All Title Author
Keywords Abstract

Archaea  2012 

Lipids of Archaeal Viruses

DOI: 10.1155/2012/384919

Full-Text   Cite this paper   Add to My Lib


Archaeal viruses represent one of the least known territory of the viral universe and even less is known about their lipids. Based on the current knowledge, however, it seems that, as in other viruses, archaeal viral lipids are mostly incorporated into membranes that reside either as outer envelopes or membranes inside an icosahedral capsid. Mechanisms for the membrane acquisition seem to be similar to those of viruses infecting other host organisms. There are indications that also some proteins of archaeal viruses are lipid modified. Further studies on the characterization of lipids in archaeal viruses as well as on their role in virion assembly and infectivity require not only highly purified viral material but also, for example, constant evaluation of the adaptability of emerging technologies for their analysis. Biological membranes contain proteins and membranes of archaeal viruses are not an exception. Archaeal viruses as relatively simple systems can be used as excellent tools for studying the lipid protein interactions in archaeal membranes. 1. Introduction Viruses are obligate parasites. Their hallmark is the virion, an infectious particle made of proteins and encapsidating the viral genome. Many viruses, however, also contain lipids as essential components of the virion [1]. The majority of viral lipids are found in membranes, but viral proteins can also be modified with lipids [2, 3]. 1.1. Membrane Containing Viruses in the Viral Universe Membrane containing viruses can roughly be divided into two subclasses [1]. The first subclass contains viruses in which the membrane, also called an envelope, is the outermost layer of the viral particle. In the second class of viruses, the membrane is underneath the usually icosahedral protein capsid. Few viruses contain both the inner membrane as well as an envelope [1]. Lipid membranes of viruses have evolved into essential components of virions that in many cases seem to be involved in the initial stages of infection [4–6]. The majority of membrane containing viruses infect animals both vertebrate and invertebrate that do not have a cell wall surrounding the cytoplasmic membrane. For other host organisms such as plants and prokaryotes there are much fewer membrane containing viruses known [1]. Usually the cells of these organisms are covered with a cell wall. By far the majority of known viruses that infect prokaryotes, that is, bacteria (bacteriophages), and archaea (archaeal viruses) belong to the order Caudovirales, the tailed viruses (Figure 1) [1, 7]. These viruses are made of the icosahedrally


[1]  A. M. Q. King, M. J. Adams, E. B. Carstens, and E. J. Lefkowitz, Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses, Elsevier, Oxford, UK, 2011.
[2]  J. Eichler and M. W. W. Adams, “Posttranslational protein modification in Archaea,” Microbiology and Molecular Biology Reviews, vol. 69, no. 3, pp. 393–425, 2005.
[3]  D. E. Hruby and C. A. Franke, “Viral acylproteins: greasing the wheels of assembly,” Trends in Microbiology, vol. 1, no. 1, pp. 20–25, 1993.
[4]  M. M. Poranen, R. Daugelavi?ius, and D. H. Bamford, “Common principles in viral entry,” Annual Review of Microbiology, vol. 56, pp. 521–538, 2002.
[5]  A. E. Smith and A. Helenius, “How viruses enter animal cells,” Science, vol. 304, no. 5668, pp. 237–242, 2004.
[6]  H. M. Oksanen, M. M. Poranen, and D. H. Bamford, “Bacteriophages: lipid-containing,” in Encyclopedia of Life Sciences (ELS), John Wiley & Sons, Chichester, UK, 2010.
[7]  H. W. Ackermann, “5500 Phages examined in the electron microscope,” Archives of Virology, vol. 152, no. 2, pp. 227–243, 2007.
[8]  B. L. Soloff, T. A. Rado, B. E. Henry II, and J. H. Bates, “Biochemical and morphological characterization of mycobacteriophage R1,” Journal of Virology, vol. 25, no. 1, pp. 253–262, 1978.
[9]  M. L. Gope and K. P. Gopinathan, “Presence of lipids in mycobacteriophage I3,” Journal of General Virology, vol. 59, no. 1, pp. 131–138, 1982.
[10]  M. K. Pietil?, N. S. Atanasova, V. Manole et al., “Virion architecture unifies globally distributed pleolipoviruses infecting halophilic Archaea,” Journal of Virology, vol. 86, no. 9, pp. 5067–5079, 2012.
[11]  J. M. Claverie, C. Abergel, and H. Ogata, “Mimivirus,” in Current Topics in Microbiology and Immunology, J. L. Van Etten, Ed., vol. 328, pp. 89–121, 2009.
