1932

Abstract

Two decades of metagenomic analyses have revealed that in many environments, small (∼5 kb), single-stranded DNA phages of the family dominate the virome. Although the emblematic microvirus X174 is ubiquitous in the laboratory, most other microviruses, particularly those of the gokushovirus and amoyvirus lineages, have proven to be much more elusive. This puzzling lack of representative isolates has hindered insights into microviral biology. Furthermore, the idiosyncratic size and nature of their genomes have resulted in considerable misjudgments of their actual abundance in nature. Fortunately, recent successes in microvirus isolation and improved metagenomic methodologies can now provide us with more accurate appraisals of their abundance, their hosts, and their interactions. The emerging picture is that X174 and its relatives are rather rare and atypical microviruses, and that a tremendous diversity of other microviruses is ready for exploration.

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2023-09-29
2024-06-18
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Literature Cited

  1. 1.
    Sinsheimer RL. 1959. A single-stranded deoxyribonucleic acid from bacteriophage ϕX174. J. Mol. Biol. 1:43–53
    [Google Scholar]
  2. 2.
    Sertic V, Boulgakov N. 1935. Classification et identification des typhi-phages. CR Soc. Biol. Paris 119:1270–72
    [Google Scholar]
  3. 3.
    Denhardt DT. 1975. The single-stranded DNA phages. CRC Crit. Rev. Microbiol. 4:161–223
    [Google Scholar]
  4. 4.
    Sinsheimer RL. 1968. Bacteriophage ϕx174 and related viruses. Prog. Nucleic Acid Res. Mol. Biol. 8:115–16
    [Google Scholar]
  5. 5.
    Calendar R 1988. The Bacteriophages. New York: Plenum
    [Google Scholar]
  6. 6.
    Breitbart M, Fane BA. 2021. Microviridae. eLS 2:1–14
    [Google Scholar]
  7. 7.
    Wichman HA, Brown CJ. 2010. Experimental evolution of viruses: Microviridae as a model system. Philos. Trans. R. Soc. B 365:2495–501
    [Google Scholar]
  8. 8.
    Sanger F, Air GM, Barrell BG, Brown NL, Coulson AR et al. 1977. Nucleotide sequence of bacteriophage ϕX174 DNA. Nature 265:687–95
    [Google Scholar]
  9. 9.
    Smith HO, Hutchison CA III, Pfannkoch C, Venter JC 2003. Generating a synthetic genome by whole genome assembly: ϕX174 bacteriophage from synthetic oligonucleotides. PNAS 100:15440–45
    [Google Scholar]
  10. 10.
    Goulian M, Kornberg A, Sinsheimer RL. 1967. Enzymatic synthesis of DNA, XXIV. Synthesis of infectious phage ϕX174 DNA. PNAS 58:2321–28
    [Google Scholar]
  11. 11.
    Kirchberger PC, Martinez ZA, Ochman H. 2022. Organizing the global diversity of microviruses. mBio 13:3e00588-22
    [Google Scholar]
  12. 12.
    Dutilh BE, Varsani A, Tong Y, Simmonds P, Sabanadzovic S et al. 2021. Perspective on taxonomic classification of uncultivated viruses. Curr. Opin. Virol. 51:207–15
    [Google Scholar]
  13. 13.
    Simmonds P, Adams MJ, Benko M, Breitbart M, Brister JR et al. 2017. Consensus statement: virus taxonomy in the age of metagenomics. Nat. Rev. Microbiol. 15:161–68
    [Google Scholar]
  14. 14.
    Luque A, Benler S, Lee DY, Brown C, White S. 2020. The missing tailed phages: prediction of small capsid candidates. Microorganisms 8:1944
    [Google Scholar]
  15. 15.
    Hua J, Huet A, Lopez CA, Toropova K, Pope WH et al. 2017. Capsids and genomes of jumbo-sized bacteriophages reveal the evolutionary reach of the HK97 fold. mBio 8:e01579-17
    [Google Scholar]
  16. 16.
    Lee H, Baxter AJ, Bator CM, Fane BA, Hafenstein SL. 2022. Cryo-EM structure of gokushovirus ϕEC6098 reveals a novel capsid architecture for a single-scaffolding protein, microvirus assembly system. J. Virol. 96:e00990–22
    [Google Scholar]
  17. 17.
    Zhan Y, Chen F. 2018. The smallest ssDNA phage infecting a marine bacterium. Environ. Microbiol. 21:1916–28
    [Google Scholar]
  18. 18.
