Hansen LH (2014) DPS – a rapid method for genome sequencing of DNA-containing bacteriophages directly from a single plaque. J Virol Methods 196:152–156. Scholar
  72. Kristensen DM, Waller AS, Yamada T et al (2013) Orthologous gene clusters and taxon signature genes for viruses of prokaryotes. J Bacteriol 195:941–950. Scholar
  73. Krupovic M, Prangishvili D, Hendrix RW, Bamford DH (2011) Genomics of bacterial and archaeal viruses: dynamics within the prokaryotic virosphere. Microbiol Mol Biol Rev 75:610–635. Scholar
  74. Labonté JM, Suttle CA (2013) Metagenomic and whole-genome analysis reveals new lineages of gokushoviruses and biogeographic separation in the sea. Front Microbiol 4:404. Scholar
  75. Labonté JM, Reid KE, Suttle CA (2009) Phylogenetic analysis indicates evolutionary diversity and environmental segregation of marine podovirus DNA polymerase gene sequences. Appl Environ Microbiol 75:3634–3640. Scholar
  76. Laver T, Harrison J, O’Neill PA et al (2015) Assessing the performance of the Oxford Nanopore Technologies MinION. Biomol Detect Quantif 3:1–8. Scholar
  77. Lee Y-J, Dai N, Walsh SE et al (2018) Identification and biosynthesis of thymidine hypermodifications in the genomic DNA of widespread bacterial viruses. Proc Natl Acad Sci.
  78. Leinonen R, Akhtar R, Birney E et al (2011a) The European nucleotide archive. Nucleic Acids Res 39:31–34. Scholar
  79. Leinonen R, Sugawara H, Shumway M (2011b) The sequence read archive. Nucleic Acids Res 39:2010–2012. Scholar
  80. Lima-Mendez G, Van Helden J, Toussaint A, Leplae R (2008) Prophinder: a computational tool for prophage prediction in prokaryotic genomes. Bioinformatics 24:863–865. Scholar
  81. Loman NJ, Misra RV, Dallman TJ et al (2012) Performance comparison of benchtop high-throughput sequencing platforms. Nat Biotechnol 30:434–439. Scholar
  82. López-Bueno A, Tamames J, Velázquez D et al (2009) High diversity of the viral community from an Antarctic lake. Science 326:858–861. Scholar
  83. Manrique P, Bolduc B, Walk ST et al (2016) Healthy human gut phageome. Proc Natl Acad Sci 113:10400–10405. Scholar
  84. Marine R, Polson SW, Ravel J et al (2011) Evaluation of a transposase protocol for rapid generation of shotgun high-throughput sequencing libraries from nanogram quantities of DNA. Appl Environ Microbiol 77:8071–8079. Scholar
  85. Marston MF, Amrich CG (2009) Recombination and microdiversity in coastal marine cyanophages. Environ Microbiol 11:2893–2903. Scholar
  86. McCallin S, Alam Sarker S, Barretto C et al (2013) Safety analysis of a Russian phage cocktail: from MetaGenomic analysis to oral application in healthy human subjects. Virology 443:187–196. Scholar
  87. Millard A, Clokie MRJ, Shub DA, Mann NH (2004) Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc Natl Acad Sci U S A 101:11007–11012. Scholar
  88. Millard AD, Zwirglmaier K, Downey MJ et al (2009) Comparative genomics of marine cyanomyoviruses reveals the widespread occurrence of Synechococcus host genes localized to a hyperplastic region: implications for mechanisms of cyanophage evolution. Environ Microbiol 11:2370–2387. Scholar
  89. Millard AD, Gierga G, Clokie MRJ et al (2010) An antisense RNA in a lytic cyanophage links psbA to a gene encoding a homing endonuclease. ISME J 4:1121–1135. Scholar
  90. Minot S, Sinha R, Chen J et al (2011) The human gut virome: inter-individual variation and dynamic response to diet. Genome Res 21:1616–1625. Scholar
  91. Mizuno CM, Rodriguez-Valera F, Kimes NE, Ghai R (2013) Expanding the marine virosphere using metagenomics. PLoS Genet 9:e1003987. Scholar
