Abstract
Chlorella viruses (or chloroviruses) are very large, plaque-forming viruses. The viruses are multilayered structures containing a large double-stranded DNA genome, a lipid bilayered membrane, and an outer icosahedral capsid shell. The viruses replicate in certain isolates of the coccal green alga, Chlorella. Sequence analysis of the 330-kbp genome of Paramecium bursaria Chlorella virus 1 (PBCV-1), the prototype of the virus family Phycodnaviridae, reveals <365 protein-encoding genes and 11 tRNA genes. Products of about 40% of these genes resemble proteins of known function, including many that are unexpected for a virus. Among these is a virus-encoded protein, called Kcv, which forms a functional K+ channel. This chapter focuses on the initial steps in virus infection and provides a plausible role for the function of the viral K+ channel in lowering the turgor pressure of the host. This step appears to be a prerequisite for delivery of the viral genome into the host.
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Notes
- 1.
The contact angle α describes the orientation of the membrane plane with respect to the inner lining of the small hole in the cell wall. An angle of 0o means that the plane of the membrane is quasi parallel to the wall; e.g. the membrane reveals an omega shape bulge. If at the other extreme the angle is 90o the membrane is perpendicular to the wall; the membrane remains flat in the plane without any budging out.
References
Abenavoli A, DiFrancesco M, Schroeder I, Epimashko S, Gazzarrini S, Hansen UP, Thiel G, Moroni A. Fast and slow gating are inherent properties of the K+ channel pore module. J. Gen. Physiol. (Submitted for publication)
Agarkova IV, Dunigan DD, Van Etten JL (2006) Virion-associated restriction endonucleases of chloroviruses. J Virol 80:8114–8123
Agarkova I, Dunigan D, Gurnon J, Greiner T, Barres J, Thiel G, Van Etten J (2008) Chlorovirus-mediated membrane depolarization of Chlorella alters secondary active transport of solutes. J Virol 82:12181–12190
Balss J, Mehmel M, Baumeister D, Hertel B, Delaroque N, Chatelain FC, Minor DJ, VanEtten JL, Moroni A, Thiel G (2008) Transmembrane domain length of viral K+ channels is a signal for mitochondria targeting. Proc Natl Acad Sci USA 105:12313–12318
Beilby MJ (1985) Potassium channels and different states of Chara plasmalemma. J. Membr Biol 89:241–249
Boulanger P, Letellier L (1992) Ion channels are likely to be involved in the two steps of phage T5 DNA penetration into Escherichia coli cells. J Biol Chem 267:3168–3172
Cerritelli ME, Trus BL, Smith CS, Cheng NQ, Conway JF et al (2003) A second symmetry mismatch at the portal vertex of bacteriophage T7: 8-fold symmetry in the procapsid core. J Mol Biol 327:1–6
Chernomordik LV, Leikina E, Kozlov MM, Frolov VA, Zimmerberg J (1999) Structural intermediates in influenza haemagglutinin-mediated fusion. Mol Membr Biol 16:33–42
Cherrier MV, Kostyuchenko VA, Xiao C, Bowman VD, Battisti AJ, Yan X, Chipman PR, Baker TS, Van Etten JL, Rossmann MG (2009) An icosahedral algal virus has a complex unique vertex decorated by a spike. Proc Natl Acad Sci USA (Epub ahead of print)
Cordov A, Desemo M, Gelbart WM, Ben-Shaul A (2003) Osmotic shock and the strength of viral capside. Biophys J 85:70–74
Dai J, Sheetz MP, Wan X, Morris CE (1998) Membrane tension in swelling and shrinking molluscan neurons. J. Neurosci 18:6681–6692
Dunigan DD, Fitzgerald LA, Van Etten JL (2006) Phycodnaviruses: a peek at genetic diversity. Virus Res 117:119–132
Felle HH (2005) pH regulation in anoxia plants. Ann Bot 96:519–532