    Cook R, Brown N, Redgwell T, Rihtman B, Barnes M et al. 2021. Infrastructure for a PHAge REference database: identification of large-scale biases in the current collection of cultured phage genomes. Phage 2:214–23
    [Google Scholar]
  19. 19.
    Zuo T, Sun Y, Wan Y, Yeoh YK, Zhang F et al. 2020. Human-gut-DNA virome variations across geography, ethnicity, and urbanization. Cell Host Microbe 28:741–51
    [Google Scholar]
  20. 20.
    Chantranupong L, Heineman RH. 2012. A common, non-optimal phenotypic endpoint in experimental adaptations of bacteriophage lysis time. BMC Evol. Biol. 12:37
    [Google Scholar]
  21. 21.
    Olo Ndela E, Roux S, Henke C, Sczyrba A, Ngando T et al. 2022. Reekeekee- and roodoodooviruses, two different Microviridae clades constituted by the smallest DNA phages. Virus Evol. 9:veac123
    [Google Scholar]
  22. 22.
    Zhang L, Li Z, Bao M, Li T, Fang F et al. 2021. A novel Microviridae phage (CLasMV1) from “Candidatus Liberibacter asiaticus. .” Front. Microbiol. 12:754245
    [Google Scholar]
  23. 23.
    Holmfeldt K, Solonenko N, Shah M, Corrier K, Riemann L et al. 2013. Twelve previously unknown phage genera are ubiquitous in global oceans. PNAS 110:12798–803
    [Google Scholar]
  24. 24.
    Bartlau N, Wichels A, Krohne G, Adriaenssens EM, Heins A et al. 2021. Highly diverse flavobacterial phages isolated from North Sea spring blooms. ISME J. 16:555–68
    [Google Scholar]
  25. 25.
    Burgess AB. 1969. Studies on the proteins of ϕX174, II. The protein composition of the ϕX coat. PNAS 64:613–17
    [Google Scholar]
  26. 26.
    Chipman PR, Agbandje-McKenna M, Renaudin J, Baker TS, McKenna R. 1998. Structural analysis of the spiroplasma virus, SpV4: implications for evolutionary variation to obtain host diversity among the Microviridae. Structure 6:135–45
    [Google Scholar]
  27. 27.
    McKenna R, Xia D, Willingmann P, Ilag LL, Rossmann MG. 1992. Structure determination of the bacteriophage ϕX174. Acta Crystallogr. B Struct. Sci. 48:499–511
    [Google Scholar]
  28. 28.
    Krupovic M, Koonin EV. 2017. Multiple origins of viral capsid proteins from cellular ancestors. PNAS 114:E2401–10
    [Google Scholar]
  29. 29.
    Henry TJ, Knippers R. 1974. Isolation and function of the gene A initiator of bacteriophage ϕX 174, a highly specific DNA endonuclease. PNAS 71:1549–53
    [Google Scholar]
  30. 30.
    Ilyina TV, Koonin EV. 1992. Conserved sequence motifs in the initiator proteins for rolling circle DNA replication encoded by diverse replicons from eubacteria, eucaryotes and archaebacteria. Nucleic Acids Res. 20:3279–85
    [Google Scholar]
  31. 31.
    Chandler M, De La Cruz F, Dyda F, Hickman AB, Moncalian G, Ton-Hoang B. 2013. Breaking and joining single-stranded DNA: the HUH endonuclease superfamily. Nat. Rev. Microbiol. 11:525–38
    [Google Scholar]
  32. 32.
    Kazlauskas D, Varsani A, Koonin EV, Krupovic M. 2019. Multiple origins of prokaryotic and eukaryotic single-stranded DNA viruses from bacterial and archaeal plasmids. Nat. Commun. 10:3425
    [Google Scholar]
  33. 33.
    Krupovic M, Varsani A, Kazlauskas D, Breitbart M, Delwart E et al. 2020. Cressdnaviricota: a virus phylum unifying seven families of Rep-encoding viruses with single-stranded, circular DNA genomes. J. Virol. 94:e00582–20
    [Google Scholar]
  34. 34.
    Krupovic M. 2013. Networks of evolutionary interactions underlying the polyphyletic origin of ssDNA viruses. Curr. Opin. Virol. 3:578–86
    [Google Scholar]
  35. 35.
    Cherwa JE Jr., Young LN, Fane BA. 2011. Uncoupling the functions of a multifunctional protein: the isolation of a DNA pilot protein mutant that affects particle morphogenesis. Virology 411:9–14
    [Google Scholar]
  36. 36.
    Sun L, Rossmann MG, Fane BA. 2014. High-resolution structure of a virally encoded DNA-translocating conduit and the mechanism of DNA penetration. J. Virol. 88:10276–79
    [Google Scholar]
  37. 37.
