Archaeal viruses and bacteriophages: Comparisons and contrasts

Trends in Microbiology

Volumn 22, Issue 6, 2014, Pages 334-344

  Pietilä, Maija K ^a   Demina, Tatiana A ^a   Atanasova, Nina S ^a   Oksanen, Hanna M ^a   Bamford, Dennis H ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Archaea; Bacteria; Morphotype; Virion; Virus

Indexed keywords

CIRCULAR DNA; DOUBLE STRANDED DNA; SINGLE STRANDED DNA;

ACIDIANUS; ARCHAEAL VIRUS; BACTERIOPHAGE; CRENARCHAEOTA; CRYOELECTRON MICROSCOPY; EUKARYOTE; GENE TRANSLOCATION; HALOARCULA; HALOBACTERIUM; HALOPHILIC ARCHAEON; HALORUBRUM; METHANOCOCCUS VOLTAE; METHANOGENIC ARCHAEON; MOLECULAR EVOLUTION; MORPHOLOGY; MORPHOTYPE; NONHUMAN; PRIORITY JOURNAL; PYROBACULUM; REVIEW; SEQUENCE HOMOLOGY; SPECIES COMPARISON; SULFOLOBUS; THERMOCOCCUS; VIRION; ARCHAEON; COMPARATIVE STUDY; ISOLATION AND PURIFICATION; PHYSIOLOGY; ULTRASTRUCTURE; VIROLOGY;

ARCHAEA; BACTERIA (MICROORGANISMS); PROKARYOTA;

ARCHAEA; ARCHAEAL VIRUSES; BACTERIOPHAGES; VIRION;

EID: 84901597419     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2014.02.007     Document Type: Review

References (117)

