Genetics and Genomics of Triangular Disc-Shaped Halophilic Archaeon Haloarcula japonica Strain TR-1

  • Satoshi Nakamura
  • Kaoru Nakasone
  • Tomonori Takashina

The extremely halophilic archaea often exhibit unusual morphologies. Some cells may take a ribbon shape, a disk shape, or occasionally a square or triangular shape (Grant and Larsen 1989a; Grant and Larsen 1989b; Grant and Larsen 1989c). Square halophilic microbes have been observed in naturally occurring brines (Walsby 1980), and box-shaped halophilic microbes have also been isolated from Californian salterns (Javor et al. 1982). The square morphology, however, had not been convincingly demonstrated in the laboratory. The extremely halophilic archaea are now divided into 27 genera. The genus Haloarcula contains a number of pleomorphic isolates (Grant and Larsen 1989b). Thus, the square microbes described so far are likely to be Haloarcula spp. Recently, two square halophilic archaea were cultured, isolated, and taxonomically identified (Oren et al. 1999; Bolhuis et al. 2004). One of them actually belongs to the genus Haloarcula.

In the course of screening a large number of samples...


Acidic Amino Acid Cell Surface Glycoprotein Halophilic Archaea High Salt Condition Basal Transcription Factor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Anderson I, Tindall BJ, Pomrenke H, Göker M, Lapidus A, Nolan M, Copeland A, Del Rio TG, Chen F, Tice H, Cheng J-F, Lucas S, Chertkov O, Bruce D, Brettin T, Detter JC, Han C, Goodwin L, Land M, Hauser L, Chang Y-J, Jeffries CD, Pitluck S, Pati A, Mavromatis K, Ivanova N, Ovchinnikova G, Chen A, Palaniappan K, Chain P, Rohde M, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP (2009) Complete genome sequence of Halorhabdus utahensis type strain (AX-2T). Stand Genomic Sci 1:218–225PubMedCrossRefGoogle Scholar
  2. Baliga NS, Bonneau R, Facciotti MT, Pan M, Glusman G, Deutsch EW, Shannon P, Chiu Y, Weng RS, Gan RR, Hung P, Date SV, Marcotte E, Hood L, Ng WV (2004) Genome sequence of Haloarcula marismortui: a halophilic archaeon from the Dead Sea. Genome Res 14:2221–2234PubMedCrossRefGoogle Scholar
  3. Bolhuis A (2002) Protein transport in the halophilic archaeon Halobacterium sp. NRC-1: a major role for the twin arginine translocation pathway? Microbiology 148:3335–3346PubMedGoogle Scholar
  4. Bolhuis H, te Poele EM, Rodriguez-Valera F (2004) Isolation and characterization of Walsby’s square archaeon. Env Micribiol 6:1287–1291CrossRefGoogle Scholar
  5. Bolhuis H, Palm P, Wende A, Falb M, Rampp M, Rodriguez-Valera F, Pfeiffer F, Oesterhelt D (2006) The genome of the square archaeon Haloquadratum walsbyi, life at the limits of water activity. BMC Genom 7:169CrossRefGoogle Scholar
  6. Bramhill D, Thompson CM (1994) GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules. Proc Natl Acad Sci USA 91:5813–5817PubMedCrossRefGoogle Scholar
  7. de Boer P, Crossley R, Rothfield L (1992) The essential bacterial cell-division protein FtsZ is a GTPase. Nature (London) 359:254–256CrossRefGoogle Scholar
  8. Erickson HP (1997) FtsZ, a tubulin homologue in prokaryote cell division. Trends Cell Biol 7:362–367PubMedCrossRefGoogle Scholar