    Sun L, Young LN, Zhang X, Boudko SP, Fokine A et al. 2014. Icosahedral bacteriophage ϕX174 forms a tail for DNA transport during infection. Nature 505:432–35
    [Google Scholar]
  38. 38.
    Jaschke PR, Dotson GA, Hung KS, Liu D, Endy D. 2019. Definitive demonstration by synthesis of genome annotation completeness. PNAS 116:24206–13
    [Google Scholar]
  39. 39.
    Clarke IN, Cutcliffe LT, Everson JS, Garner SA, Lambden PR et al. 2004. Chlamydiaphage Chp2, a skeleton in the ϕX174 closet: scaffolding protein and procapsid identification. J. Bacteriol. 186:7571–74
    [Google Scholar]
  40. 40.
    Fremin BJ, Bhatt AS, Kyrpides NC, Global Phage Small Open Read. Frame (GP-SmORF) Consort 2022. Thousands of small, novel genes predicted in global phage genomes. Cell Rep. 39:110984
    [Google Scholar]
  41. 41.
    Pavesi A. 2006. Origin and evolution of overlapping genes in the family Microviridae. J. Gen. Virol. 87:1013–17
    [Google Scholar]
  42. 42.
    Adams M, Hendrickson R, Dempsey D, Lefkowitz E. 2015. Tracking the changes in virus taxonomy. Arch. Virol. 160:1375–83
    [Google Scholar]
  43. 43.
    Lwoff A, Tournier P. 1966. The classification of viruses. Annu. Rev. Microbiol. 20:45–74
    [Google Scholar]
  44. 44.
    Lacković Z, Toljan K. 2020. Vladimir Sertić: forgotten pioneer of virology and bacteriophage therapy. Notes Records 74:567–78
    [Google Scholar]
  45. 45.
    Krupovic M, Dutilh BE, Adriaenssens EM, Wittmann J, Vogensen FK et al. 2016. Taxonomy of prokaryotic viruses: update from the ICTV Bacterial and Archaeal Viruses Subcommittee. Arch. Virol. 161:1095–99
    [Google Scholar]
  46. 46.
    Renaudin J, Pascarel M, Garnier M, Carle-Junca P, Bove J. 1984. SpV4, a new spiroplasma virus with circular, single-stranded DNA. Ann. Inst. Pasteur Virol. 135:343–61
    [Google Scholar]
  47. 47.
    Francki RIB 1991. President's Report 1987–1990. Classification and Nomenclature of Viruses RIB Francki, CM Fauquet, DL Knudson, F Brown 38–42. Vienna: Springer
    [Google Scholar]
  48. 48.
    Brentlinger KL, Hafenstein S, Novak CR, Fane BA, Borgon R et al. 2002. Microviridae, a family divided: isolation, characterization, and genome sequence of ϕMH2K, a bacteriophage of the obligate intracellular parasitic bacterium Bdellovibrio bacteriovorus. J. Bacteriol. 184:1089–94
    [Google Scholar]
  49. 49.
    Storey CC, Lusher M, Richmond SJ. 1989. Analysis of the complete nucleotide sequence of Chp1, a phage which infects avian Chlamydia psittaci. J. Gen. Virol. 70:3381–90
    [Google Scholar]
  50. 50.
    Carstens E. 2010. Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses 2009. Arch. Virol. 155:133–46
    [Google Scholar]
  51. 51.
    Kirchberger PC, Ochman H. 2020. Resurrection of a global, metagenomically defined gokushovirus. eLife 9:e51599
    [Google Scholar]
  52. 52.
    Walker PJ, Siddell SG, Lefkowitz EJ, Mushegian AR, Adriaenssens EM et al. 2022. Recent changes to virus taxonomy ratified by the International Committee on Taxonomy of Viruses 2022. Arch. Virol. 167:2429–40
    [Google Scholar]
  53. 53.
    Diez-Villasenor C, Rodriguez-Valera F. 2019. CRISPR analysis suggests that small circular single-stranded DNA smacoviruses infect Archaea instead of humans. Nat. Commun. 10:294
    [Google Scholar]
  54. 54.
    Koonin EV, Dolja VV, Krupovic M, Varsani A, Wolf YI et al. 2020. Global organization and proposed megataxonomy of the virus world. Microbiol. Mol. Biol. Rev. 84:e00061–19
    [Google Scholar]
  55. 55.
    Edgell MH, Hutchison CA III, Sinsheimer RL 1969. The process of infection with bacteriophage ϕX174: XXVIII. Removal of the spike proteins from the phage capsid. J. Mol. Biol. 42:547–57
    [Google Scholar]
  56. 56.
