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Halophilic microorganisms from man-made and natural hypersaline environments: Physiology, ecology, and biotechnological potential

  • Madalin Enache
  • Gabriela Popescu
  • Takashi Itoh
  • Masahiro Kamekura

Abstract

What are hypersaline environments? Geologists or geochemists define saline lakes sensu lato as bodies of water with salinity more than 3 g/l (0.3%), while those sensu stricto (hypersaline) are bodies of water that exceed the modest 35 g/l (3.5%) salt of oceans (Williams 1998). Many microbiologists use the term hypersaline to denote the well-known salt lakes, such as the Dead Sea and the Great Salt Lake or crystallizer ponds of solar salterns, environments almost saturated with salt.

Keywords

Salt Lake Halophilic Bacterium Great Salt Lake Hypersaline Environment Halophilic Archaea 
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.

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References

  1. Anderson H (1954) The reddening of salted hides and fish. Appl Microbiol 2:64–69PubMedGoogle Scholar
  2. Anton J, Meseguer I, Rodriguez-Valera F (1988) Production of an extracellular polysaccharide by Haloferax mediterranei.Appl Environ Microbiol 54:2381–2386PubMedGoogle Scholar
  3. Borgne SL, Paniagua D, Vazquez-Duhalt R (2008) Biodegradation of organic pollutants by halophilic bacteria and archaea. J Mol Microbiol Biotechnol 15:74–92PubMedCrossRefGoogle Scholar
  4. Broşteanu C (1901) Our salt mine. Historic, juridical and economical study towards saline exploitations and salt monopoly on Romans and Romanian (in Romanian). In: Lazareanu GA (ed) BucharestGoogle Scholar
  5. Bulgăreanu VAC (1993) The protection and management of saline lakes of therapeutic value in Romania. Int J Salt Lake Res 2:165–171CrossRefGoogle Scholar
  6. Burns DG, Janssen PH, Itoh T, Kamekura M, Echigo A, Dyall-Smith ML (2010) Halonotius pteroides gen. nov., sp. nov., an extremely halophilic archaeon recovered from a saltern crystallizer in southern Australia. Int J Syst Evol Microbiol 60:1196–1199PubMedCrossRefGoogle Scholar
  7. Chervinskaya AV, Zilber NA (1995) Halotherapy for treatment of respiratory diseases. J Aerosol Med 8:221–232PubMedCrossRefGoogle Scholar
  8. Cojoc R, Merciu S, Oancea P, Pincu E, Dumitru L, Enache M (2009) Highly thermostable exopolysaccharide produced by the moderately halophilic bacterium isolated from a man-made young salt lake in Romania. Pol J Microbiol 58:289–294PubMedGoogle Scholar
  9. Drăgănescu L (1990) Dates from historic salt exploitation at Slanic-Prahova (in Romanian). Rev Muzeelor 27:68–71Google Scholar
  10. Drăgănescu L, Drăgănescu S (2001) The history of the evolution of salt working methods in Romania, from antiquity to the present. In: 17th Intl Mining Congress and Exhibition of Turkey-IMCET, pp 627–633Google Scholar
  11. Duggen S, Hoernle K, van den Bogaard P, Rüpke L, Morgan JP (2003) Deep roots of the Messinian salinity crisis. Nature 422:602–606PubMedCrossRefGoogle Scholar
  12. Dumitru L, Teodosiu G, Enache E (2002) The tolerance of extremely halophilic archaea to heavy metals. Proc Inst Biol 4:261–267Google Scholar
  13. Dumitru L, Teodosiu-Popescu G, Enache M, Cojoc R, Kleps I, Ignat T (2007) S-layer of Haloferax sp. GR 2 (JCM 13922): isolation, characterization and binding to silicon nanostructurated substrates. In: Kleps I, Ion AC, Dascalu D (eds) Progress in nanoscience and nanotechnologies, Seria vol 11, Micro and nanoengineering. Ed. Acad Române, Bucharest, pp 146–152Google Scholar