[12]  W. H. Wilson, J. L. Van Etten, and M. J. Allen, “The Phycodnaviridae: the story how tiny giants rule the world,” in Current Topics in Microbiology and Immunology, J. L. Van Etten, Ed., pp. 1–42, 2009.
[13]  G. J. Brewer, “Control of membrane morphogenesis in bacteriophage,” International Review of Cytology, vol. 68, pp. 53–96, 1980.
[14]  S. Laurinavi?ius, Phospholipids of lipid-containing bacteriophages and their transbilayer distribution. [Ph.D. thesis], University of Helsinki, Helsinki, Finland, 2008.
[15]  H. Garoff, R. Hewson, and D. J. E. Opstelten, “Virus maturation by budding,” Microbiology and Molecular Biology Reviews, vol. 62, no. 4, pp. 1171–1190, 1998.
[16]  L. Mindich, D. Bamford, T. McGraw, and G. Mackenzie, “Assembly of bacteriophage PRD1: particle formation with wild-type and mutant viruses,” Journal of Virology, vol. 44, no. 3, pp. 1021–1030, 1982.
[17]  D. H. Bamford, J. Caldentey, and J. K. Bamford, “Bacteriophage PRD1: a broad host range dsDNA tectivirus with an internal membrane,” Advances in Virus Research, vol. 45, pp. 281–319, 1995.
[18]  P. S. Rydman, J. K. H. Bamford, and D. H. Bamford, “A minor capsid protein P30 is essential for bacteriophage PRD1 capsid assembly,” Journal of Molecular Biology, vol. 313, no. 4, pp. 785–795, 2001.
[19]  A. K. Vidaver, R. K. Koski, and J. L. Van Etten, “Bacteriophage ?6: a lipid containing virus of Pseudomonas phaseolicola,” Journal of Virology, vol. 11, no. 5, pp. 799–805, 1973.
[20]  L. Mindich and J. Lehman, “Cell wall lysin as a component of the bacteriophage ?6 virion,” Journal of Virology, vol. 30, no. 2, pp. 489–496, 1979.
[21]  K. H. Lundstr?m, D. H. Bamford, E. T. Palva, and K. Lounatmaa, “Lipid-containing bacteriophage PR4: structure and life cycle,” Journal of General Virology, vol. 43, no. 3, pp. 583–592, 1979.
[22]  D. Bamford and L. Mindich, “Structure of the lipid-containing bacteriophage PRD1: disruption of wild-type and nonsense mutant phage particles with guanidine hydrochloride,” Journal of Virology, vol. 44, no. 3, pp. 1031–1038, 1982.
[23]  A. M. Grahn, R. Daugelavi?ius, and D. H. Bamford, “Sequential model of phage PRD1 DNA delivery: active involvement of the viral membrane,” Molecular Microbiology, vol. 46, no. 5, pp. 1199–1209, 2002.
[24]  H. M. Kivel?, R. Daugelavi?ius, R. H. Hankkio, J. K. H. Bamford, and D. H. Bamford, “Penetration of membrane-containing double-stranded-DNA bacteriophage PM2 into Pseudoalteromonas hosts,” Journal of Bacteriology, vol. 186, no. 16, pp. 5342–5354, 2004.
[25]  R. Khayat, L. Tang, E. T. Larson, C. M. Lawrence, M. Young, and J. E. Johnson, “Structure of an archaeal virus capsid protein reveals a common ancestry to eukaryotic and bacterial viruses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 52, pp. 18944–18949, 2005.
[26]  N. G. Abrescia, J. M. Grimes, H. M. Kivel? et al., “Insights into virus evolution and membrane biogenesis from the structure of the marine lipid-containing bacteriophage PM2,” Molecular cell, vol. 31, no. 5, pp. 749–761, 2008.
[27]  S. T. Jaatinen, L. J. Happonen, P. Laurinm?ki, S. J. Butcher, and D. H. Bamford, “Biochemical and structural characterisation of membrane-containing icosahedral dsDNA bacteriophages infecting thermophilic Thermus thermophilus,” Virology, vol. 379, no. 1, pp. 10–19, 2008.
[28]  H. T. J??linoja, E. Roine, P. Laurinm?ki, H. M. Kivel?, D. H. Bamford, and S. J. Butcher, “Structure and host-cell interaction of SH1, a membrane-containing, halophilic euryarchaeal virus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 23, pp. 8008–8013, 2008.
[29]  V. Cvirkait?-Krupovi?, M. Krupovi?, R. Daugelavi?ius, and D. H. Bamford, “Calcium ion-dependent entry of the membrane-containing bacteriophage PM2 into its Pseudoalteromonas host,” Virology, vol. 405, no. 1, pp. 120–128, 2010.