    Read TD, Fraser CM, Hsia R-C, Bavoil PM. 2000. Comparative analysis of Chlamydia bacteriophages reveals variation localized to a putative receptor binding domain. Microb. Comp. Genom. 5:223–31
    [Google Scholar]
  57. 57.
    Beller L, Deboutte W, Vieira-Silva S, Falony G, Tito RY et al. 2022. The virota and its transkingdom interactions in the healthy infant gut. PNAS 119:e2114619119
    [Google Scholar]
  58. 58.
    Zheng Q, Chen Q, Xu Y, Suttle CA, Jiao N. 2018. A virus infecting marine photoheterotrophic Alphaproteobacteria (Citromicrobium spp.) defines a new lineage of ssDNA viruses. Front. Microbiol. 9:1418
    [Google Scholar]
  59. 59.
    Wigington CH, Sonderegger D, Brussaard CP, Buchan A, Finke JF et al. 2016. Re-examination of the relationship between marine virus and microbial cell abundances. Nat. Microbiol. 1:15024
    [Google Scholar]
  60. 60.
    Holmfeldt K, Odic D, Sullivan MB, Middelboe M, Riemann L. 2012. Cultivated single-stranded DNA phages that infect marine Bacteroidetes prove difficult to detect with DNA-binding stains. Appl. Environ. Microbiol. 78:892–94
    [Google Scholar]
  61. 61.
    Kaletta J, Pickl C, Griebler C, Klingl A, Kurmayer R, Deng L. 2020. A rigorous assessment and comparison of enumeration methods for environmental viruses. Sci. Rep. 10:18625
    [Google Scholar]
  62. 62.
    Sawaya NA, Baran N, Mahank S, Varsani A, Lindell D, Breitbart M. 2021. Adaptation of the polony technique to quantify Gokushovirinae, a diverse group of single-stranded DNA phage. Environ. Microbiol. 23:6622–36
    [Google Scholar]
  63. 63.
    Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM et al. 2002. Genomic analysis of uncultured marine viral communities. PNAS 99:14250–55
    [Google Scholar]
  64. 64.
    Callanan J, Stockdale SR, Shkoporov A, Draper LA, Ross RP, Hill C. 2021. Biases in viral metagenomics-based detection, cataloguing and quantification of bacteriophage genomes in human faeces, a review. Microorganisms 9:524
    [Google Scholar]
  65. 65.
    Thurber RV, Haynes M, Breitbart M, Wegley L, Rohwer F. 2009. Laboratory procedures to generate viral metagenomes. Nat. Protoc. 4:470–83
    [Google Scholar]
  66. 66.
    Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA et al. 2006. The marine viromes of four oceanic regions. PLOS Biol. 4:2121–31
    [Google Scholar]
  67. 67.
    Creasy A, Rosario K, Leigh BA, Dishaw LJ, Breitbart M. 2018. Unprecedented diversity of ssDNA phages from the family Microviridae detected within the gut of a protochordate model organism (Ciona robusta). Viruses 10:404
    [Google Scholar]
  68. 68.
    Tisza MJ, Pastrana DV, Welch NL, Stewart B, Peretti A et al. 2020. Discovery of several thousand highly diverse circular DNA viruses. eLife 9:e51971
    [Google Scholar]
  69. 69.
    Everson J, Garner S, Fane B, Liu B-L, Lambden P, Clarke I. 2002. Biological properties and cell tropism of Chp2, a bacteriophage of the obligate intracellular bacterium Chlamydophila abortus. J. Bacteriol. 184:2748–54
    [Google Scholar]
  70. 70.
    Kuhn H, Frank-Kamenetskii MD. 2005. Template-independent ligation of single-stranded DNA by T4 DNA ligase. FEBS J. 272:5991–6000
    [Google Scholar]
  71. 71.
    Roux S, Solonenko NE, Dang VT, Poulos BT, Schwenck SM et al. 2016. Towards quantitative viromics for both double-stranded and single-stranded DNA viruses. PeerJ 4:e2777
    [Google Scholar]
  72. 72.
    Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M et al. 2016. Uncovering Earth's virome. Nature 536:425–30
    [Google Scholar]
  73. 73.
    Gregory AC, Zayed AA, Conceicao-Neto N, Temperton B, Bolduc B et al. 2019. Marine DNA viral macro- and microdiversity from pole to pole. Cell 177:1109–23
    [Google Scholar]
  74. 74.