  14. Eichler J (2003) Facing extremes: archaeal surface-layer (glyco) proteins. Microbiology 149:3347–3351PubMedCrossRefGoogle Scholar
  15. Enache M, Faghi AM (1999) Detection of extracellular halophilic amylase activity from the extreme halophilic genus Haloferax. Proc Inst Biol 2:143–146Google Scholar
  16. Enache M, Dumitru L, Faghi AM (1999a) Occurrence of halocins in mixed archaebacteria culture. Proc Inst Biol 2:151–154Google Scholar
  17. Enache M, Teodosiu G, Dumitru L, Faghi AM, Zarnea G (1999b) Diversity of halobacteria in accordance with their membrane lipids composition. Proc Inst Biol 2:147–149Google Scholar
  18. Enache M, Teodosiu G, Faghi AM, Dumitru L (2000a) Identification of halophilic Archaebacteria isolated from some Romanian salts lakes on the basis of lipids composition. Rev Roum Biol Biol Veg 45:93–99Google Scholar
  19. Enache M, Faghi AM, Teodosiu G, Dumitru L, Zarnea G (2000b) Effect of temperature and NaCl concentration of growth media on neutral lipid in Haloferax volcanii and Haloferax sp. GR1 strain. Proc Inst Biol 3:251–256Google Scholar
  20. Enache E, Faghi AM, Teodosiu G, Dumitru L, Zarnea G (2000c) The halophilic microorganisms response to heavy metals. Rev Roum Biol Biol Veg 45:111–116Google Scholar
  21. Enache M, Faghi AM, Dumitru L, Zarnea G (2001) Halophilic α-amylase from the extremely halophilic archaea Haloferax sp. strain GR1. Proc Rom Acad Series B 2:107–109Google Scholar
  22. Enache M, Teodosiu G, Dumitru L, Zarnea G (2004a) The effect of NaCl concentrations on the growth and lipase activity at Haloferax sp. GR1. Proc Inst Biol 6:233–236Google Scholar
  23. Enache M, Faghi AM, Dumitru L, Teodosiu G, Zarnea G (2004b) Halocin HF 1 a bacteriocin produced by Haloferax sp. GR 1. Proc Rom Acad Series B 1:27–32Google Scholar
  24. Enache M, Itoh T, Kamekura M, Teodosiu G, Dumitru L (2007a) Haloferax prahovense sp. nov., an extremely halophilic archaeon isolated from a Romanian salt lake. Int J Syst Evol Microbiol 57:393–397PubMedCrossRefGoogle Scholar
  25. Enache M, Itoh T, Fukushima, Usami R, Dumitru L, Kamekura M (2007b) Phylogenetic relationship within the family Halobacteriaceae inferred from rpoB′ gene and protein sequences. Int J Syst Evol Microbiol 57:2289–2295PubMedCrossRefGoogle Scholar
  26. Enache M, Itoh T, Kamekura M, Popescu G, Dumitru L (2008a) Halophilic archaea of Haloferax genus isolated from anthropocentric Telega (Palada) salt lake. Proc Rom Acad Series B 10:11–16Google Scholar
  27. Enache M, Itoh T, Kamekura M, Popescu G, Dumitru L (2008b) Halophilic archaea isolated from man-made young (200 years) salt lakes in Slănic, Prahova, Romania. Cent Eur J Biol 3:388–395CrossRefGoogle Scholar
  28. Enache M, Popescu G, Dumitru L, Kamekura M (2009) The effect of Na+/Mg2+ ratio on the amylase activity of haloarchaea isolated from Techirghiol lake, Romania, a low salt environment. Proc Rom Acad Series B 11:3–7Google Scholar
  29. Faghi AM, Teodosiu G, Dumitru L (1999) The dynamic of the halophilic microorganisms growth at different values of pH and temperature. I. Moderately halophilic bacteria. Proc Inst Biol 2:155–161Google Scholar
  30. Fendrihan S, Bérces A, Lammer H, Musso M, Rontó G, Polacsek TK, Holzinger A, Kolb C, Stan-Lotter H (2009a) Investigating the effects of simulated Martian ultraviolet radiation on Halococcus dombrowskii and other extremely halophilic archaebacteria. Astrobiol 9:104–112CrossRefGoogle Scholar
