Abstract
The tolerance limits of extremophiles in term of temperature, pH, salinity, desiccation, hydrostatic pressure, radiation, anaerobiosis far exceed what can support non-extremophilic organisms. Like all other organisms, extremophiles serve as hosts for viral replication. Many lines of evidence suggest that viruses could no more be regarded as simple infectious “fragments of life” but on the contrary as one of the major components of the biosphere. The exploration of niches with seemingly harsh life conditions as hypersaline and soda lakes, Sahara desert, polar environments or hot acid springs and deep sea hydrothermal vents, permitted to track successfully the presence of viruses. Substantial populations of double-stranded DNA virus that can reach 109 particles per milliliter were recorded. All these viral communities, with genome size ranging from 14 kb to 80 kb, seem to be genetically distinct, suggesting specific niche adaptation. Nevertheless, at this stage of the knowledge, very little is known of their origin, activity, or importance to the in situ microbial dynamics. The continuous attempts to isolate and to study viruses that thrive in extreme environments will be needed to address such questions. However, this topic appears to open a new window on an unexplored part of the viral world.
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References
Ahn DG, Kim SI, Rhee JK, Kim KP, Oh JW (2004) TTSV1, a novel globuloviridae family virus isolated from the hyperthermophilic crenarchaeote Thermoproteus tenax. GenBank Accession: NC_00655
Arnold HP, Zillig W, Ziese U, Holz I, Crosby M, Utterback T, Weidmann JF, Kristjansson JK, Klenk HP, Nelson KE, Fraser CM (2000a) A novel lipothrixvirus, SIFV, of the extremely thermophilic crenarchaeon Sulfolobus. Virology 267:252–266
Arnold HP, Ziese U, Zillig W (2000b) SNDV, a novel virus of the extremely thermohpilic and acidophilic archaeon Sulfolobus. Virology 272:409–416
Bamford DH (2003) Do viruses form lineage across different domains of life? Res Microbiol 154:231–236
Bamford DH, Ravantti JJ, Rönnholm G, Laurinavicius S, Kukkaro P, Dyall-Smith M, Somerharju P, Kalkkinen N, Bamford JKH (2005) Constituents of SH1, a novel lipid-containing virus infecting the halophilic auryarchaeon Haloarcula hispanica. J Virol 79(14):9097–9107
Bath C, Dyall-Smith ML (1998) His1, an archaeal virus of the Fuselloviridae family that infects Haloarcula hispanica. J Virol 72:9392–9395
Bath C, Cukalac T, Porter K, Dyall-Smith ML (2006) His1 and His2 are distantly related, spindle-shaped haloviruses belonging to the novel virus group, Salterprovirus. Virology 350:228–239
Bettstetter M, Peng X, Garrett RA, Prangishvili D (2003) AFV1, a novel virus infecting hyperthermophilic archaea of the genus Acidianus. Virology 315:68–79
Bird DF, Juniper SK, Ricciardi-Rigault M, Martineu P, Prairie YT, Calvert SE (2001) Subsurface viruses and bacteria in Holocene/Late Pleistocene sediments of Saanich Inlet, BC: ODP Holes 1033B and 1034B, Leg 169S. Mar Geol 174:227–239
Borriss M, Helmke E, Hanschke R, Schweder T (2003) Isolation and characterization of marine psychrophilic phage–host systems from Arctic sea ice. Extremophiles 7:377–384
Breibart M, Rohwer F (2005) Here a virus, there a virus, everywhere the same virus? Trends Microbiol 13:278–284
Breitbart M, Wegley L, Leeds S, Schoenfeld T, Rohwer F (2004) Phage community dynamics in hot springs. Appl Environ Microbiol 70:1633–1640