    Camarillo-Guerrero LF, Almeida A, Rangel-Pineros G, Finn RD, Lawley TD. 2021. Massive expansion of human gut bacteriophage diversity. Cell 184:1098–109
    [Google Scholar]
  75. 75.
    Nishijima S, Nagata N, Kiguchi Y, Kojima Y, Miyoshi-Akiyama T et al. 2022. Extensive gut virome variation and its associations with host and environmental factors in a population-level cohort. Nat. Commun. 13:5252
    [Google Scholar]
  76. 76.
    Dean FB, Nelson JR, Giesler TL, Lasken RS. 2001. Rapid amplification of plasmid and phage DNA using Phi29 DNA polymerase and multiply-primed rolling circle amplification. Genome Res. 11:1095–99
    [Google Scholar]
  77. 77.
    Gregory AC, Zablocki O, Zayed AA, Howell A, Bolduc B, Sullivan MB. 2020. The Gut Virome Database reveals age-dependent patterns of virome diversity in the human gut. Cell Host Microbe 28:724–40
    [Google Scholar]
  78. 78.
    Wang H, Ling Y, Shan T, Yang S, Xu H et al. 2019. Gut virome of mammals and birds reveals high genetic diversity of the family Microviridae. Virus Evol. 5:vez013
    [Google Scholar]
  79. 79.
    Norman JM, Handley SA, Baldridge MT, Droit L, Liu CY et al. 2015. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160:447–60
    [Google Scholar]
  80. 80.
    Liang G, Gao H, Bushman FD. 2022. The pediatric virome in health and disease. Cell Host Microbe 30:639–49
    [Google Scholar]
  81. 81.
    Lim ES, Zhou Y, Zhao G, Bauer IK, Droit L et al. 2015. Early life dynamics of the human gut virome and bacterial microbiome in infants. Nat. Med. 21:1228–34
    [Google Scholar]
  82. 82.
    Reyes A, Blanton LV, Cao S, Zhao G, Manary M et al. 2015. Gut DNA viromes of Malawian twins discordant for severe acute malnutrition. PNAS 112:11941–46
    [Google Scholar]
  83. 83.
    Kim KH, Bae JW. 2011. Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl. Environ. Microbiol. 77:7663–68
    [Google Scholar]
  84. 84.
    Yilmaz S, Allgaier M, Hugenholtz P. 2010. Multiple displacement amplification compromises quantitative analysis of metagenomes. Nat. Methods 7:943–44
    [Google Scholar]
  85. 85.
    Schumacher C, Kurihara L, Cunningham K. 2015. NGS library preparation for balanced, comprehensive methylome coverage from low-input quantities. Nat. Methods 12:5–6
    [Google Scholar]
  86. 86.
    Trubl G, Roux S, Solonenko N, Li YF, Bolduc B et al. 2019. Towards optimized viral metagenomes for double-stranded and single-stranded DNA viruses from challenging soils. PeerJ 7:e7265
    [Google Scholar]
  87. 87.
    Shkoporov AN, Stockdale SR, Lavelle A, Kondova I, Heuston C et al. 2022. Viral biogeography of the mammalian gut and parenchymal organs. Nat. Microbiol. 7:1301–11
    [Google Scholar]
  88. 88.
    Draper LA, Ryan FJ, Smith MK, Jalanka J, Mattila E et al. 2018. Long-term colonisation with donor bacteriophages following successful faecal microbial transplantation. Microbiome 6:220
    [Google Scholar]
  89. 89.
    Zuo T, Wong SH, Lam K, Lui R, Cheung K et al. 2018. Bacteriophage transfer during faecal microbiota transplantation in Clostridium difficile infection is associated with treatment outcome. Gut 67:634–43
    [Google Scholar]
  90. 90.
    Fujimoto K, Kimura Y, Allegretti JR, Yamamoto M, Zhang YZ et al. 2021. Functional restoration of bacteriomes and viromes by fecal microbiota transplantation. Gastroenterology 160:2089–102.e12
    [Google Scholar]
  91. 91.
    Yoshida M, Mochizuki T, Urayama SI, Yoshida-Takashima Y, Nishi S et al. 2018. Quantitative viral community DNA analysis reveals the dominance of single-stranded DNA viruses in offshore upper bathyal sediment from Tohoku, Japan. Front. Microbiol. 9:75
    [Google Scholar]
  92. 92.
    Godson GN. 1974. Evolution of ϕX174. Isolation of four new ϕX-like phages and comparison with ϕX174. Virology 58:272–89
    [Google Scholar]
  93. 93.
    Rokyta DR, Burch CL, Caudle SB, Wichman HA. 2006. Horizontal gene transfer and the evolution of microvirid coliphage genomes. J. Bacteriol. 188:1134–42
    [Google Scholar]
  94. 94.