Fitzgerald LA, Graves MV, Li X, Pfitzner AJ, Hoffart E, VanEtten JL (2007a) Sequence and annotation of the 288-kb ATCV-1 virus that infects an endosymbiotic Chlorella strain of the heliozoon Acanthocystis turfacea. Virology 362:350–361
Fitzgerald LA, Graves MV, Li X, Feldblyum T, Nierman WC, Van Etten JL (2007b) Sequence and annotation of the 369-kb NY-2A and the 345-kb AR158 viruses that infect Chlorella NC64A. Virology 358:472–484
Frohns F, Käsmann A, Kramer D, Schäfer B, Mehmel M, Kang M, Van Etten JL, Gazzarrini S, Moroni A, Thiel G (2006) Potassium ion channels of Chlorella viruses cause rapid depolarization of host cell during infection. J Virol 80:2437–2444
Gazzarrini S, Kang M, Empimashko S, Van Etten JL, Dainty J, Koroni A (2006) Chlorella viru MT325 encodes wate and potassium channels that interact synergistically. Proc Natl Acad Sci USA 103:5355–5360
Gazzarrini S, Kang M, Abenavoli A, Romani G, Olivari C, Gaslini D, Ferrara G, Van Etten JL, Kreim M, Kast SM, Thiel G, Moroni A (2009) Eighty-two amino acids are sufficient for making a potassium selective channel. Biochemical Journal (Epub ahead of print)
Gonzalez-Huici V, Salas M, Hermoso JM (2004) The push-pull mechanisms of bacteriophyge phi.29 DNA injection. Mol Microbiol 52:529–540
Grayson P, Molineux IJ (2007) Is phage DNA injected into cells- biologists and physicists can agree. Curr Opin Microbiol 10:401–409
Grayson P, Han L, Winther T, Philips R (2007) Real-time observations of single bacteriophage λ DNA ejections in vitro. Proc Natl Acad Sci USA 104:14652–14657
Harrison SC (2008) Viral membrane fusion. Nat Struct Mol Biol 15:690–698
Jahn R, Scheller RH (2006) SNARE-engines for membrane fusion. Nat Rev Mol Cell Biol 7:631–643
Kang M, Graves M, Mehmel M, Moroni A, Gazzarrini S, Thiel G, Gurnon J, Van Etten JL (2004a) Genetic diversity in Chlorella viruses flanking kcv, a gene that encodes a potassium ion channel protein. Virology 326:150–159
Kang M, Moroni A, Gazzarrini S, DiFrancesco D, Thiel G, Severino M, Van Etten JL (2004b) Small potassium ion channel protein encoded by Chlorella viruses. Proc Natl Acad Sci USA 101:5318–5324
Kawasaki T, Tanaka M, Fujie M, Usami S, Yamada T (2004) Immediate early genes expressed in chlorovirus infection. Virology 318:214–223
Kim Y, Ye Q, Reinhardt H, Steudle E (2006) Further quantification of the role of internal unstirred layers during the measurements of transport coefficients in giant internodes of Chara by a new stop-flow technique. J Exp Bot 57:4133–4144
Kuznetsov YG, Gurnon JR, Van Etten JL, McPherson A (2005) Atomic force microscopy investigation of a Chlorella virus, PBCV-1. J Struct Biol 149:256–263
Labedan B, Letellier L (1981) Membrane potential changes during the first step of coliphage infection. Proc Natl Acad Sci USA 78:215–219
Landstein D, Burbank DE, Nietfeldt JW, Van Etten JL (1995) Large deletions in antigenic variants of the Chlorella virus PBCV-1. Virology 214:413–420
Lebedev AA, Krause MH, Isidro AL, Vagin AA, Orlova EV et al (2007) Structural framework for DNA translocation via the viral portal protein. EMBO J 26:1984–1994
Li Z, Wu J, Wang ZG (2008) Osmotic pressure and packing structure of caged DNA. Biophys J 94:737–746
Meints RH, Lee K, Burbank DE, Van Etten JL (1984) Infection of a Chlorella-like alga with the virus PBCV-1: Ultrastructural studies. Virology 138:341–346
Molineux IJ (2006) Fifty-three years since Hershey and Chase; much ado about pressure but which pressure is it? Virology 344:221–229
Morris CE, Homann U (2001) Cell surface regulation and membrane tension. J Membr Biol 179:79–102