Bulat S, Alekhina IA, Blot M, Petit JR, de Angelis M, Wagenbach D, Lipenkov VY, Vasilyeva L, Wloch D, Raynaud D, Lukin VV (2004) DNA signature of thermophilic bacteria from the aged accretion ice of Lake Vostok: implications for searching life in extreme icy environments. Int J Astrobiol 1:1–12
Dyall-Smith M, Tang SL, Bath C (2003) Haloarchaeal viruses: how diverse are they? Res Microbiol 154:309–313
Edwards RA, Rohwer F (2005) Viral metagenomics. Nat Rev Microbiol 3:504–510
Evans RD, Johansen JR (1999) Microbiotic crusts and ecosystem processes. Cri Rev Pl Sci 18:182–225
Forterre P (2006) Three RNA cells for ribosomal lineages and three DNa viruses to replicate their genomes: a hypothesis for the origin of cellular domain. Proc Natl Acad Sci USA 103:3669–3674
Fuhrman JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399:541–548
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
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
Gowing MM (2003) Large viruses and infected microeukaryotes in Ross Sea summer pack ice habitats. Mar Biol 142:1029–1040
Gropp F, Palm P, Zillig W (1989) Expression and regulation of Halobacterium halobium phage ϕH genes. Can J Microbiol 35:182–188
Grossi SM, Kottmeier S, Sullivan CW (1984) Sea ice microbial communities. III. Seasonal abundance of microalgae and associated bacteria, McMurdo Sound, Antarctica. Microb Ecol 10:231–242
Guixa-Boixareu N, Calderon-Paz JI, Heldal M, Bratbak G, Pedros-Alio C (1996) Viral lysis and bacterivory as prokaryotic loss factors along a salinity gradient. Aquat Microb Ecol 11:215–227
Häring M, Peng X, Brügger K, Rachel R, Stetter KO, Garrett RA, Prangishvili D (2004) Morphology and genome organization of the virus PSV of the hyperthermophilic archaeal genera Pyrobaculum and Thermoproteus: a novel virus family, the Globuloviridae. Virology 323:233–242
Häring M, Vestergaard G, Rachel R, Chen L, Garrett RA, Prangishvili D (2005a) Independent virus development outside a host. Nature 436:1101–1102
Häring M, Rachel R, Peng X, Garrett RA, Prangishvili D (2005b) Viral diversity in hot springs of Puzzoli, Italy and characterization of a unique archaeal virus, Acidianus bottle-shaped virus, from a new family, the Ampullaviridae. J Virol 79(15):9904–9911
Häring M, Vestergaard G, Brügger K, Rachel R, Garrett RA, Prangishvili D (2005c) Structure and genome organization of AFV2, a novel archaeal Lipothrixvirus with unusual terminal and core structures. J Bact 187(11):3855–3858
Janekovic D, Wunderl S, Holz I, Zillig W, Gierl A, Neumann H (1983) TTV1, TTV2 and TTV3, a family of viruses of the extremely thermophilic, anaerobic sulfur reducing archaebacterium Thermoproteus tenax. Mol Gen Genet 192:39–45
Jiang S, Steward G, Jellison R, Chu W, Choi S (2004) Abundance, distribution and diversity of viruses in alkaline hypersaline Mono Lake, California. Microb Ecol 47:9–17
Khayat R, Tang L, Larson ET, Lawrence CM, Young M, Johnson JE (2005) Structure of an archaeal virus capsid protein reveals a common ancestry to eukaryotic and bacterial viruses. Proc Natl Acad Sci USA 102:1894–1899
Kepner RL, Wharton RA Jr, Suttle CA (1998) Viruses in Antarctic lakes. Limnol Oceanogr 43:1754–1761
Klein R, Baranyi U, Rössler N, Greineder B, Scholz H, Witte A (2002) Natrialba magadii virus ϕCh1: first complete nucleotide sequence and functional organization of a virus infecting a haloalkalophilic archaeon. Mol Microbiol 45:851–863
Kottmeier ST, Grossi SM, Sullivan CW (1987) Sea ice microbial communities. VII. Bacterial production in annual sea ice of Mc Murdo Sound, Antartica. Mar Ecol Prog Ser 35:175–186