    Carroll-Portillo A, Coffman CN, Varga MG, Alcock J, Singh SB, Lin HC. 2021. Standard bacteriophage purification procedures cause loss in numbers and activity. Viruses 13:328
    [Google Scholar]
  95. 95.
    Olsen NS, Hendriksen NB, Hansen LH, Kot W. 2020. A new high-throughput screening method for phages: enabling crude isolation and fast identification of diverse phages with therapeutic potential. Phage 1:137–48
    [Google Scholar]
  96. 96.
    Castillo D, Kauffman K, Hussain F, Kalatzis P, Rorbo N et al. 2018. Widespread distribution of prophage-encoded virulence factors in marine Vibrio communities. Sci. Rep. 8:9973
    [Google Scholar]
  97. 97.
    Kauffman KM, Hussain FA, Yang J, Arevalo P, Brown JM et al. 2018. A major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria. Nature 554:118–22
    [Google Scholar]
  98. 98.
    Guo R, Zheng K, Luo L, Liu Y, Shao H et al. 2022. Characterization and genomic analysis of ssDNA vibriophage vB_VpaM_PG19 within Microviridae, representing a novel viral genus. Microbiol. Spectr. 10:e00585–22
    [Google Scholar]
  99. 99.
    Xu W, Xuan G, Lin H, Wang J. 2022. Complete genome analysis of the newly isolated Vibrio phage vB_VpP_WS1 of the family Microviridae. Arch. Virol. 167:1311–16
    [Google Scholar]
  100. 100.
    Labonte JM, Suttle CA. 2013. Metagenomic and whole-genome analysis reveals new lineages of gokushoviruses and biogeographic separation in the sea. Front. Microbiol. 4:404
    [Google Scholar]
  101. 101.
    Hopkins M, Kailasan S, Cohen A, Roux S, Tucker KP et al. 2014. Diversity of environmental single-stranded DNA phages revealed by PCR amplification of the partial major capsid protein. ISME J. 8:2093–103
    [Google Scholar]
  102. 102.
    Zucker F, Bischoff V, Olo Ndela E, Heyerhoff B, Poehlein A et al. 2022. New Microviridae isolated from Sulfitobacter reveals two cosmopolitan subfamilies of ssDNA phages infecting marine and terrestrial Alphaproteobacteria. Virus Evol. 8:veac070
    [Google Scholar]
  103. 103.
    Russell DA, Hatfull GF. 2017. PhagesDB: the actinobacteriophage database. Bioinformatics 33:784–86
    [Google Scholar]
  104. 104.
    Sliwa-Dominiak J, Suszynska E, Pawlikowska M, Deptula W. 2013. Chlamydia bacteriophages. Arch. Microbiol. 195:765–71
    [Google Scholar]
  105. 105.
    Van Cauwenberghe J, Santamaria RI, Bustos P, Juarez S, Ducci MA et al. 2021. Spatial patterns in phage-Rhizobium coevolutionary interactions across regions of common bean domestication. ISME J. 15:2092–106
    [Google Scholar]
  106. 106.
    Fitzgerald CB, Shkoporov AN, Upadrasta A, Khokhlova EV, Ross RP, Hill C. 2021. Probing the “dark matter” of the human gut phageome: Culture assisted metagenomics enables rapid discovery and host-linking for novel bacteriophages. Front. Cell. Infect. Microbiol. 11:616918
    [Google Scholar]
  107. 107.
    Pascarel-Devilder M-C, Renaudin J, Bove JM. 1986. The spiroplasma virus 4 replicative form cloned in Escherichia coli transfects spiroplasmas. Virology 151:390–93
    [Google Scholar]
  108. 108.
    White RA III. 2021. The future of virology is synthetic. mSystems 6:e00770–21
    [Google Scholar]
  109. 109.
    Liu Y, Han Y, Huang W, Duan Y, Mou L et al. 2012. Whole-genome synthesis and characterization of viable S13-like bacteriophages. PLOS ONE 7:e41124
    [Google Scholar]
  110. 110.
    Sugimoto R, Nishimura L, Nguyen PT, Ito J, Parrish NF et al. 2021. Comprehensive discovery of CRISPR-targeted terminally redundant sequences in the human gut metagenome: viruses, plasmids, and more. PLOS Comput. Biol. 17:e1009428
    [Google Scholar]
  111. 111.
    Deecker SR, Urbanus ML, Nicholson B, Ensminger AW. 2021. Legionella pneumophila CRISPR-Cas suggests recurrent encounters with one or more phages in the family Microviridae. Appl. Environ. Microbiol. 87:e00467–21
    [Google Scholar]
  112. 112.