  9. Falbet M, Pfeiffer F, Palm P, Rodewald K, Hickmann V, Tittor J, Oesterhelt D (2005) Living with two extremes: conclusions from the genome sequence of Natronomonas pharaonis. Genome Res 15:1336–1343CrossRefGoogle Scholar
  10. Frolow F, Harel M, Sussman JL, Mevarech M, Shoham M (1996) Insight into protein adaptation to a saturated salt environment from the crystal structure of a halophilic 2Fe-2S ferredoxin. Nat Struct Biol 3:452–458PubMedCrossRefGoogle Scholar
  11. Grant WD, Larsen H (1989a) Halobacteriales. In: Staley JT (ed) Bergey’s manual of systematic bacteriology, vol 3, 9th edn. Williams & Wilkins, Baltimore, pp 2216–2219Google Scholar
  12. Grant WD, Larsen H (1989b) Haloarcula. In: Staley JT (ed) Bergey’s manual of systematic bacteriology, vol 3, 9th edn. Williams & Wilkins, Baltimore, pp 2224–2226Google Scholar
  13. Grant WD, Larsen H (1989c) Haloferax. In: Staley JT (ed) Bergey’s manual of systematic bacteriology, vol 3, 9th edn. Williams & Wilkins, Baltimore, pp 2226–2228Google Scholar
  14. Hall DO, Evans MC (1969) Iron-sulphur proteins. Nature (London) 223:1342–1348CrossRefGoogle Scholar
  15. Hall DO, Cammack R, Rao KK (1974) Non-haem iron proteins. In: Jacobs A, Worwood M (eds) Iron in biochemistry and medicine. Academic, New York, pp 279–334Google Scholar
  16. Hamamoto T, Takashina T, Grant WD, Horikoshi K (1988) Asymmetric cell division of a triangular halophilic archaebacterium. FEMS Microbiol Lett 56:221–224CrossRefGoogle Scholar
  17. Hirota N, Matsuo T, Ikeda A, Yatsunami R, Fukui T, Nakamura S (2005) Role of an N-terminal domain found in the ferredoxin from extremely halophilic archaeon Haloarcula japonica. J Jpn Soc Extr 4:14–24Google Scholar
  18. Horikoshi K, Aono R, Nakamura S (1993) The triangular halophilic archaebacterium Haloarcula japonica strain TR-1. Experientia 49:497–502CrossRefGoogle Scholar
  19. Ihara K, Mukohata Y (1991) The ATP synthase of Halobacterium salinarium (halobium) is an archaebacterial type as revealed from the amino acid sequences of its two major subunits. Arch Biochem Biophys 286:111–116PubMedCrossRefGoogle Scholar
  20. Javor B, Requadt C, Stoeckenius W (1982) Box-shaped halophilic bacteria. J Bacteriol 151:1532–1542PubMedGoogle Scholar
  21. Juez G, Rodriguez-Valera F, Ventosa A, Kushner DJ (1986) Haloarcula hispanica spec. nov. and Haloferax gibbonsii spec. nov. Two new species of extremely halophilic archaebacteria. Syst Appl Micribiol 8:75–79CrossRefGoogle Scholar
  22. Katharina T, Bleiholder A, Griesbach T, Pfeifer F (2008) Variations in the multiple tbp genes in different Halobacterium salinarum strains and their expression during growth. Arch Microbiol 190:309–318CrossRefGoogle Scholar
  23. Kersher L, Oesterhert D, Cammack R, Hall DO (1976) A new plant-type ferredoxin from halobacteria. Eur J Biochem 71:101–108CrossRefGoogle Scholar
  24. Kessel M, Wildhaber I, Cohen S, Baumeister W (1988) Three-dimensional structure of the regular surface glycoprotein layer of Halobacterium volcanii from the Dead Sea. EMBO J 7:1549–1554PubMedGoogle Scholar