Madigan MT, Martinko JM, Parker J (2003) Extremely halophilic Archaea. In: Carlson G, Snavely SL, Wechsler DA, Schiaparelli K (eds) Brock biology of microorganisms, 10th edn. Prentice Hall, USA, pp 448–452
Maranger R, Bird DF, Juniper SK (1994) Viral and bacterial dynamics in Arctic sea ice during the spring algal bloom near Resolute, N.W.T., Canada. Mar Ecol Prog Ser 111:121–127
Martin A, Yeats S, Janekovic D, Reiter W-D, Aicher W, Zillig W (1984) SAV1, a temperate u.-v. inducible DNA virus-like particle from the archaebacterium Sulfolobus acidocaldarius isolate B12. EMBO J 3(9):2165–2168
Nuttall SD, Dyall-Smith ML (1993) HF1 and HF2: novel bacteriophages of halophilic archaea. Virology 197(2):678–684
Oren A, Bratbak G, Heldal M (1997) Occurrence of virus-like particles in the Dead Sea. Extremophiles 1:143–149
Ortmann AC, Suttle CA (2005) High abundances of viruses in deep-sea hydrothermal vent system indicate viral mediated microbial mortality. Deep-sea Res I 52:1515–1527
Palm P, Schleper C, Grampp B, Yeats S, McWilliam P, Reiter W-D, Zillig W (1991) Complete nucleotide sequence of the virus SSV1 of the archaebacterium Sulfolobus shibatae. Virology 185:242–250
Parkes RJ, Cragg BA, Bale SJ, Getliff JM, Goodman K, Rochelle PA, Fry JC, Weightman AJ, Harvey SM (1994) Deep bacterial biosphere in Pacific ocean sediments. Nature 371:410–413
Parkes RJ, Cragg BA, Wellsbury P (2000) Recent studies on bacterial populations and processes in subseafloor sediments: a review. Hydrogeol J 8:11–28
Porter K, Kukkaro P, Bamford JK, Bath C, Kivela HM, Dyall-Smith ML, Bamford DH (2005) SH1: a novel, spherical halovirus isolated from an Australian lake. Virology 335:22–33
Prangishvili D, Arnold HP, Gotz D, Ziese U, Holz I, Kristjansson JK, Zillig W (1999) A novel virus family, the Rudiviridae: structure, virus–host interactions and genome variability of the Sulfolobus viruses SIRV1 and SIRV2. Genetics 152(4):1387–1396
Prangishvili D, Garrett RA (2004) Exceptionally diverse morphotypes and genomes of crenarchaeal hyperthermophilic viruses. Bioch Soc Trans 32:204–208
Prangishvili D, Garrett RA (2005) Viruses of hyperthermophilic Crenarchaea. Trends Microbiol 13:535–542
Prangishvili D, Garrett RA, Koonin EV (2006) Evolutionary genomics of archaeal viruses: unique viral genomes in the third domain of life. Virus Res 117:52–67
Prieur D (1997) Microbiology of deep-sea hydrothermal vents. Trends Biotech 15:242–244
Prigent M, Leroy M, Confalonieri F, Dutertre M, DuBow MS (2005) A diversity of bacteriophage forms and genomes can be isolated from the surface sands of the Sahara Desert. Extremophiles 9:289–296
Rachel R, Bettstetter M, Hedlund BP, Häring M, Kessler A, Stetter KO, Prangishvili P (2002) Remarkable morphological diversity of viruses and virus-like particles in hot terrestrial environments. Arch Virol 147(12):2419–2429
Rice G, Stedman K, Snyder J, Wiedenheft B, Willits D, Brumfield S, McDermott T, Young M (2001) Viruses from extreme thermal environments. Proc Natl Acad Sci USA 98:13341–13345
Rice G, Tang I, Stedman K, Roberto F, Spuhler J, Gillitzer E, Johnson JE, Douglas T, Young M (2004) The structure of a thermophilic archaeal virus shows a double-stranded viral capsid type that spans all domains of life. Proc Natl Acad Sci USA 101:7716–7720
Rohwer F (2003) Global phage diversity. Cell 113:141
Rothschild LJ, Mancinelli RL (2001) Life in extreme environments. Nature 409:1092–1101
Sandaa RA, Skjoldal EF, Bratbak G (2003) Virioplankton community structure along a salinity gradient in a solar saltern. Extremophiles 7:347–351
Schleper C, Kubo K, Zillid W (1992) 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 USA 89:7645–7649
