Viruses of Haloarchaea

In hypersaline environments, haloarchaea (halophilic members of the Archaea) are the dominant organisms, and the viruses that infect them, haloarchaeoviruses are at least ten times more abundant. Since their discovery in 1974, described haloarchaeoviruses include head-tailed, pleomorphic, spherical and spindle-shaped morphologies, representing Myoviridae, Siphoviridae, Podoviridae, Pleolipoviridae, Sphaerolipoviridae and Fuselloviridae families. This review overviews current knowledge of haloarchaeoviruses, providing information about classification, morphotypes, macromolecules, life cycles, genetic manipulation and gene regulation, and host-virus responses. In so doing, the review incorporates knowledge from laboratory studies of isolated viruses, field-based studies of environmental samples, and both genomic and metagenomic analyses of haloarchaeoviruses. What emerges is that some haloarchaeoviruses possess unique morphological and life cycle properties, while others share features with other viruses (e.g., bacteriophages). Their interactions with hosts influence community structure and evolution of populations that exist in hypersaline environments as diverse as seawater evaporation ponds, to hot desert or Antarctic lakes. The discoveries of their wide-ranging and important roles in the ecology and evolution of hypersaline communities serves as a strong motivator for future investigations of both laboratory-model and environmental systems.

[1]  W. Doolittle,et al.  Phage evolution: New worlds of genomic diversity , 2003, Current Biology.

[2]  L. Paulin,et al.  Related haloarchaeal pleomorphic viruses contain different genome types , 2012, Nucleic acids research.

[3]  Matthew Z. DeMaere,et al.  High level of intergenera gene exchange shapes the evolution of haloarchaea in an isolated Antarctic lake , 2013, Proceedings of the National Academy of Sciences.

[4]  Charles A. Bowman,et al.  Snapshot of haloarchaeal tailed virus genomes , 2013, RNA biology.

[5]  Michael S. Spilman,et al.  Functional domains of the bacteriophage P2 scaffolding protein: identification of residues involved in assembly and protease activity. , 2009, Virology.

[6]  Yuan-ming Luo,et al.  Sulfolobus tengchongensis Spindle-Shaped Virus STSV1: Virus-Host Interactions and Genomic Features , 2005, Journal of Virology.

[7]  W. Doolittle,et al.  Transformation methods for halophilic archaebacteria. , 1989, Canadian journal of microbiology.

[8]  M. Dyall-Smith,et al.  HF1 and HF2: novel bacteriophages of halophilic archaea. , 1993, Virology.

[9]  M. Dyall-Smith,et al.  His1, an Archaeal Virus of theFuselloviridae Family That Infects Haloarcula hispanica , 1998, Journal of Virology.

[10]  I. Wang,et al.  Bacteriophage Adsorption Rate and Optimal Lysis Time , 2008, Genetics.

[11]  H. Schnabel,et al.  Structural variability in the genome of phage ϕH of Halobacterium halobium , 1982, Molecular and General Genetics MGG.

[12]  G. Bratbak,et al.  Viral lysis and bacterivory as prokaryotic loss factors along a salinity gradient , 1996 .

[13]  Shiraz A. Shah,et al.  Archaeal CRISPR-based immune systems: exchangeable functional modules. , 2011, Trends in microbiology.

[14]  D. Oesterhelt,et al.  Isolation of a halobacterial phage with a fully cytosine-methylated genome , 1988, Molecular and General Genetics MGG.

[15]  Harri T Jäälinoja,et al.  Structure and host-cell interaction of SH1, a membrane-containing, halophilic euryarchaeal virus , 2008, Proceedings of the National Academy of Sciences.

[16]  M. Dyall-Smith,et al.  28 The Isolation and Study of Viruses of Halophilic Microorganisms , 2006 .

[17]  E. Casamayor,et al.  Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. , 2002, Environmental microbiology.