  92. Moustafa A, Xie C, Kirkness E et al (2017) The blood DNA virome in 8,000 humans. PLoS Pathog 13:e1006292. Scholar
  93. Owen SV, Wenner N, Canals R et al (2017) Characterization of the prophage repertoire of African Salmonella Typhimurium ST313 reveals high levels of spontaneous induction of novel phage BTP1. Front Microbiol 8:235. Scholar
  94. Perez Sepulveda B, Redgwell T, Rihtman B et al (2016) Marine phage genomics: the tip of the iceberg. FEMS Microbiol Lett 363:fnw158. Scholar
  95. Phillippy AM (2017) New advances in sequence assembly. Genome Res 27:xi–xiii. Scholar
  96. Pride DT, Salzman J, Haynes M et al (2012) Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. ISME J 6:915–926. Scholar
  97. Puxty RJ, Perez-Sepulveda B, Rihtman B et al (2015) Spontaneous deletion of an “ORFanage” region facilitates host adaptation in a “photosynthetic” cyanophage. PLoS One 10:e0132642. Scholar
  98. Rand AC, Jain M, Eizenga JM et al (2017) Mapping DNA methylation with high-throughput nanopore sequencing. Nat Methods 14:411–413. Scholar
  99. Raya R, Hébert EM (2009) Isolation of phage via induction of lysogens. In: Clokie MR, Kropinski AM (eds) Bacteriophages: methods and protocols. Humana Press, New York, pp 23–32CrossRefGoogle Scholar
  100. Reyes A, Haynes M, Hanson N et al (2010) Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466:334–338. Scholar
  101. Reyes A, Semenkovich NP, Whiteson K et al (2012) Going viral: next-generation sequencing applied to phage populations in the human gut. Nat Rev Microbiol 10:607–617. Scholar
  102. Reyes A, Blanton LV, Cao S et al (2015) Gut DNA viromes of Malawian twins discordant for severe acute malnutrition. Proc Natl Acad Sci 112:201514285. Scholar
  103. Rhoads A, Au KF (2015) PacBio sequencing and its applications. Genomics Proteomics Bioinform 13:278–289. Scholar
  104. Rihtman B, Meaden S, Clokie MRJ et al (2016) Assessing Illumina technology for the high-throughput sequencing of bacteriophage genomes. PeerJ 4:e2055. Scholar
  105. Rohwer F, Edwards R (2002) The Phage Proteomic Tree: a genome-based taxonomy for phage. J Bacteriol 184:4529–4535. Scholar
  106. Roux S, Enault F, Robin A et al (2012) Assessing the diversity and specificity of two freshwater viral communities through metagenomics. PLoS One 7:e33641. Scholar
  107. Roux S, Tournayre J, Mahul A et al (2014) Metavir 2: new tools for viral metagenome comparison and assembled virome analysis. BMC Bioinform 15:76. Scholar
  108. Roux S, Enault F, Hurwitz BL, Sullivan MB (2015) VirSorter: mining viral signal from microbial genomic data. PeerJ 3:e985. Scholar
  109. Roux S, Brum JR, Dutilh BE et al (2016) Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537:689–693. Scholar
  110. Sabehi G, Shaulov L, Silver DH et al (2012) A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans. Proc Natl Acad Sci U S A 109:2037–2042. Scholar
  111. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci 74:5463–5467. Scholar
  112. Sanger F, Coulson AR, Hong GF et al (1982) Nucleotide sequence of bacteriophage lambda DNA. J Mol Biol 162:729–773CrossRefGoogle Scholar
  113. Santiago-Rodriguez TM, Ly M, Bonilla N, Pride DT (2015) The human urine virome in association with urinary tract infections. Front Microbiol 6:1–12. Scholar
  114. Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. Scholar
  115. Short CM, Suttle CA (2005) Nearly identical bacteriophage structural gene sequences are widely distributed in both marine and freshwater environments. Appl Environ Microbiol 71:480–486. Scholar
  116. Skvortsov T, de Leeuwe C, Quinn JP et al (2016) Metagenomic characterisation of the viral community of Lough Neagh, the largest freshwater lake in Ireland. PLoS One 11:e0150361. Scholar