  31. Fendrihan S, Musso M, Stan-Lotter H (2009b) Raman spectroscopy as a potential method for the detection of extremely halophilic archaea embedded in halite in terrestrial and possibly extraterrestrial samples. J Raman Spectr 40:1996–2003CrossRefGoogle Scholar
  32. Gâştescu P (1965) On the origin of salt lakes from Romanian Plain (in Romanian). Natura-Seria Geografie-Geologie 2:42–45Google Scholar
  33. Gâştescu P (1971) The lake from Romania (in Romanian). Ed Acad Rep Soc România, BucharestGoogle Scholar
  34. Gibbons NE (1974) Family V. Halobacteriaceae fam. nov. In: Buchanan RE, Gibbons NE (eds) Bergey’s manual of determinative bacteriology, 8th edn. Williams & Wilkins, Baltimore, pp 269–273Google Scholar
  35. Grant WD, Gemmell RT, McGenity TJ (1998) Halobacteria: the evidence for longevity. Extremophiles 2:279–287PubMedCrossRefGoogle Scholar
  36. Grant WD, Kamekura M, McGenity TJ, Ventosa A (2001) The order Halobacteriales. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology, vol 1, 2nd edn. Springer, New York, pp 294–334Google Scholar
  37. Gruber C, Legat A, Pfaffenhuemer M, Radax C, Weidler G, Busse HJ, Stan-Lotter H (2004) Halobacterium noricense sp. nov., an archaeal isolate from a bore core of an alpine Permian salt deposit, classification of Halobacterium sp. NRC-1 as a strain of H. salinarum and emended description of H. salinarum. Extremophiles, 8:431–439PubMedCrossRefGoogle Scholar
  38. Har N, Barbu O, Codrea V, Petrescu I (2006) New data on the mineralogy of the salt deposit from Slănic Prahova (Romania). Studia UBB, Geologia 51:29–33Google Scholar
  39. Hedman J, Hagg T, Sandell J, Haahtela T (2006) The effect of salt chamber treatment on bronchial hyperresponsiveness in asthmatics. Allergy 61:605–610PubMedCrossRefGoogle Scholar
  40. Horikoshi K (1999) Alkaliphiles: some applications of their products for biotechnology. Microbiol Mol Biol Rev 63:735–750PubMedGoogle Scholar
  41. Itoh T, Yamaguchi T, Zhou P, Takashina T (2005) Natronolimnobius baerhuensis gen. nov., sp. nov., and Natronolimnobius innermongolicus sp. nov., novel haloalkaliphilic archaea isolated from soda lakes in Inner Mongolia, China. Extremophiles 9:111–116PubMedCrossRefGoogle Scholar
  42. Javor B (1989a) Chapter 1. Geology and chemistry. In: Hypersaline environments. Microbiology and biogeochemistry. Springer-Verlag, Berlin, Heidelberg, New York, pp 5–25CrossRefGoogle Scholar
  43. Javor B (1989b) Chapter 15. Gavish Sabkha and other hypersaline marine sabkhas, pools and lagoons. In: Hypersaline environments. Microbiology and biogeochemistry. Springer-Verlag, Berlin, Heidelberg, New York, pp 222–235CrossRefGoogle Scholar
  44. Juez G (1988) Taxonomy of extremely halophilic archaebacteria. In: Rodriguez-Valera F (ed) Halophilic Bacteria, vol II. CRC Press, Boca Raton, FL, pp 3–24Google Scholar
  45. Kamekura M, Seno Y (1993) Partial sequence of the gene for a serine protease from a halophilic archaeum Haloferax mediterranei R4, and nucleotide sequences of 16S rRNA encoding genes from several halophilic archaea. Experientia 49:503–513PubMedCrossRefGoogle Scholar
  46. Kamekura M, Dyall-Smith ML, Upasani V, Ventosa A, Kates M (1997) Diversity of alkaliphilic halobacteria: proposal for transfer of Natronobacterium vacuolatum, Natronobacterium magadii and Natronobacterium pharaonis to Halorubrum, Natrialba and Natronomonas gen. nov., respectively, as Halorubrum vacuolatum comb. nov., Natrialba magadii comb. nov., and Natronomonas pharaonis comb. nov., respectively. Int J Syst Bacteriol 47:853–857PubMedCrossRefGoogle Scholar