[18]  H. Schnabel An immune strain of Halobacterium halobium carries the invertible L segment of phage PhiH as a plasmid. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[19]  D. Stuart,et al.  Structure unifies the viral universe. , 2012, Annual review of biochemistry.

[20]  G. Bertani Transduction-Like Gene Transfer in the MethanogenMethanococcus voltae , 1999, Journal of bacteriology.

[21]  F. Blattner,et al.  Genome of Bacteriophage P1 , 2004, Journal of bacteriology.

[22]  A. Marchfelder,et al.  The immune system of halophilic archaea , 2012, Mobile genetic elements.

[23]  Fernando Santos,et al.  Reconstructing Viral Genomes from the Environment Using Fosmid Clones: The Case of Haloviruses , 2012, PloS one.

[24]  F. Rodríguez-Valera,et al.  Genomic plasticity in prokaryotes: the case of the square haloarchaeon , 2007, The ISME Journal.

[25]  D. Bamford,et al.  Archaeal viruses and bacteriophages: comparisons and contrasts. , 2014, Trends in microbiology.

[26]  J. Antón,et al.  Archaeal Biodiversity in Crystallizer Ponds from a Solar Saltern: Culture versus PCR , 2000, Microbial Ecology.

[27]  H. Ackermann Tailed Bacteriophages: The Order Caudovirales , 1998, Advances in Virus Research.

[28]  R. E. MacDonald,et al.  Salt-dependent bacteriophage infecting Halobacterium cutirubrum and H. halobium , 1975, Nature.

[29]  Pascal Lapierre,et al.  Low Species Barriers in Halophilic Archaea and the Formation of Recombinant Hybrids , 2012, Current Biology.

[30]  U. Baranyi,et al.  The lysogenic region of virus φCh1: identification of a repressor-operator system and determination of its activity in halophilic Archaea , 2007, Extremophiles.

[31]  H. Scholz,et al.  Haloarchaeal myovirus φCh1 harbours a phase variation system for the production of protein variants with distinct cell surface adhesion specificities , 2012, Molecular microbiology.

[32]  H. Scholz,et al.  Inversion within the haloalkaliphilic virus φCh1 DNA results in differential expression of structural proteins , 2004, Molecular microbiology.

[33]  D. Bamford,et al.  Closely Related Archaeal Haloarcula hispanica Icosahedral Viruses HHIV-2 and SH1 Have Nonhomologous Genes Encoding Host Recognition Functions , 2012, Journal of Virology.

[34]  W. Zillig,et al.  In vivo studies on the effects of immunity genes on early lytic transcription in the Halobacterium salinarium phage ϕ H , 1992, Molecular and General Genetics MGG.

[35]  Jacques Nicolas,et al.  CRISPI: a CRISPR interactive database , 2009, Bioinform..

[36]  Nisse Kalkkinen,et al.  An ssDNA virus infecting archaea: a new lineage of viruses with a membrane envelope , 2009, Molecular microbiology.

[37]  H. Schnabel,et al.  Halobacterium halobium phage øH , 1982, The EMBO journal.

[38]  M. Krupovic,et al.  Order to the Viral Universe , 2010, Journal of Virology.

[39]  I. Dundas,et al.  Persisting Phage Infection in Halobacterium salinarium str. 1 , 1980 .

[40]  Pentti Somerharju,et al.  New, Closely Related Haloarchaeal Viral Elements with Different Nucleic Acid Types , 2010, Journal of Virology.

[41]  C. Pauling Bacteriophages of Halobacterium halobium: isolated from fermented fish sauce and primary characterization. , 1982, Canadian journal of microbiology.

[42]  Brian C. Thomas,et al.  Dynamic Viral Populations in Hypersaline Systems as Revealed by Metagenomic Assembly , 2012, Applied and Environmental Microbiology.

[43]  W. Zillig,et al.  Gene Regulation in Halophage ΦH; more than Promoters , 1993 .

[44]  T. Allers,et al.  Archaeal genetics — the third way , 2005, Nature Reviews Genetics.