1. Comeau A.M., et al. Exploring the prokaryotic virosphere. Res. Microbiol. 2008, 159:306-313.
2. Suttle C.A. Marine viruses - major players in the global ecosystem. Nat. Rev. Microbiol. 2007, 5:801-812.
3. Ackermann H.W. Bacteriophage electron microscopy. Adv. Virus Res. 2012, 82:1-32.
4. Woese C.R., et al. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:4576-4579.
5. Torsvik T., Dundas I.D. Bacteriophage of Halobacterium salinarium. Nature 1974, 248:680-681.
6. Atanasova N.S., et al. Global network of specific virus-host interactions in hypersaline environments. Environ. Microbiol. 2012, 14:426-440.
7. Pina M., et al. The archeoviruses. FEMS Microbiol. Rev. 2011, 35:1035-1054.
8. Ackermann H.W., Prangishvili D. Prokaryote viruses studied by electron microscopy. Arch. Virol. 2012, 157:1843-1849.
9. Winker S., Woese C.R. A definition of the domains Archaea, Bacteria and Eucarya in terms of small subunit ribosomal RNA characteristics. Syst. Appl. Microbiol. 1991, 14:305-310.
10. Cavicchioli R. Archaea - timeline of the third domain. Nat. Rev. Microbiol. 2011, 9:51-61.
11. Gribaldo S., Brochier-Armanet C. Time for order in microbial systematics. Trends Microbiol. 2012, 20:209-210.
12. DasSarma S., DasSarma P. Halophiles. In Encyclopedia of Life Sciences 2012, John Wiley & Sons. 10.1002/9780470015902.a0000394.pub3.
13. Chaban B., et al. Archaeal habitats - from the extreme to the ordinary. Can. J. Microbiol. 2006, 52:73-116.
14. DeLong E.F., Pace N.R. Environmental diversity of bacteria and archaea. Syst. Biol. 2001, 50:470-478.
15. Oren A. Molecular ecology of extremely halophilic Archaea and Bacteria. FEMS Microbiol. Ecol. 2002, 39:1-7.
16. Aalto A.P., et al. Snapshot of virus evolution in hypersaline environments from the characterization of a membrane-containing Salisaeta icosahedral phage 1. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:7079-7084.
17. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses 2012, Elsevier Academic Press. A.M.Q. King (Ed.).
18. Borrel G., et al. Unexpected and novel putative viruses in the sediments of a deep-dark permanently anoxic freshwater habitat. ISME J. 2012, 6:2119-2127.
19. Krupovič M., et al. A thaumarchaeal provirus testifies for an ancient association of tailed viruses with archaea. Biochem. Soc. Trans. 2011, 39:82-88.
20. Mochizuki T., et al. Provirus induction in hyperthermophilic archaea: characterization of Aeropyrum pernix spindle-shaped virus 1 and Aeropyrum pernix ovoid virus 1. J. Bacteriol. 2011, 193:5412-5419.
21. Krupovič M., et al. Comparative analysis of the mosaic genomes of tailed archaeal viruses and proviruses suggests common themes for virion architecture and assembly with tailed viruses of bacteria. J. Mol. Biol. 2010, 397:144-160.
22. Krupovič M., Bamford D.H. Archaeal proviruses TKV4 and MVV extend the PRD1-adenovirus lineage to the phylum Euryarchaeota. Virology 2008, 375:292-300.
23. Held N.L., Whitaker R.J. Viral biogeography revealed by signatures in Sulfolobus islandicus genomes. Environ. Microbiol. 2009, 11:457-466.
24. Prangishvili D., et al. Evolutionary genomics of archaeal viruses: unique viral genomes in the third domain of life. Virus Res. 2006, 117:52-67.
25. Guixa-Boixareu N., et al. Viral lysis and bacterivory as prokaryotic loss factors along a salinity gradient. Aquat. Microb. Ecol. 1996, 11:215-227.
26. Oren A., et al. Occurrence of virus-like particles in the Dead Sea. Extremophiles 1997, 1:143-149.
27. Sime-Ngando T., et al. Diversity of virus-host systems in hypersaline Lake Retba, Senegal. Environ. Microbiol. 2011, 13:1956-1972.
28. Santos F., et al. Metagenomic approach to the study of halophages: the environmental halophage 1. Environ. Microbiol. 2007, 9:1711-1723.
29. Rachel R., et al. Remarkable morphological diversity of viruses and virus-like particles in hot terrestrial environments. Arch. Virol. 2002, 147:2419-2429.
30. Nuttall S.D., Dyall-Smith M.L. HF1 and HF2: novel bacteriophages of halophilic archaea. Virology 1993, 197:678-684.
31. Tang S.L., et al. Haloviruses HF1 and HF2: evidence for a recent and large recombination event. J. Bacteriol. 2004, 186:2810-2817.
32. Pietilä M.K., et al. Insights into head-tailed viruses infecting extremely halophilic archaea. J. Virol. 2013, 87:3248-3260.