[30]  R. Khayat, C. Y. Fu, A. C. Ortmann, M. J. Young, and J. E. Johnson, “The architecture and chemical stability of the archaeal Sulfolobus turreted icosahedral virus,” Journal of Virology, vol. 84, no. 18, pp. 9575–9583, 2010.
[31]  C. Y. Fu, K. Wang, L. Gan et al., “In vivo assembly of an archaeal virus studied with whole-cell electron cryotomography,” Structure, vol. 18, no. 12, pp. 1579–1586, 2010.
[32]  P. Kukkaro and D. H. Bamford, “Virus-host interactions in environments with a wide range of ionic strengths,” Environmental Microbiology Reports, vol. 1, no. 1, pp. 71–77, 2009.
[33]  K. Porter, P. Kukkaro, J. K. H. Bamford et al., “SH1: a novel, spherical halovirus isolated from an Australian hypersaline lake,” Virology, vol. 335, no. 1, pp. 22–33, 2005.
[34]  M. K. Pietil?, E. Roine, L. Paulin, N. Kalkkinen, and D. H. Bamford, “An ssDNA virus infecting Archaea: a new lineage of viruses with a membrane envelope,” Molecular Microbiology, vol. 72, no. 2, pp. 307–319, 2009.
[35]  M. L. Dyall-Smith, “Genus Salterprovirus,” in Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses, A. M. Q. King, M. J. Adams, E. B. Carstens, and E. J. Lefkowitz, Eds., pp. 183–186, ElsevierOxford, UK, 2011.
[36]  E. Roine, P. Kukkaro, L. Paulin et al., “New, closely related haloarchaeal viral elements with different nucleic acid types,” Journal of Virology, vol. 84, no. 7, pp. 3682–3689, 2010.
[37]  J. P. Prat, J. N. Lamy, and J. D. Weill, “Staining of lipoproteins after electrophoresis in polyacrylamide gel,” Bulletin de la Société de Chimie Biologique, vol. 51, no. 9, article 1367, 1969.
[38]  A. Corcelli and S. Lobasso, “Characterization of lipids of halophilic Archaea,” in Methods in Microbiology: Extremophiles, F. A. Rainey and A. Oren, Eds., vol. 35, pp. 585–613, Elsevier, New York, NY, USA, 2006.
[39]  M. S. da Costa, M. F. Nobre, and R. Wait, “Analysis of lipids from extremophilic bacteria,” in Methods in Microbiology: Extremophiles, F. A. Rainey and A. Oren, Eds., vol. 35, pp. 127–159, Elsevier, New York, NY, USA, 2006.
[40]  D. H. Bamford, J. J. Ravantti, G. R?nnholm et al., “Constituents of SH1, a novel lipid-containing virus infecting the halophilic euryarchaeon Haloarcula hispanica,” Journal of Virology, vol. 79, no. 14, pp. 9097–9107, 2005.
[41]  M. K. Pietil?, S. Laurinavi?ius, J. Sund, E. Roine, and D. H. Bamford, “The single-stranded DNA genome of novel archaeal virus Halorubrum pleomorphic virus 1 is enclosed in the envelope decorated with glycoprotein spikes,” Journal of Virology, vol. 84, no. 2, pp. 788–798, 2010.
[42]  H. M. Kivel?, E. Roine, P. Kukkaro, S. Laurinavi?ius, P. Somerharju, and D. H. Bamford, “Quantitative dissociation of archaeal virus SH1 reveals distinct capsid proteins and a lipid core,” Virology, vol. 356, no. 1-2, pp. 4–11, 2006.
[43]  M. Kates, “The phytanyl ether-linked polar lipids and isoprenoid neutral lipids of extremely halophilic bacteria,” Progress in the Chemistry of Fats and Other Lipids, vol. 15, no. 4, pp. 301–342, 1977.
[44]  G. D. Sprott, “Structures of archaebacterial membrane lipids,” Journal of Bioenergetics and Biomembranes, vol. 24, no. 6, pp. 555–566, 1992.
[45]  S. V. Albers, W. N. Konings, and A. J. M. Driessen, “Membranes of thermophiles and other extremophiles,” in Methods in Microbiology: Extremophiles, F. A. Rainey and A. Oren, Eds., vol. 35, pp. 161–171, Elsevier, New York, NY, USA, 2006.
[46]  Y. Boucher, “Lipids: biosynthesis, function, and evolution,” in Archaea: Molecular and Cellular Biology, R. Cavicchioli, Ed., pp. 341–353, ASM Press, Washington, DC, USA, 2007.