Neupärtl M, Meyer C, Woll I, Frohns F, Kang M, Van Etten JL, Kramer D, Hertel B, Moroni A, Thiel G (2007) Chlorella viruses evoke a rapid release of K+ from host cells during early phase of infection. Virology 372:340–348
Onimatsu H, Suganuma K, Uenoyama S, Yamada T (2006) C-terminal repetitive motifs in Vp130 present at the unique vertex of the chlorovirus capsid are essential for binding to the host Chlorella cell wall. Virology 353:432–442
Pagliuca C, Goetze TA, Wagner R, Thiel G, Moroni A, Parcej D (2007) Molecular properties of Kcv, a viral-encoded K+ channel. Biochemistry 46:1079–1090
Plugge B, Gazzarrini S, Cerana R, Van Etten JL, Nelson M, DiFrancesco D, Moroni A, Thiel G (2000) A potassium ion channel protein encoded by Chlorella virus PBCV-1. Science 287:1641–1644
Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:401–417
Schuster AM, Girton L, Burbank DE, Van Etten JL (1986) Infection of a Chlorella-like alga with the virus PBCV-1: transcriptional studies. Virology 148:181–189
Seaton GR, Lee K, Rohozinski J (1995) Photosynthetic shutdown in Chlorells NC64A associated with the infection cycle of Paramecium bursaria Chlorella virus-1. Plant Physiol 108:1431–1438
Seaton GR, Hurry VM, Rohozinski J (1996) Novel amplification of non-photochemical chlorophyll fluorescence quenching following viral infection in Chlorells. FEBS Lett 389:319–323
Shillcock JC, Lipowsky R (2008) Tension-induced fusion of bilayer membranes and vesicles. Nat Mater 4:225–228
Thiel G, Gradmann D (1994) Electrophysiology of stomata. Prog Bot 55:59–78
Thiel G, Wolf A (1997) Operation of K+-channels in stomatal movement. Trends Plant Sci 2:339–345
Thiel G, Sutter J-U, Homann U (2000) Ca2+-sensitive and Ca2+ insensitive exocytosis in maize coleoptile protoplasts. Pflügers Archive Eur J Physiol 439:R152–R153
Van Etten JL (2003) Unusual life style of giant Chlorella viruses. Annu Rev Genet 37:153–195
Van Etten JL, Burbank DE, Xia Y, Meints RH (1983) Growth cycle of a virus, PBCV-1, that infects Chlorella-like algae. Virology 126:117–125
Van Etten JL, Burbank DE, Joshi J, Meints RH (1984) DNA synthesis in a Chlorella-like alga following infection with the virus PBCV-1. Virology 134:443–449
Van Etten JL, Lane LC, Meints RH (1991) Viruses and viruslike particles of eukaryotic alage. Microbiol Rev 55:586–620
Wilson WH, Van Etten JL, Allen MJ (2009) The Phycodnaviridae: the story of how tiny giants rule the world. In: Van Etten J (ed) Lesser known large dsDNA viruses. Springer, Berlin, pp 1–42
Yamada T, Onimatsu H, Van Etten JL (2006) Chlorella viruses. Adv Virus Res 66:293–336
Zauberman N, Mutsafi Y, Halevy DH, Shimoni E, Klein E, Xiao C, Sun S, Minsky A (2008) Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga mimivirus. PLoS Biol 13:e114
Acknowledgments
The authors are grateful for financial support for this research by the Deutsche Forschungsgemeinschaft to GT and the European Drug Initiative on Channels and Transporters (EDICT) project EU FP7 (201924) to A.M. Research in the Van Etten laboratory was supported in part by Public Health Service grant GM32441 from the National Institute of General Medical Sciences and NIH grant P20-RR1565 from the COBRE program of the National Center for Research Resources.
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Thiel, G., Moroni, A., Dunigan, D., Van Etten, J.L. (2010). Initial Events Associated with Virus PBCV-1 Infection of Chlorella NC64A. In: Lüttge, U., Beyschlag, W., Büdel, B., Francis, D. (eds) Progress in Botany 71. Progress in Botany, vol 71. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-02167-1_7
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