[45]  J. Bamford,et al.  Viruses and Life: Can There Be One Without the Other? , 2010 .

[46]  R. Barrangou,et al.  CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. , 2011, Annual review of genetics.

[47]  Prokaryote viruses studied by electron microscopy , 2012, Archives of Virology.

[48]  G. Bratbak,et al.  Occurrence of virus-like particles in the Dead Sea , 1997, Extremophiles.

[49]  I. Dundas,et al.  Bacteriophage of Halobacterium salinarium , 1974, Nature.

[50]  Zhiwei Zhao,et al.  Genome Sequence of Halorubrum sp. Strain T3, an Extremely Halophilic Archaeon Harboring a Virus-Like Element , 2012, Journal of bacteriology.

[51]  J. Banfield,et al.  De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities , 2011, The ISME Journal.

[52]  P. Laurinmäki,et al.  Structure of the archaeal head-tailed virus HSTV-1 completes the HK97 fold story , 2013, Proceedings of the National Academy of Sciences.

[53]  M. Dyall-Smith,et al.  The transcription programme of the protein-primed halovirus SH1. , 2008, Microbiology.

[54]  A. Oren,et al.  Halobacterium salinarum nom. corrig., a Name To Replace Halobacterium salinarium (Elazari-Volcani) and To Include Halobacterium halobium and Halobacterium cutirubrum , 1996 .

[55]  Philippe Horvath,et al.  The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA , 2010, Nature.

[56]  Paul Grayson,et al.  Real-time observations of single bacteriophage λ DNA ejections in vitro , 2007, Proceedings of the National Academy of Sciences.

[57]  W. Lubitz,et al.  Characterization of Natronobacterium magadii phage ΦCh1, a unique archaeal phage containing DNA and RNA , 1997, Molecular microbiology.

[58]  P. Laurinmäki,et al.  Insights into Head-Tailed Viruses Infecting Extremely Halophilic Archaea , 2013, Journal of Virology.

[59]  Sen-Lin Tang,et al.  Haloarchaeal viruses: how diverse are they? , 2003, Research in microbiology.

[60]  J. Maniloff,et al.  Identification of an enveloped phage, mycoplasma virus L172, that contains a 14-kilobase single-stranded DNA genome , 1985, Journal of virology.

[61]  E. Roine,et al.  Quantitative dissociation of archaeal virus SH1 reveals distinct capsid proteins and a lipid core. , 2006, Virology.

[62]  H. Scholz,et al.  Natrialba magadii virus φCh1: first complete nucleotide sequence and functional organization of a virus infecting a haloalkaliphilic archaeon , 2002, Molecular microbiology.

[63]  D. Bamford,et al.  Virus-host interactions in environments with a wide range of ionic strengths. , 2009, Environmental microbiology reports.

[64]  J. Antón,et al.  The metavirome of a hypersaline environment. , 2010, Environmental microbiology.

[65]  J. Banfield,et al.  Virus-Host and CRISPR Dynamics in Archaea-Dominated Hypersaline Lake Tyrrell, Victoria, Australia , 2013, Archaea.

[66]  Friedhelm Pfeiffer,et al.  An Archaeal Immune System Can Detect Multiple Protospacer Adjacent Motifs (PAMs) to Target Invader DNA* , 2012, The Journal of Biological Chemistry.

[67]  Shiraz A Shah,et al.  CRISPR adaptive immune systems of Archaea , 2014, RNA biology.

[68]  E. Roine,et al.  Global network of specific virus-host interactions in hypersaline environments. , 2012, Environmental microbiology.

[69]  Restriction and modification of Halophage S45 inHalobacterium , 1984, Current Microbiology.

[70]  J. Antón,et al.  Metatranscriptomic analysis of extremely halophilic viral communities , 2011, The ISME Journal.

[71]  R. Rachel,et al.  Alternative flagellar filament types in the haloarchaeon Haloarcula marismortui. , 2008, Canadian journal of microbiology.