  25. Kitajima T, Hirayama J-I, Ihara K, Sugiyama Y, Kamo N, Mukohata Y (1996) Novel bacterial rhodopsins from Haloarcula vallismortis. Biochem Biophys Res Commun 220:341–345PubMedCrossRefGoogle Scholar
  26. Lam WL, Doolittle WF (1989) Shuttle vectors for the archaebacterium Halobacterium volcanii. Proc Natl Acad Sci USA 86:5478–5482PubMedCrossRefGoogle Scholar
  27. Lechner J, Sumper M (1987) The primary structure of a prokaryotic glycoprotein. J Biol Chem 262:9724–9729PubMedGoogle Scholar
  28. Lutkenhaus J, Addinall SG (1997) Bacterial cell division and the Z ring. Ann Rev Biochem 66:93–116PubMedCrossRefGoogle Scholar
  29. Malfatti S, Tindall BJ, Schneider S, Fähnrich R, Lapidus A, LaButti K, Copeland A, Del Rio TG, Nolan M, Chen F, Lucas S, Tice H, Cheng JF, Bruce D, Goodwin L, Pitluck S, Anderson IJ, Pati A, Ivanova N, Mavromatis K, Chen A, Palaniappan K, D’haeseleer P, Göker M, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk H-P, Chain P (2009) Complete genome sequence of Halogeometricum borinquense type strain (PR3T). Stand Genomic Sci 1:150–158PubMedCrossRefGoogle Scholar
  30. Margolin W, Wang R, Kumar M (1996) Isolation of an ftsZ homolog from the archaebacterium Halobacterium salinarum: implications for the evolution of FtsZ and tubulin. J Bacteriol 178:1320–1327PubMedGoogle Scholar
  31. Matsuo T, Ikeda A, Seki H, Ichimata T, Sugimori D, Nakamura S (2001) Cloning and expression of the ferredoxin gene from extremely halophilic archaeon Haloarcula japonica strain TR-1. BioMetals 14:135–142PubMedCrossRefGoogle Scholar
  32. Mescher MF, Strominger JL (1976) Structural (shape-maintaining) role of the cell surface glycoprotein of Halobacterium salinarium. Proc Natl Acad Sci USA 73:2687–2691PubMedCrossRefGoogle Scholar
  33. Mescher MF, Strominger JL, Watson SW (1974) Protein and carbohydrate composition of the cell envelope of Halobacterium salinarium. J Bacteriol 120:945–954PubMedGoogle Scholar
  34. Mevarech M, Frolow F, Gloss ML (2000) Halophilic enzymes: proteins with a grain of salt. Biophys Chem 86:155–164PubMedCrossRefGoogle Scholar
  35. Mori H, Ito K (2001) The Sec protein-translocation pathway. Trends Microbiol 9:494–500PubMedCrossRefGoogle Scholar
  36. Mukherjee A, Lutkenhaus J (1994) Guanine nucleotide-dependent assembly of FtsZ into filaments. J Bacteriol 176:2754–2758PubMedGoogle Scholar
  37. Mukohata Y, Ihara K, Tamura T, Sugiyama Y (1999) Halobacterial rhodopsins. J Biochem 125:649–657PubMedCrossRefGoogle Scholar
  38. Nakamura S, Aono R, Mizutani S, Takashina T, Grant WD, Horikoshi K (1992) The cell surface glycoprotein of Haloarcula japonica TR-1. Biosci Biotechnol Biochem 56:996–998CrossRefGoogle Scholar
  39. Nakamura S, Mizutani S, Wakai H, Kawasaki H, Aono R, Horikoshi K (1995) Purification and partial characterization of cell surface glycoprotein from extremely halophilic archaeon Haloarcula japonica strain TR-1. Biotechnol Lett 17:705–706CrossRefGoogle Scholar