    Dzunkova M, Low SJ, Daly JN, Deng L, Rinke C, Hugenholtz P. 2019. Defining the human gut host-phage network through single-cell viral tagging. Nat. Microbiol. 4:2192–203
    [Google Scholar]
  113. 113.
    Mukherjee S, Huntemann M, Ivanova N, Kyrpides NC, Pati A. 2015. Large-scale contamination of microbial isolate genomes by Illumina PhiX control. Stand. Genom. Sci. 10:18
    [Google Scholar]
  114. 114.
    Szekely AJ, Breitbart M. 2016. Single-stranded DNA phages: from early molecular biology tools to recent revolutions in environmental microbiology. FEMS Microbiol. Lett. 363:fnw027
    [Google Scholar]
  115. 115.
    Camargo AP, Nayfach S, Chen IA, Palaniappan K, Ratner A et al. 2022. IMG/VR v4: an expanded database of uncultivated virus genomes within a framework of extensive functional, taxonomic, and ecological metadata. Nucleic Acids Res. 50:D733–43
    [Google Scholar]
  116. 116.
    Johnson G, Banerjee S, Putonti C. 2022. Diversity of Pseudomonas aeruginosa temperate phages. mSphere 7:e01015–21
    [Google Scholar]
  117. 117.
    Krupovic M, Forterre P. 2011. Microviridae goes temperate: Microvirus-related proviruses reside in the genomes of Bacteroidetes. PLOS ONE 6:e19893
    [Google Scholar]
  118. 118.
    Kirchberger PC, Martinez ZA, Luker LJ, Ochman H. 2021. Defensive hypervariable regions confer superinfection exclusion in microviruses. PNAS 118:e2102786118
    [Google Scholar]
  119. 119.
    Michel A, Clermont O, Denamur E, Tenaillon O. 2010. Bacteriophage PhiX174’s ecological niche and the flexibility of its Escherichia coli lipopolysaccharide receptor. Appl. Environ. Microbiol. 76:7310–13
    [Google Scholar]
  120. 120.
    Sillankorva S, Oliveira D, Moura A, Henriques M, Faustino A et al. 2011. Efficacy of a broad host range lytic bacteriophage against E. coli adhered to urothelium. Curr. Microbiol. 62:1128–32
    [Google Scholar]
  121. 121.
    Suzuki M, Kaneko-Tanaka Y, Azegami M. 1974. Transfection of non-host bacterial spheroplasts with bacteriophage ϕX174 DNA. Nature 252:319–21
    [Google Scholar]
  122. 122.
    Slater SC, Maurer R. 1991. Requirements for bypass of UV-induced lesions in single-stranded DNA of bacteriophage ϕX174 in Salmonella typhimurium. PNAS 88:1251–55
    [Google Scholar]
  123. 123.
    Jiang C, Tanaka M, Nishikawa S, Mino S, Romalde JL et al. 2022. Vibrio Clade 3.0: new Vibrionaceae evolutionary units using genome-based approach. Curr. Microbiol. 79:10
    [Google Scholar]
  124. 124.
    Everson JS, Garner SA, Lambden PR, Fane BA, Clarke IN. 2003. Host range of chlamydiaphages phiCPAR39 and Chp3. J. Bacteriol. 185:6490–92
    [Google Scholar]
  125. 125.
    Van Cauwenberghe J, Santamaria RI, Bustos P, Gonzalez V. 2022. Novel lineages of single-stranded DNA phages that coevolved with the symbiotic bacteria Rhizobium. Front. Microbiol. 13:990394
    [Google Scholar]
  126. 126.
    Liu D, Reeves PR. 1994. Escherichia coli K12 regains its O antigen. Microbiology 140:49–57
    [Google Scholar]
  127. 127.
    Roznowski AP, Young RJ, Love SD, Andromita AA, Guzman VA et al. 2019. Recessive host range mutants and unsusceptible cells that inactivate virions without genome penetration: ecological and technical implications. J. Virol. 93:e01767–18
    [Google Scholar]
  128. 128.
    Brown DT, MacKenzie JM, Bayer ME. 1971. Mode of host cell penetration by bacteriophage ϕX174. J. Virol. 7:836–46
    [Google Scholar]
  129. 129.
    Maffei E, Shaidullina A, Burkolter M, Heyer Y, Estermann F et al. 2021. Systematic exploration of Escherichia coli phage-host interactions with the BASEL phage collection. PLOS Biol. 19:e3001424
    [Google Scholar]
  130. 130.