[47]  A. Gliozzi, R. Rolandi, M. de Rosa, and A. Gambacorta, “Monolayer black membranes from bipolar lipids of archaebacteria and their temperature-induced structural changes,” The Journal of Membrane Biology, vol. 75, no. 1, pp. 45–56, 1983.
[48]  B. Nicolaus, A. Trincone, E. Esposito, M. R. Vaccaro, A. Gambacorta, and M. de Rosa, “Calditol tetraether lipids of the archaebacterium Sulfolobus solfataricus. Biosynthetic studies,” Biochemical Journal, vol. 266, no. 3, pp. 785–791, 1990.
[49]  A. Corcelli, “The cardiolipin analogues of Archaea,” Biochimica et Biophysica Acta, vol. 1788, no. 10, pp. 2101–2106, 2009.
[50]  M. H?ring, X. Peng, K. Brügger 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, vol. 323, no. 2, pp. 233–242, 2004.
[51]  M. Rettenberger, Das Virus TTV1 des extreme thermophilen Schwefel-Archaebacteriums Thermoproteus tenax: Zusammensetzung und Structur [Ph.D. thesis], Ludwig-Maximillians-Universit?t, Munich, Germany, 1990.
[52]  D. Janekovic, S. Wunderl, and I. Holz, “TTV1, TTV2 and TTV3, a family of viruses of the extremely thermophilic, anaerobic, sulfur reducing archaebacterium Thermoproteus tenax,” Molecular and General Genetics, vol. 192, no. 1-2, pp. 39–45, 1983.
[53]  M. Bettstetter, X. Peng, R. A. Garrett, and D. Prangishvili, “AFV1, a novel virus infecting hyperthermophilic Archaea of the genus Acidianus,” Virology, vol. 315, no. 1, pp. 68–79, 2003.
[54]  H. P. Arnold, W. Zillig, U. Ziese et al., “A novel lipothrixvirus, SIFV, of the extremely thermophilic crenarchaeon Sulfolobus,” Virology, vol. 267, no. 2, pp. 252–266, 2000.
[55]  C. Bath, T. Cukalac, K. Porter, and M. L. Dyall-Smith, “His1 and His2 are distantly related, spindle-shaped haloviruses belonging to the novel virus group, Salterprovirus,” Virology, vol. 350, no. 1, pp. 228–239, 2006.
[56]  N. S. Atanasova, E. Roine, A. Oren, D. H. Bamford, and H. M. Oksanen, “Global network of specific virus-host interactions in hypersaline environments,” Environmental Microbiology, vol. 14, no. 2, pp. 426–440, 2012.
[57]  G. Rice, L. Tang, K. Stedman et al., “The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 20, pp. 7716–7720, 2004.
[58]  L. J. Happonen, P. Redder, X. Peng, L. J. Reigstad, D. Prangishvili, and S. J. Butcher, “Familial relationships in hyperthermo- and acidophilic archaeal viruses,” Journal of Virology, vol. 84, no. 9, pp. 4747–4754, 2010.
[59]  X. Xiang, L. Chen, X. Huang, Y. Luo, Q. She, and L. Huang, “Sulfolobus tengchongensis spindle-shaped virus STSV1: virus-host interactions and genomic features,” Journal of Virology, vol. 79, no. 14, pp. 8677–8686, 2005.
[60]  H. Sagami, A. Kikuchi, K. Ogura, K. Fushihara, and T. Nishino, “Novel isoprenoid modified proteins in Halobacteria,” Biochemical and Biophysical Research Communications, vol. 203, no. 2, pp. 972–978, 1994.
[61]  H. Sagami, A. Kikuchi, and K. Ogura, “A novel type of protein modification by isoprenoid-derived materials. Diphytanylglycerylated proteins in Halobacteria,” The Journal of Biological Chemistry, vol. 270, no. 25, pp. 14851–14854, 1995.
[62]  Z. Konrad and J. Eichler, “Lipid modification of proteins in Archaea: attachment of a mevalonic acid-based lipid moiety to the surface-layer glycoprotein of Haloferax volcanii follows protein translocation,” Biochemical Journal, vol. 366, no. 3, pp. 959–964, 2002.
[63]  M. H?ring, R. Rachel, X. Peng, R. A. Garrett, and D. Prangishvili, “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,” Journal of Virology, vol. 79, no. 15, pp. 9904–9911, 2005.
[64]  S. Paula, A. G. Volkov, A. N. Van Hoek, T. H. Haines, and D. W. Deamer, “Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness,” Biophysical Journal, vol. 70, no. 1, pp. 339–348, 1996.