[72]  Roger W. Hendrix,et al.  Length determination in bacteriophage lambda tails , 1984, Cell.

[73]  Larry L. Daniels,et al.  Ecophysiology of Bacteriophage S5100 Infecting Halobacterium cutirubrum , 1990, Applied and environmental microbiology.

[74]  J. Bamford,et al.  A Unique Group of Virus-Related, Genome-Integrating Elements Found Solely in the Bacterial Family Thermaceae and the Archaeal Family Halobacteriaceae , 2010, Journal of bacteriology.

[75]  O. Kandler,et al.  Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[76]  M. Dyall-Smith,et al.  Virus-host interactions in salt lakes. , 2007, Current opinion in microbiology.

[77]  R. Terns,et al.  CRISPR-based adaptive immune systems. , 2011, Current opinion in microbiology.

[78]  J. Antón,et al.  Virioplankton Community Structure in Tunisian Solar Salterns , 2012, Applied and Environmental Microbiology.

[79]  O. Zhaxybayeva,et al.  Gene transfer agents: phage-like elements of genetic exchange , 2012, Nature Reviews Microbiology.

[80]  R. Garrett,et al.  Chaperone Role for Proteins p618 and p892 in the Extracellular Tail Development of Acidianus Two-Tailed Virus , 2011, Journal of Virology.

[81]  P. Forterre,et al.  The archeoviruses. , 2011, FEMS microbiology reviews.

[82]  E. Roine,et al.  A Glimpse of the genomic diversity of haloarchaeal tailed viruses , 2014, Front. Microbiol..

[83]  D. Prangishvili The wonderful world of archaeal viruses. , 2013, Annual review of microbiology.

[84]  E. Roine,et al.  The Single-Stranded DNA Genome of Novel Archaeal Virus Halorubrum Pleomorphic Virus 1 Is Enclosed in the Envelope Decorated with Glycoprotein Spikes , 2009, Journal of Virology.

[85]  R. Garrett,et al.  Virology: Independent virus development outside a host , 2005, Nature.

[86]  P. Forterre,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. , 2010, Journal of molecular biology.

[87]  D. Bamford,et al.  Virion Architecture Unifies Globally Distributed Pleolipoviruses Infecting Halophilic Archaea , 2012, Journal of Virology.

[88]  W. Zillig,et al.  Antisense RNA mediates transcriptional processing in an archaebacterium, indicating a novel kind of RNase activity , 1993, Molecular Microbiology.

[89]  R. Cavicchioli Extremophiles and the search for extraterrestrial life. , 2002, Astrobiology.

[90]  A. Simpson,et al.  Halocafeteria seosinensis gen. et sp. nov. (Bicosoecida), a halophilic bacterivorous nanoflagellate isolated from a solar saltern , 2006, Extremophiles.

[91]  R. Hendrix Bacteriophage HK97: assembly of the capsid and evolutionary connections. , 2005, Advances in virus research.

[92]  Ibtissem Grissa,et al.  The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats , 2007, BMC Bioinformatics.

[93]  W. Zillig,et al.  Transcription of the halophage ΦH repressor gene is abolished by transcription from an inversely oriented lytic promoter , 1994, FEBS letters.

[94]  R. Sanjuán,et al.  Viral Mutation Rates , 2010, Journal of Virology.

[95]  Aidan C. Parte,et al.  LPSN—list of prokaryotic names with standing in nomenclature , 2013, Nucleic Acids Res..

[96]  A. Marchfelder,et al.  The ring of confidence: a haloarchaeal CRISPR/Cas system. , 2013, Biochemical Society transactions.

[97]  M. Krupovic,et al.  Virus evolution: how far does the double β-barrel viral lineage extend? , 2008, Nature Reviews Microbiology.

[98]  A. Spang,et al.  A thaumarchaeal provirus testifies for an ancient association of tailed viruses with archaea. , 2011, Biochemical Society transactions.