  40. Ng WV, Kennedy SP, Mahairas GG, Berquist B, Pan M, Shukla HD, Lasky SR, Baliga NS, Thorsson V, Sbrogna J, Swartzell S, Weir D, Hall J, Dahl TA, Welti R, Goo YA, Leithauser B, Keller K, Cruz R, Danson MJ, Hough DW, Maddocks DG, Jablonski PE, Krebs MP, Angevine CM, Dale H, Isenbarger TA, Peck RF, Pohlschroder M, Spudich JL, Jung KH, Alam M, Freitas T, Hou S, Daniels CJ, Dennis PP, Omer AD, Ebhaedt H, Lowe TM, Liang P, Riley M, Hood L, DasSarma S (2000) Genome sequence of Halobacterium species NRC-1. Proc Natl Acad Sci USA 97:12176–12181PubMedCrossRefGoogle Scholar
  41. Nishiyama Y, Takashina T, Grant WD, Horikoshi K (1992) Ultrastructure of the cell wall of the triangular halophilic archaebacterium Haloarcula japonica strain TR-1. FEMS Microbiol Lett 99:43–48CrossRefGoogle Scholar
  42. Nishiyama Y, Nakamura S, Aono R, Horikoshi K (1995) Electron microscopy of halobacteria. In: Robb FT, Sowers KR, DasSarma S, Place AP, Schreier HJ, Fleischmann EM (eds) Archaea: a laboratory manual, halophiles. Cold Spring Harbor Laboratory Press, New York, pp 29–33Google Scholar
  43. Oesterhelt D, Stoeckenius W (1973) Functions of a new photoreceptor membrane. Proc Natl Acad Sci USA 70:2853–2857PubMedCrossRefGoogle Scholar
  44. Ohtani H, Itoh H, Shinmura T (1992) Time-resolved fluorometry of purple membrane of Halobacterium halobium: O640 and an O-like red-shifted intermediate Q. FEBS Lett 305:6–8PubMedCrossRefGoogle Scholar
  45. Oren A, Ventosa A, Gutierrez MC, Kamekura M (1999) Haloarcula quadrata sp. nov., a square, motile archaeon isolated from a brine pool in Sinai (Egypt). Int J Syst Bacteriol 49:1149–1155PubMedCrossRefGoogle Scholar
  46. Otozai K, Takashina T, Grant WD (1991) A novel triangular archaebacterium, Haloarcula japonica. In: Horikoshi K, Grant WD (eds) Superbugs, microorganisms in extreme environmrnts. Japan Scientific Societies Press, Tokyo, pp 63–75Google Scholar
  47. Ozawa K, Harashina T, Yatsunami R, Nakamura S (2005) Gene cloning, expression and partial characterization of cell division protein FtsZ1 from extremely halophilic archaeon Haloarcula japonica strain TR-1. Extremophiles 9:281–288PubMedCrossRefGoogle Scholar
  48. Peck RF, DasSarma S, Krebs MP (2000) Homologous gene knockout in the archaeon Halobacterium salinarum with ura3 as a counterselectable marker. Mol Microbiol 35:667–676PubMedCrossRefGoogle Scholar
  49. Pfeifer F, Griffig J, Oesterhelt D (1993) The fdx gene encoding the [2Fe-2S] ferredoxin of Halobacterium salinarium. Mol Gen Genet 239:66–71PubMedGoogle Scholar
  50. Pfeiffer F, Schuster SC, Broicher A, Falb M, Palm P, Rodewald K, Ruepp A, Soppa J, Tittor J, Oesterhelt D (2008) Evolution in the laboratory: the genome of Halobacterium salinarum strain R1 compared to that of strain NRC-1. Genomics 91:335–346PubMedCrossRefGoogle Scholar
  51. Poplawski A, Gullbrand B, Bernander R (2000) The ftsZ gene of Haloferax mediterranei: sequence, conserved gene order, and visualization of the FtsZ ring. Gene 242:357–367PubMedCrossRefGoogle Scholar
  52. RayChaudhuri D, Park JT (1992) Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature (London) 359:251–254CrossRefGoogle Scholar
  53. Rose RW, Brüser T, Kissinger JC, Pohlschröder M (2002) Adaptation of secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway. Mol Microbiol 45:943–950PubMedCrossRefGoogle Scholar