[65]  Y. Zhai, P. L. Chong, L. J. Taylor et al., “Physical properties of archaeal tetraether lipid membranes as revealed by differential scanning and pressure perturbation calorimetry, molecular acoustics, and neutron reflectometry: effects of pressure and cell growth temperature,” Langmuir, vol. 28, no. 11, pp. 5211–5217, 2012.
[66]  W. D. Reiter, W. Zillig, and P. Palm, “Archaebacterial viruses,” Advances in Virus Research, vol. 34, pp. 143–188, 1988.
[67]  D. Prangishvili, “Family Fuselloviridae,” in Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses, A. M. Q. King, M. J. Adams, E. B. Carstens, and E. J. Lefkowitz, Eds., pp. 183–186, Elsevier, Oxford, UK, 2011.
[68]  D. Prangishvili, “Family Lipothrixviridae,” in Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses, A. M. Q. King, M. J. Adams, E. B. Carstens, and E. J. Lefkowitz, Eds., pp. 211–221, Elsevier, Oxford, UK, 2011.
[69]  M. H?ring, G. Vestergaard, K. Brügger, R. Rachel, R. A. Garrett, and D. Prangishvili, “Structure and genome organization of AFV2, a novel archaeal lipothrixvirus with unusual terminal and core structures,” Journal of Bacteriology, vol. 187, no. 11, pp. 3855–3858, 2005.
[70]  W. S. A. Maaty, A. C. Ortmann, M. Dlaki? 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,” Journal of Virology, vol. 80, no. 15, pp. 7625–7635, 2006.
[71]  C. Y. Fu and J. E. Johnson, “Structure and cell biology of archaeal virus STIV,” Current Opinion in Virology, vol. 2, no. 2, pp. 122–127, 2012.
[72]  S. T. Jaakkola, R. K. Penttinen, S. T. Vilén et al., “Closely related archaeal Haloarcula hispanica icosahedral viruses HHIV-2 and SH1 have nonhomologous genes encoding host recognition functions,” Journal of Virology, vol. 86, no. 9, pp. 4734–4742, 2012.
[73]  E. Roine and H. M. Oksanen, “Viruses from the hypersaline environment,” in Halophiles and Hypersaline Environments: Current Research and Future Trends, Ventosa, A. Oren, and Y. Ma, Eds., pp. 153–172, Springer, Berlin, Germany, 2011.
[74]  J. J. B. Cockburn, N. G. A. Abrescia, J. M. Grimes et al., “Membrane structure and interactions with protein and DNA in bacteriophage PRD1,” Nature, vol. 432, no. 7013, pp. 122–125, 2004.
[75]  A. Sen?ilo, L. Paulin, S. Kellner, M. Helm, and E. Roine, “Related haloarchaeal pleomorphic viruses contain different genome types,” Nucleic Acids Research, vol. 40, no. 12, pp. 5523–5534, 2012.
[76]  L. Kandiba, O. Aitio, J. Helin et al., “Diversity in prokaryotic glycosylation: an archaeal-derived N-linked glycan contains legionaminic acid,” Molecular Microbiology, vol. 84, no. 3, pp. 578–593, 2012.
[77]  R. Montalvo-Rodríguez, R. H. Vreeland, A. Oren, M. Kessel, C. Betancourt, and J. López-Garriga, “Halogeometricum borinquense gen. nov., sp. nov., a novel halophilic archaeon from Puerto Rico,” International Journal of Systematic Bacteriology, vol. 48, no. 4, pp. 1305–1312, 1998.
[78]  I. R. Cooke and M. Deserno, “Coupling between lipid shape and membrane curvature,” Biophysical Journal, vol. 91, no. 2, pp. 487–495, 2006.
[79]  L. Adamian, H. Naveed, and J. Liang, “Lipid-binding surfaces of membrane proteins: evidence from evolutionary and structural analysis,” Biochimica et Biophysica Acta, vol. 1808, no. 4, pp. 1092–1102, 2011.
[80]  N. G. A. Abrescia, J. J. B. Cockburn, J. M. Grimes et al., “Insights into assembly from structural analysis of bacteriophage PRD1,” Nature, vol. 432, no. 7013, pp. 68–74, 2004.
[81]  B. Tenchov, E. M. Vescio, G. D. Sprott, M. L. Zeidel, and J. C. Mathai, “Salt tolerance of archaeal extremely halophilic lipid membranes,” The Journal of Biological Chemistry, vol. 281, no. 15, pp. 10016–10023, 2006.


comments powered by Disqus