[99]  G. Rohrmann,et al.  Bacteriophages of Halobacterium halobium: virion DNAs and proteins. , 1983, Canadian journal of microbiology.

[100]  P. Forterre,et al.  Unification of the Globally Distributed Spindle-Shaped Viruses of the Archaea , 2013, Journal of Virology.

[101]  A. Oren,et al.  Diversity of halophilic microorganisms: Environments, phylogeny, physiology, and applications , 2002, Journal of Industrial Microbiology and Biotechnology.

[102]  Stan J. J. Brouns,et al.  Clustered regularly interspaced short palindromic repeats (CRISPRs): the hallmark of an ingenious antiviral defense mechanism in prokaryotes , 2011, Biological chemistry.

[103]  R. Garrett,et al.  Viruses of the Archaea: a unifying view , 2006, Nature Reviews Microbiology.

[104]  R. Garrett,et al.  Viruses of hyperthermophilic Crenarchaea. , 2005, Trends in microbiology.

[105]  Y. Liu,et al.  Temperate membrane-containing halophilic archaeal virus SNJ1 has a circular dsDNA genome identical to that of plasmid pHH205. , 2012, Virology.

[106]  M. Dyall-Smith,et al.  Constituents of SH1, a Novel Lipid-Containing Virus Infecting the Halophilic Euryarchaeon Haloarcula hispanica , 2005, Journal of Virology.

[107]  R. Barrangou,et al.  CRISPR Provides Acquired Resistance Against Viruses in Prokaryotes , 2007, Science.

[108]  D. Bamford,et al.  Modified coat protein forms the flexible spindle-shaped virion of haloarchaeal virus His1. , 2013, Environmental microbiology.

[109]  F. Pfeifer,et al.  Transformation of Halobacterium halobium: development of vectors and investigation of gas vesicle synthesis. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[110]  Ricardo Cavicchioli,et al.  Archaea — timeline of the third domain , 2011, Nature Reviews Microbiology.

[111]  Sen-Lin Tang,et al.  Haloviruses HF1 and HF2: Evidence for a Recent and Large Recombination Event , 2004, Journal of bacteriology.

[112]  S. Schuster,et al.  Haloquadratum walsbyi : Limited Diversity in a Global Pond , 2011, PloS one.

[113]  Jong Soo Park,et al.  Active flagellates grazing on prokaryotes in high salinity waters of a solar saltern , 2003 .

[114]  Y. Bettarel,et al.  Ecological traits of planktonic viruses and prokaryotes along a full-salinity gradient. , 2011, FEMS microbiology ecology.

[115]  B. Jones,et al.  Sequence analysis of an Archaeal virus isolated from a hypersaline lake in Inner Mongolia, China , 2007, BMC Genomics.

[116]  Molecular characterization of pHRDV1, a new virus-like mobile genetic element closely related to pleomorphic viruses in haloarchaea , 2014, Extremophiles.

[117]  M. Krupovic,et al.  Gammasphaerolipovirus, a newly proposed bacteriophage genus, unifies viruses of halophilic archaea and thermophilic bacteria within the novel family Sphaerolipoviridae , 2014, Archives of Virology.

[118]  E. Koonin,et al.  Is evolution Darwinian or/and Lamarckian? , 2009, Biology Direct.

[119]  D. Stuart,et al.  What does structure tell us about virus evolution? , 2005, Current opinion in structural biology.

[120]  D. Bamford,et al.  The Closest Relatives of Icosahedral Viruses of Thermophilic Bacteria Are among Viruses and Plasmids of the Halophilic Archaea , 2009, Journal of Virology.

[121]  R. Amann,et al.  Metagenomic approach to the study of halophages: the environmental halophage 1. , 2007, Environmental microbiology.

[122]  D. Bamford Do viruses form lineages across different domains of life? , 2003, Research in microbiology.

[123]  R. Stepanauskas,et al.  Cell sorting analysis of geographically separated hypersaline environments , 2013, Extremophiles.