Schnabel H, Schramm E, Schnabel R, Zillig W (1982a) Structural variability in the genome of phage ϕH of Halobacterium halobium. Mol Gen Genet 188:370–377
Schnabel H, Zillig W, Pfäffle M, Schnabel R, Michel H, Delius H (1982b) Halobacterium halobium phage ϕH. EMBO J 1:87–92
Smith REH, Clement P, Cota GF (1989) Population dynamics of bacteria in Arctic sea ice. Microb Ecol 17:63–76
Staley JT, Gosink JJ (1999) Poles apart: biodiversity and biogeography of sea ice bacteria. Ann Rev Microbiol 53:189–215
Stedman KM, She Q, Phan H, Arnold HP, Holz I, Garrett RA, Zillig W (2003) Relationships between fuselloviruses infecting the extremely thermophilic archaeon Sulfolobus: SSV1 and SSV2. Res Microbiol 154:295–302
Stolt P, Zillig W (1992) In vivo studies of the effects of immunity genes on early lytic transcription in the Halobacterium salinarium phage ϕH. Mol Gen Genet 235:197–204
Stolt P, Zillig W (1993) In vivo and in vitro analysis of traznscription of the L region from Halobacterium salinarium phage ϕH: definition of a repressor-enhancing gene. Virology 195:649–658
Stolt P, Zillig W (1994) Gene regulation in halophage phi-H – more than promoters. Syst Apll Microbiol 16:591–596
Suttle CA (2005) Viruses in the sea. Nature 437:356–361
Tang SL, Nuttall S, Ngui K, Fisher C, Lopez P, Dyall-Smith M (2002) HF2: a double-stranded DNA tailed haloarcheal virus with a mosaic genome. Mol Microbiol 44:283–296
Tang S-L, Nuttall S, Dyall-Smith M (2004) Haloviruses HF1 and HF2: evidence for a recent and large recombination event. J Bacteriol 186:2810–2817
Thomas DN, Dieckmann GS (2002) Antarctic sea ice – a habitat for extremophiles. Science 295:641–644
Vestergaard G, Häring M, Peng X, Rachel R, Garrett RA, Prangishvili D (2005) A novel rudivirus, ARV1, of the hyperthermophilic archaeal genus Acidianus. Virology 336:83–92
Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181
Wiedenheft B, Stedman K, Roberto F, Willits D, Gleske A-K, Zoeller L, Snyder J, Douglas T, Young M (2004) Comparative genomic analysis of the hyperthermophilic archaeal Fuselloviridae viruses. J Virol 78(4):1954–1961
Witte A, Baranyi U, Klein R, Sulzner M, Luo C, Wanner G, Krüger DH, Lubitz W (1997) Characterization of Natronobacterium magadii phage ϕCh1, a unique archaeal phage containing DNA and RNA. Mol Microbiol 23(3):603–616
Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Micr Mol Biol Rev 64:69–114
Xiang X, Chen L, Huang X, Luo Y, She Q, Huang L (2005) Sulfolobus tengchongensis spindle-shaped virus STSV1: virus–host interactions and genomic features. J Virol 79:8677–8686
Acknowledgements
Many thanks to the Editorial Board of Reviews in Environment Science and Bio/Technology for the invitation to contribute this review. MLR and DP thank the European Science Foundation for the invitation to the ESF workshop on “Investigating life in extreme environments” in Sant Feliu de Guixols, Spain, November 2005. Two anonymous reviewers provided very constructive suggestions that improve the paper. MG is funded through a PhD grant from the Ministère National de l’Enseignement et de la Recherche.
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Marc Le Romancer and Mélusine Gaillard contributed equally to this work.
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Le Romancer, M., Gaillard, M., Geslin, C. et al. Viruses in extreme environments. Rev Environ Sci Biotechnol 6, 17–31 (2007). https://doi.org/10.1007/s11157-006-0011-2
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DOI: https://doi.org/10.1007/s11157-006-0011-2