33. Klein R., et al. Natrialba magadii virus φCh1: first complete nucleotide sequence and functional organization of a virus infecting a haloalkaliphilic archaeon. Mol. Microbiol. 2002, 45:851-863.
34. Schnabel H., et al. Halobacterium halobium phage φH. EMBO J. 1982, 1:87-92.
35. Witte A., et al. Characterization of Natronobacterium magadii phage φCh1, a unique archaeal phage containing DNA and RNA. Mol. Microbiol. 1997, 23:603-616.
36. Pietilä M.K., et al. Virion architecture unifies globally distributed pleolipoviruses infecting halophilic archaea. J. Virol. 2012, 86:5067-5079.
37. Porter K., et al. SH1: a novel, spherical halovirus isolated from an Australian hypersaline lake. Virology 2005, 335:22-33.
38. Pietilä M.K., et al. Structure of the archaeal head-tailed virus HSTV-1 completes the HK97 fold story. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:10604-10609.
39. Häring M., et al. Morphology and genome organization of the virus PSV of the hyperthermophilic archaeal genera Pyrobaculum and Thermoproteus: a novel virus family, the Globuloviridae. Virology 2004, 323:233-242.
40. Happonen L.J., et al. Familial relationships in hyperthermo- and acidophilic archaeal viruses. J. Virol. 2010, 84:4747-4754.
41. Jaakkola S.T., et al. Closely related archaeal Haloarcula hispanica icosahedral viruses HHIV-2 and SH1 have nonhomologous genes encoding host recognition functions. J. Virol. 2012, 86:4734-4742.
42. Veesler D., et al. Atomic structure of the 75MDa extremophile Sulfolobus turreted icosahedral virus determined by CryoEM and X-ray crystallography. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:5504-5509.
43. Porter K., et al. PH1: an archaeovirus of Haloarcula hispanica related to SH1 and HHIV-2. Archaea 2013, 2013:456318.
44. Prangishvili D. The wonderful world of archaeal viruses. Annu. Rev. Microbiol. 2013, 67:565-585.
45. Bamford D.H., et al. Constituents of SH1, a novel lipid-containing virus infecting the halophilic euryarchaeon Haloarcula hispanica. J. Virol. 2005, 79:9097-9107.
46. Laurinavičius S., et al. The origin of phospholipids of the enveloped bacteriophage phi6. Virology 2004, 326:182-190.
47. Laurinavičius S., et al. Phospholipid molecular species profiles of tectiviruses infecting Gram-negative and Gram-positive hosts. Virology 2004, 322:328-336.
48. Zhang Z., et al. Temperate membrane-containing halophilic archaeal virus SNJ1 has a circular dsDNA genome identical to that of plasmid pHH205. Virology 2012, 434:233-241.
49. Strömsten N.J., et al. In vitro DNA packaging of PRD1: a common mechanism for internal-membrane viruses. J. Mol. Biol. 2005, 348:617-629.
50. Häring M., et al. Structure and genome organization of AFV2, a novel archaeal lipothrixvirus with unusual terminal and core structures. J. Bacteriol. 2005, 187:3855-3858.
51. Goulet A., et al. Acidianus filamentous virus 1 coat proteins display a helical fold spanning the filamentous archaeal viruses lineage. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:21155-21160.
52. Prangishvili D., et al. A novel virus family, the Rudiviridae: structure, virus-host interactions and genome variability of the Sulfolobus viruses SIRV1 and SIRV2. Genetics 1999, 152:1387-1396.
53. Prangishvili D., Krupovič M. A new proposed taxon for double-stranded DNA viruses, the order "Ligamenvirales". Arch. Virol. 2012, 157:791-795.
54. Mochizuki T., et al. Diversity of viruses of the hyperthermophilic archaeal genus Aeropyrum, and isolation of the Aeropyrum pernix bacilliform virus 1, APBV1, the first representative of the family Clavaviridae. Virology 2010, 402:347-354.
55. Mochizuki T., et al. Archaeal virus with exceptional virion architecture and the largest single-stranded DNA genome. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:13386-13391.
56. Snyder J.C., et al. Insights into a viral lytic pathway from an archaeal virus-host system. J. Virol. 2013, 87:2186-2192.
57. Quemin E.R., et al. First insights into the entry process of hyperthermophilic archaeal viruses. J. Virol. 2013, 87:13379-13385.
58. Redder P., et al. Four newly isolated fuselloviruses from extreme geothermal environments reveal unusual morphologies and a possible interviral recombination mechanism. Environ. Microbiol. 2009, 11:2849-2862.