[124]  H. Xiang,et al.  Characterization of CRISPR RNA Biogenesis and Cas6 Cleavage-Mediated Inhibition of a Provirus in the Haloarchaeon Haloferax mediterranei , 2012, Journal of bacteriology.

[125]  W. Doolittle,et al.  Efficient transfection of the archaebacterium Halobacterium halobium , 1987, Journal of bacteriology.

[126]  P. Shen,et al.  Induction and preliminary characterization of a novel halophage SNJ1 from lysogenic Natrinema sp. F5. , 2007, Canadian journal of microbiology.

[127]  B. Rodriguez-Mueller,et al.  Metagenomic islands of hyperhalophiles: the case of Salinibacter ruber , 2009, BMC Genomics.

[128]  E. Roine,et al.  Lipids of Archaeal Viruses , 2012, Archaea.

[129]  E. Hæggström,et al.  DNA ejection from an archaeal virus--a single-molecule approach. , 2013, Biophysical journal.

[130]  M. Dyall-Smith,et al.  Halophage HF2: genome organization and replication strategy , 1995, Journal of virology.

[131]  Shiraz A. Shah,et al.  A novel single-tailed fusiform Sulfolobus virus STSV2 infecting model Sulfolobus species , 2013, Extremophiles.

[132]  R. M. Burnett,et al.  Does common architecture reveal a viral lineage spanning all three domains of life? , 2004, Molecular cell.

[133]  Philippe Horvath,et al.  Phage Response to CRISPR-Encoded Resistance in Streptococcus thermophilus , 2007, Journal of bacteriology.

[134]  J. Oost,et al.  Unravelling the structural and mechanistic basis of CRISPR–Cas systems , 2014, Nature Reviews Microbiology.

[135]  In vivo and in vitro analysis of transcription of the L region from the Halobacterium salinarium phage phi H: definition of a repressor-enhancing gene. , 1993, Virology.

[136]  Sen-Lin Tang,et al.  PH1: An Archaeovirus of Haloarcula hispanica Related to SH1 and HHIV-2 , 2013, Archaea.

[137]  Matthew S. Fullmer,et al.  Population and genomic analysis of the genus Halorubrum , 2014, Front. Microbiol..

[138]  M. Dyall-Smith,et al.  His1 and His2 are distantly related, spindle-shaped haloviruses belonging to the novel virus group, Salterprovirus. , 2006, Virology.

[139]  P. Laurinmäki,et al.  Biochemical and structural characterisation of membrane-containing icosahedral dsDNA bacteriophages infecting thermophilic Thermus thermophilus. , 2008, Virology.

[140]  J. Peter Gogarten,et al.  Quantifying Homologous Replacement of Loci between Haloarchaeal Species , 2012, Genome biology and evolution.

[141]  R. Stepanauskas,et al.  New Abundant Microbial Groups in Aquatic Hypersaline Environments , 2011, Scientific reports.

[142]  M. Dyall-Smith,et al.  SH1: A novel, spherical halovirus isolated from an Australian hypersaline lake. , 2005, Virology.

[143]  Shiladitya DasSarma,et al.  Extreme Halophiles Are Models for Astrobiology , 2006 .

[144]  W. Zillig,et al.  Expression and regulation of Halobacterium halobium phage ΦH genes , 1989 .

[145]  Sen-Lin Tang,et al.  HF2: a double‐stranded DNA tailed haloarchaeal virus with a mosaic genome , 2002, Molecular microbiology.

[146]  M. Dyall-Smith,et al.  Transfection of haloarchaea by the DNAs of spindle and round haloviruses and the use of transposon mutagenesis to identify non‐essential regions , 2008, Molecular microbiology.

[147]  P. Forterre,et al.  Diversity of virus-host systems in hypersaline Lake Retba, Senegal. , 2011, Environmental microbiology.

[148]  W. Jacobs,et al.  Origins of Highly Mosaic Mycobacteriophage Genomes , 2003, Cell.