  54. Saunders E, Tindall BJ, Fähnrich R, Lapidus A, Copeland A, Del Rio TG, Lucas S, Chen F, Tice H, Cheng J-F, Han C, Detter JC, Bruce D, Goodwin L, Chain P, Pitluck S, Pati A, Ivanova N, Mavromatis K, Chen A, Palaniappan K, Land M, Hauser L, Chang Y-J, Jeffries CD, Brettin T, Rohde M, Göker M, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Klenk H-P, Kyrpides NC (2009) Complete genome sequence of Haloterrigena turkmenica type strain (4kT). Stand Genomic Sci 1:107–116CrossRefGoogle Scholar
  55. Schobert B, Lanyi JK (1982) Halorhodopsin is a light-driven chloride pump. J Biol Chem 257:10306–10313PubMedGoogle Scholar
  56. Sleytr UB, Messner P (1983) Crystalline surface layers on bacteria. Ann Rev Microbiol 37:311–339CrossRefGoogle Scholar
  57. Steinert K, Wagner V, Kroth-Pancic PG, Bickel-Sandkotter S (1997) Characterization and subunit structure of the ATP synthase of the halophilic archaeon Haloferax volcanii and organization of the ATP synthase genes. J Biol Chem 272:6261–6269PubMedCrossRefGoogle Scholar
  58. Sugimori D, Ichimata T, Ikeda A, Nakamura S (2000) Purification and characterization of a ferredoxin from Haloarcula japonica strain TR-1. BioMetals 13:23–28PubMedCrossRefGoogle Scholar
  59. Sugiyama Y, Maeda M, Futai M, Mukohata Y (1989) Isolation of a gene that encodes a new retinal protein, archaerhodopsin, from Halobacterium sp. aus-1. J Biol Chem 264:20859–20862PubMedGoogle Scholar
  60. Sugiyama Y, Yamada N, Mukohata Y (1994) The light-driven proton pump, cruxrhodopsin-2 in Haloarcula sp. arg-2 (bR+, hR), and its coupled ATP formation. Biochim Biophys Acta 1188:287–292PubMedCrossRefGoogle Scholar
  61. Sumper M (1987) Halobacterial glycoprotein biosynthesis. Biochim Biophys Acta 906:69–79PubMedCrossRefGoogle Scholar
  62. Sumper M, Berg E, Mengele R, Strobel I (1990) Primary structure and glycosylation of the S-layer protein of Haloferax volcanii. J Bacteriol 172:7111–7118PubMedGoogle Scholar
  63. Takashina T, Hamamoto T, Otozai K, Grant WD, Horikoshi K (1990) Haloarcula japonica sp. nov., a new triangular halophilic archaebacterium. Syst Appl Microbiol 13:177–181CrossRefGoogle Scholar
  64. Tateno M, Ihara K, Mukohata Y (1994) The novel ion pump rhodopsins from Haloarcula form a family independent from both the bacteriorhodopsin and archaerhodopsin families/tribes. Arch Biochem Biophys 315:127–132PubMedCrossRefGoogle Scholar
  65. Thomson AJ (1985) Met al.loproteins. In: Harrison PM (ed) Iron-sulfur proteins. Macmillan, London, pp 79–120Google Scholar
  66. Tindall BJ, Schneider S, Lapidus A, Copeland A, Del Rio TG, Nolan M, Lucas S, Chen F, Tice H, Cheng J-F, Saunders E, Bruce D, Goodwin L, Pitluck S, Mikhailova N, Pati A, Ivanova N, Mavrommatis K, Chen A, Palaniappan K, Chain P, Land M, Hauser L, Chang Y-J, Jeffries CD, Brettin T, Han C, Rohde M, Göker M, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Klenk H-P, Kyrpides NC, Detter JC (2009) Complete genome sequence of Halomicrobium mukohataei type strain (arg-2T). Stand Genomic Sci 1:270–277PubMedCrossRefGoogle Scholar
  67. Uegaki K, Sugiyama Y, Mukohata Y (1991) Archaerhodopsin-2 from Halobacterium sp. aus-2, further reveals essential amino acid residues for light-driven proton pumps. Arch Biochem Biophys 286:107–110PubMedCrossRefGoogle Scholar