    Cuevas JM, Duffy S, Sanjuán R. 2009. Point mutation rate of bacteriophage ϕX174. Genetics 183:747–49
    [Google Scholar]
  131. 131.
    Sanjuán R, Domingo-Calap P. 2016. Mechanisms of viral mutation. Cell. Mol. Life Sci. 73:4433–48
    [Google Scholar]
  132. 132.
    Minot S, Bryson A, Chehoud C, Wu GD, Lewis JD, Bushman FD. 2013. Rapid evolution of the human gut virome. PNAS 110:12450–55
    [Google Scholar]
  133. 133.
    Rokyta DR, Abdo Z, Wichman HA. 2009. The genetics of adaptation for eight microvirid bacteriophages. J. Mol. Evol. 69:229–39
    [Google Scholar]
  134. 134.
    Suttle CA. 2007. Marine viruses—major players in the global ecosystem. Nat. Rev. Microbiol. 5:801–12
    [Google Scholar]
  135. 135.
    Ranasinghe R. 2019. Literature study of virus size, burst size, latent period and genome size across different lytic eukaryotic and prokaryotic virus groups-an overview of traits and possible trade-offs Master's Thesis University of Bergen Bergen, Nor:.
    [Google Scholar]
  136. 136.
    Midonet C, Barre FX. 2014. Xer site-specific recombination: promoting vertical and horizontal transmission of genetic information. Microbiol. Spectr. 2:163–82
    [Google Scholar]
  137. 137.
    Midonet C, Barre FX. 2016. How Xer-exploiting mobile elements overcome cellular control. PNAS 113:8343–45
    [Google Scholar]
  138. 138.
    Shkoporov AN, Khokhlova EV, Fitzgerald CB, Stockdale SR, Draper LA et al. 2018. ϕCrAss001 represents the most abundant bacteriophage family in the human gut and infects Bacteroides intestinalis. Nat. Commun. 14:4781
    [Google Scholar]
  139. 139.
    Roux S, Hawley AK, Torres Beltran M, Scofield M, Schwientek P et al. 2014. Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta-genomics. eLife 3:e03125
    [Google Scholar]
  140. 140.
    Diaz-Munoz SL. 2017. Viral coinfection is shaped by host ecology and virus–virus interactions across diverse microbial taxa and environments. Virus Evol. 3:vex011
    [Google Scholar]
  141. 141.
    Millman A, Melamed S, Leavitt A, Doron S, Bernheim A et al. 2022. An expanded arsenal of immune systems that protect bacteria from phages. Cell Host Microbe 30:1556–69
    [Google Scholar]
  142. 142.
    Chamakura KR, Young R. 2020. Single-gene lysis in the metagenomic era. Curr. Opin. Microbiol. 56:109–17
    [Google Scholar]
  143. 143.
    Bryson SJ, Thurber AR, Correa AM, Orphan VJ, Thurber RV. 2015. A novel sister clade to the enterobacteria microviruses (family Microviridae) identified in methane seep sediments. Environ. Microbiol. 17:3708–21
    [Google Scholar]
  144. 144.
    Roux S, Krupovic M, Poulet A, Debroas D, Enault F. 2012. Evolution and diversity of the Microviridae viral family through a collection of 81 new complete genomes assembled from virome reads. PLOS ONE 7:e40418
    [Google Scholar]
  145. 145.
    Quaiser A, Dufresne A, Ballaud F, Roux S, Zivanovic Y et al. 2015. Diversity and comparative genomics of Microviridae in Sphagnum-dominated peatlands. Front. Microbiol. 6:375
    [Google Scholar]
  146. 146.
    Rosario K, Dayaram A, Marinov M, Ware J, Kraberger S et al. 2012. Diverse circular ssDNA viruses discovered in dragonflies (Odonata: Epiprocta). J. Gen. Virol. 93:2668–81
    [Google Scholar]
  147. 147.
    Tikhe CV, Husseneder C. 2018. Metavirome sequencing of the termite gut reveals the presence of an unexplored bacteriophage community. Front. Microbiol. 8:2548
    [Google Scholar]
  148. 148.
    Liu Y, Demina TA, Roux S, Aiewsakun P, Kazlauskas D et al. 2021. Diversity, taxonomy, and evolution of archaeal viruses of the class Caudoviricetes. PLOS Biol. 19:e3001442
    [Google Scholar]
  149. 149.
    Salim O, Skilton RJ, Lambden PR, Fane BA, Clarke IN. 2008. Behind the chlamydial cloak: the replication cycle of chlamydiaphage Chp2, revealed. Virology 377:440–45
    [Google Scholar]
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