59. Prangishvili D., et al. Structural and genomic properties of the hyperthermophilic archaeal virus ATV with an extracellular stage of the reproductive cycle. J. Mol. Biol. 2006, 359:1203-1216.
60. Xiang X., et al. Sulfolobus tengchongensis spindle-shaped virus STSV1: virus-host interactions and genomic features. J. Virol. 2005, 79:8677-8686.
61. Pietilä M.K., et al. Modified coat protein forms the flexible spindle-shaped virion of haloarchaeal virus His1. Environ. Microbiol. 2013, 15:1674-1686.
62. Wood A.G., et al. Isolation and characterization of an archaebacterial viruslike particle from Methanococcus voltae A3. J. Bacteriol. 1989, 171:93-98.
63. Martin A., et al. SAV 1, a temperate u.v.-inducible DNA virus-like particle from the archaebacterium Sulfolobus acidocaldarius isolate B12. EMBO J. 1984, 3:2165-2168.
64. Gorlas A., et al. TPV1, the first virus isolated from the hyperthermophilic genus Thermococcus. Environ. Microbiol. 2012, 14:503-516.
65. Geslin C., et al. Analysis of the first genome of a hyperthermophilic marine virus-like particle, PAV1, isolated from Pyrococcus abyssi. J. Bacteriol. 2007, 189:4510-4519.
66. Hanhijärvi K.J., et al. DNA ejection from an archaeal virus-a single-molecule approach. Biophys. J. 2013, 104:2264-2272.
67. Bath C., et al. His1 and His2 are distantly related, spindle-shaped haloviruses belonging to the novel virus group, Salterprovirus. Virology 2006, 350:228-239.
68. Schleper C., et al. The particle SSV1 from the extremely thermophilic archaeon Sulfolobus is a virus: demonstration of infectivity and of transfection with viral DNA. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:7645-7649.
69. Reiter W.D., et al. Identification and characterization of the genes encoding three structural proteins of the Sulfolobus virus-like particle SSV1. Mol. Gen. Genet. 1987, 206:144-153.
70. Geslin C., et al. PAV1, the first virus-like particle isolated from a hyperthermophilic euryarchaeote, "Pyrococcus abyssi". J. Bacteriol. 2003, 185:3888-3894.
71. Krupovic M., et al. Unification of the globally distributed spindle-shaped viruses of the archaea. J. Virol. 2014, 88:2354-2358.
72. Erdmann S., et al. SMV1 virus-induced CRISPR spacer acquisition from the conjugative plasmid pMGB1 in Sulfolobus solfataricus P2. Biochem. Soc. Trans. 2013, 41:1449-1458.
73. Erdmann S., et al. A novel single-tailed fusiform Sulfolobus virus STSV2 infecting model Sulfolobus species. Extremophiles 2014, 18:51-60.
74. Pietilä M.K., et al. The single-stranded DNA genome of novel archaeal virus Halorubrum pleomorphic virus 1 is enclosed in the envelope decorated with glycoprotein spikes. J. Virol. 2010, 84:788-798.
75. Kandiba L., et al. Diversity in prokaryotic glycosylation: an archaeal-derived N-linked glycan contains legionaminic acid. Mol. Microbiol. 2012, 84:578-593.
76. Vestergaard G., et al. A novel rudivirus, ARV1, of the hyperthermophilic archaeal genus Acidianus. Virology 2005, 336:83-92.
77. Maaty W.S., et al. Characterization of the archaeal thermophile Sulfolobus turreted icosahedral virus validates an evolutionary link among double-stranded DNA viruses from all domains of life. J. Virol. 2006, 80:7625-7635.
78. Senčilo A., et al. Related haloarchaeal pleomorphic viruses contain different genome types. Nucleic Acids Res. 2012, 40:5523-5534.
79. Pietilä M.K., et al. An ssDNA virus infecting archaea: a new lineage of viruses with a membrane envelope. Mol. Microbiol. 2009, 72:307-319.
80. Roine E., et al. New, closely related haloarchaeal viral elements with different nucleic acid types. J. Virol. 2010, 84:3682-3689.
81. Häring M., et al. Viral diversity in hot springs of Pozzuoli, Italy, and characterization of a unique archaeal virus, Acidianus bottle-shaped virus, from a new family, the Ampullaviridae. J. Virol. 2005, 79:9904-9911.
82. Arnold H.P., et al. SNDV, a novel virus of the extremely thermophilic and acidophilic archaeon Sulfolobus. Virology 2000, 272:409-416.
83. Wikoff W.R., et al. Topologically linked protein rings in the bacteriophage HK97 capsid. Science 2000, 289:2129-2133.
84. Abrescia N.G., et al. Structure unifies the viral universe. Annu. Rev. Biochem. 2012, 81:795-822.
85. Baker M.L., et al. Common ancestry of herpesviruses and tailed DNA bacteriophages. J. Virol. 2005, 79:14967-14970.
86. Hendrix R.W., et al. Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:2192-2197.