  68. Umemura K, Wakai H, Takada K, Nakamura S, Hara M (1998) Atomic force microscopy of an extremely halophilic archaeon using rapid membrane filtration method. Bioimages 6:77–81Google Scholar
  69. Wakai H, Nakamura S, Kawasaki H, Takada K, Mizutani S, Aono R, Horikoshi K (1997) Cloning and sequencing of the gene encoding the cell surface glycoprotein of Haloarcula japonica strain TR-1. Extremophiles 1:29–35PubMedCrossRefGoogle Scholar
  70. Walsby AE (1980) A square bacterium. Nature (London) 283:69–71CrossRefGoogle Scholar
  71. Wang X, Lutkenhaus J (1996) FtsZ ring: the eubacterial division apparatus conserved in archaebacteria. Mol Microbiol 21:313–319PubMedCrossRefGoogle Scholar
  72. Werber MM, Mevarech M (1978) Purification and characterization of a highly acidic 2Fe-ferredoxin from Halobacterium of the Dead Sea. Arch Biochem Biophys 187:447–456PubMedCrossRefGoogle Scholar
  73. Wieland F, Dompert W, Bernhardt G, Sumper M (1980) Halobacterial glycoprotein saccharides contain covalently linked sulphate. FEBS Lett 120:110–114PubMedCrossRefGoogle Scholar
  74. Yatsunami R, Kawakami T, Ohtani H, Nakamura S (1997) Primary structure of the novel bacterial rhodopsin from extremely halophilic archaeon Haloarcula japonica strain TR-1. Nucleic Acids Symp Ser 37:111–112PubMedGoogle Scholar
  75. Yatsunami R, Kawakami T, Ohtani H, Nakamura S (1999a) Transcriptional regulation of cruxrhodopsin gene from extremely halophilic archaeon Haloarcula japonica strain TR-1. Nucleic Acids Symp Ser 42:73–74PubMedCrossRefGoogle Scholar
  76. Yatsunami R, Iwamoto M, Ihara K, Nakamura S (1999b) Molecular cloning of A1-ATPase gene from extremely halophilic archaeon Haloarcula japonica strain TR-1. Nucleic Acids Symp Ser 42:75–76PubMedCrossRefGoogle Scholar
  77. Yatsunami R, Kawakami T, Ohtani H, Nakamura S (2000a) A novel bacteriorhodopsin-like protein from Haloarcula japonica strain TR-1: gene cloning, sequencing and transcript analysis. Extremophiles 4:109–114PubMedCrossRefGoogle Scholar
  78. Yatsunami R, Aono S, Nakamura S (2000b) The gene encoding a novel halorhodopsin-like protein of extremely halophilic archaeon Haloarcula japonica strain TR-1. Nucleic Acids Symp Ser 44:1–2PubMedCrossRefGoogle Scholar
  79. Yatsunami R, Iwamoto M, Ihara K, Nakamura S (2001) Gene clusters encoding ATP synthase of Haloarcula japonica strain TR-1. Nucleic Acids Res Suppl 1:51–52PubMedCrossRefGoogle Scholar
  80. Yatsunami R, Sato M, Orishimo K, Hatori Y, Zhang Y, Takashina T, Fukui T, Nakamura S (2010) Gene expression and characterization of a novel GH family 18 chitinase from extremely halophilic archaeon Halobacterium salinarum NRC-1. J Jpn Soc Extr 9:19–24Google Scholar

Copyright information

© Springer 2011

Authors and Affiliations

  • Satoshi Nakamura
    • 1
  • Kaoru Nakasone
    • 2
  • Tomonori Takashina
    • 3
  1. 1.Department of BioengineeringTokyo Institute of TechnologyYokohama-shiJapan
  2. 2.Department of Biotechnology and ChemistryKinki UniversityHigashi-Hiroshima-shiJapan
  3. 3.Department of Applied BiosciencesToyo UniversityOura-gunJapan

Personalised recommendations