  117. Sullivan MB (2015) Viromes, not gene markers, for studying double-stranded DNA virus communities. J Virol 89:2459–2461. Scholar
  118. Sullivan MB, Lindell D, Lee JA et al (2006) Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol 4:e234. Scholar
  119. Sullivan MB, Krastins B, Hughes JL et al (2009) The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial “mobilome”. Environ Microbiol 11:2935–2951. Scholar
  120. Sullivan MB, Weitz JS, Wilhelm S (2017) Viral ecology comes of age. Environ Microbiol Rep 9:33–35. Scholar
  121. Székely AJ, Breitbart M (2016) Single-stranded DNA phages: from early molecular biology tools to recent revolutions in environmental microbiology. FEMS Microbiol Lett 363:1–9. Scholar
  122. Thompson LR, Zeng Q, Kelly L et al (2011) Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc Natl Acad Sci 108:E757–E764. Scholar
  123. Tseng E, Underwood JG (2013) Full length cDNA sequencing on the PacBio® RS. J Biomol Tech 24:S45PubMedCentralGoogle Scholar
  124. Utter B, Deutsch DR, Schuch R et al (2014) Beyond the chromosome: the prevalence of unique extra-chromosomal bacteriophages with integrated virulence genes in pathogenic Staphylococcus aureus. PLoS One 9:e100502. Scholar
  125. Vega Thurber R, Haynes M, Breitbart M et al (2009) Laboratory procedures to generate viral metagenomes. Nat Protoc 4:470–483. Scholar
  126. Wang K, Chen F (2008) Prevalence of highly host-specific cyanophages in the estuarine environment. Environ Microbiol 10:300–312. Scholar
  127. Wang G, Hayashi M, Saito M et al (2009a) Survey of major capsid genes (g23) of T4-type bacteriophages in Japanese paddy field soils. Soil Biol Biochem 41:13–20. Scholar
  128. Wang G, Murase J, Taki K et al (2009b) Changes in major capsid genes (g23) of T4-type bacteriophages with soil depth in two Japanese rice fields. Biol Fertil Soils 45:521–529. Scholar
  129. Zablocki O, Van Zyl L, Adriaenssens EM et al (2014) High-level diversity of tailed phages, eukaryote-associated viruses and virophage-like elements in the metaviromes of Antarctic soils. Appl Environ Microbiol 80:6888–6897. Scholar
  130. Zablocki O, Adriaenssens EM, Frossard A et al (2017) Metaviromes of extracellular soil viruses along a Namib Desert aridity gradient. Genome Announc 5:e01470–e01416. Scholar
  131. Zeidner G, Preston CM, Delong EF et al (2003) Molecular diversity among marine picophytoplankton as revealed by psbA analyses. Environ Microbiol 5:212–216. Scholar
  132. Zhong Y, Chen F, Wilhelm SW et al (2002) Phylogenetic diversity of marine cyanophage isolates and natural virus communities as revealed by sequences of viral capsid assembly protein gene g20. Appl Environ Microbiol 68:1576–1584. Scholar
  133. Zhong X, Guidoni B, Jacas L, Jacquet S (2015) Structure and diversity of ssDNA Microviridae viruses in two peri-alpine lakes (Annecy and Bourget, France). Res Microbiol 166:644–654. Scholar
  134. Zhou Y, Liang Y, Lynch KH et al (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39:W347–W352. Scholar
  135. Zschach H, Joensen KG, Lindhard B et al (2015) What can we learn from a metagenomic analysis of a Georgian bacteriophage cocktail? Viruses 7:6570–6589. Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Siân V. Owen
    • 1
    • 2
  • Blanca M. Perez-Sepulveda
    • 1
  • Evelien M. Adriaenssens
    • 1
    Email author
  1. 1.Microbiology Research Group, Institute of Integrative BiologyUniversity of LiverpoolLiverpoolUK
  2. 2.Department of Biomedical Informatics and Laboratory of Systems PharmacologyHarvard Medical SchoolBostonUSA

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