87. Senčilo A., et al. Snapshot of haloarchaeal tailed virus genomes. RNA Biol. 2013, 10:803-816.
88. Abrescia N.G., et al. Insights into assembly from structural analysis of bacteriophage PRD1. Nature 2004, 432:68-74.
89. Cockburn J.J., et al. Membrane structure and interactions with protein and DNA in bacteriophage PRD1. Nature 2004, 432:122-125.
90. Krupovič M., et al. Identification and functional analysis of the Rz/Rz1-like accessory lysis genes in the membrane-containing bacteriophage PRD1. Mol. Microbiol. 2008, 68:492-503.
91. Peralta B., et al. Mechanism of membranous tunnelling nanotube formation in viral genome delivery. PLoS Biol. 2013, 11:e1001667.
92. Rydman P.S., et al. A minor capsid protein P30 is essential for bacteriophage PRD1 capsid assembly. J. Mol. Biol. 2001, 313:785-795.
93. Abrescia N.G., et al. Insights into virus evolution and membrane biogenesis from the structure of the marine lipid-containing bacteriophage PM2. Mol. Cell 2008, 31:749-761.
94. Benson S.D., et al. Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures. Cell 1999, 98:825-833.
95. Khayat R., et al. Structure of an archaeal virus capsid protein reveals a common ancestry to eukaryotic and bacterial viruses. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:18944-18949.
96. Rux J.J., et al. Structural and phylogenetic analysis of adenovirus hexons by use of high-resolution x-ray crystallographic, molecular modeling, and sequence-based methods. J. Virol. 2003, 77:9553-9566.
97. Bahar M.W., et al. Insights into the evolution of a complex virus from the crystal structure of vaccinia virus D13. Structure 2011, 19:1011-1020.
98. Nandhagopal N., et al. The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:14758-14763.
99. Zhang X., et al. Structure of Sputnik, a virophage, at 3.5-Å resolution. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:18431-18436.
100. Karhu N.J., et al. Efficient DNA packaging of bacteriophage PRD1 requires the unique vertex protein P6. J. Virol. 2007, 81:2970-2979.
101. Iyer L.M., et al. Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res. 2004, 32:5260-5279.
102. Jäälinoja H.T., et al. Structure and host-cell interaction of SH1, a membrane-containing, halophilic euryarchaeal virus. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:8008-8013.
103. Rissanen I., et al. Bacteriophage P23-77 capsid protein structures reveal the archetype of an ancient branch from a major virus lineage. Structure 2013, 21:718-726.
104. Pawlowski A., et al. Gammasphaerolipovirus, a newly proposed bacteriophage genus, unifies viruses of halophilic archaea and thermophilic bacteria within the novel family Sphaerolipoviridae. Arch. Virol. 2014, 10.1007/s00705-013-1970-6.
105. Bamford D.H., et al. Evolution of viral structure. Theor. Popul. Biol. 2002, 61:461-470.
106. Bamford D.H., et al. What does structure tell us about virus evolution?. Curr. Opin. Struct. Biol. 2005, 15:655-663.
107. Dybvig K., et al. Identification of an enveloped phage, mycoplasma virus L172, that contains a 14-kilobase single-stranded DNA genome. J. Virol. 1985, 53:384-390.
108. Al-Shammari A.J.N., Smith P.F. Lipid composition of two mycoplasmaviruses, MV-Lg-L172 and MVL2. J. Gen. Virol. 1981, 54:455-458.
109. Maniloff J., et al. Sequence analysis of a unique temperature phage: mycoplasma virus L2. Gene 1994, 141:1-8.
110. Roine E., Bamford D.H. Lipids of archaeal viruses. Archaea 2012, 10.1155/2012/384919.
111. Bettstetter M., et al. AFV1, a novel virus infecting hyperthermophilic archaea of the genus Acidianus. Virology 2003, 315:68-79.
112. Szymczyna B.R., et al. Synergy of NMR, computation, and X-ray crystallography for structural biology. Structure 2009, 17:499-507.
113. Bamford D.H. Do viruses form lineages across different domains of life?. Res. Microbiol. 2003, 154:231-236.
114. Raoult D., et al. The 1.2-megabase genome sequence of Mimivirus. Science 2004, 306:1344-1350.
115. Philippe N., et al. Pandoraviruses: amoeba viruses with genomes up to 2.5Mb reaching that of parasitic eukaryotes. Science 2013, 341:281-286.
116. Baltimore D. Expression of animal virus genomes. Bacteriol. Rev. 1971, 35:235-241.
117. Bolduc B., et al. Identification of novel positive-strand RNA viruses by metagenomic analysis of archaea-dominated Yellowstone hot springs. J. Virol. 2012, 86:5562-5573.