  47. Kates M (1995) Adventures with membrane lipids. Biochem Soc Transac 23:697–709Google Scholar
  48. Kleps I, Ignat T, Miu M, Simion M, Teodosiu-Popescu G, Enache M, Dumitru L (2009) Protein-mesoporous silicon matrix obtained by S-layer technology. Phys Status Solidi C 6:1605–1609CrossRefGoogle Scholar
  49. Kocur M, Hodgkiss W (1973) Taxonomic status of the genus Halococcus Schoop. Int J Syst Bacteriol 23:151–156CrossRefGoogle Scholar
  50. Kunte HJ, Trueper HG, Stan-Lotter H (2002) Halophilic microorganism. In: Horneck G, Baumstark-Khan C (eds) Astrobiology. The quest for the conditions of life. Springer Verlag, Berlin, Heidelberg, pp 185–200CrossRefGoogle Scholar
  51. Kushner DJ (1985) The Halobacteriaceae. In: Woese CR, Wolfe RS (eds) The Bacteria, vol VIII. Academic Press, New York, pp 171–214Google Scholar
  52. Lequerica JL, O’Connor JE, Such L, Alberola A, Meseguer I, Dolz M, Torreblanca M, Moya A, Colom F, Soria B (2006) A halocin acting on Na+/H+ exchanger of Haloarchaea as a new type of inhibitor in NHE of mammals. J Physiol Biochem 62:253–262PubMedCrossRefGoogle Scholar
  53. Lochhead AG (1934) Bacteriological studies on the red discoloration of salted hides. Can J Res 10:275–286CrossRefGoogle Scholar
  54. Magrum LJ, Luehrsen KR, Woese CR (1978) Are extreme halophiles actually “bacteria”? J Mol Evol 11:1–8PubMedCrossRefGoogle Scholar
  55. Mellado E, Ventosa A (2003) Biotechnological potential of moderately and extremely halophilic microorganisms. In: Barredo JL (ed) Microorganisms for health care, food and enzyme production. Research Signpost, Kerala, pp 233–256Google Scholar
  56. Merciu S, Vacaroiu C, Filimon R, Popescu G, Preda S, Anastasescu C, Zaharescu M, Enache M (2009) Nanotubes biologically active in media with high salt concentration. Biotechnol Biotechnol Eq 23:827–831Google Scholar
  57. Minegishi H, Echigo A, Nagaoka S, Kamekura M, Usami R (2010) Halarchaeum acidiphilum gen. nov., sp. nov., a moderately acidophilic haloarchaeon isolated from commercial solar salt. Int J Syst Evol Microbiol (in press). DOI: 10.1099/ijs.0.013722-0Google Scholar
  58. Multhauf RP (1978) Neptune’s gift. A history of common salt. The Johns Hopkins University Press, Baltimore and LondonGoogle Scholar
  59. Nica SA, Meilă AM, Macovei L (2007) Speleotherapy (in Romanian). Rom J Rheumatol 4:269–273Google Scholar
  60. Nieto JJ (1991) The response of halophilic bacteria to heavy metals. In: Rodriguez-Valera F (ed) General and applied aspects of halophilic microorganisms. Plenum Press, New York and London, pp 173–179CrossRefGoogle Scholar
  61. O’Connor EM, Shand RF (2002) Halocins and sulfolobicins: the emerging story of archaeal protein and peptide antibiotics. J Ind Micrbiol Biotechnol 28:23–31Google Scholar
  62. Oncescu T, Oancea P, Enache M, Popescu G, Dumitru L, Kamekura M (2007) Halophilic bacteria are able to decontaminate dichlorvos, a pesticide, from saline environments. Cent Eur J Biol 2: 563–573CrossRefGoogle Scholar
  63. Oren A (2002) Preface. In: Halophilic microorganisms and their environments. Kluwer Academic Publishers, Dordrecht, pp xv–xviiiCrossRefGoogle Scholar
  64. Oren A (2004) Prokaryote diversity and taxonomy: current status and future challenges. Philos Trans R Soc Lond B 359:623–638CrossRefGoogle Scholar
  65. Park JS, Vreeland RH, Cho BC, Lowenstein TK, Timofeeff MN, Rosenzweig WD (2009) Haloarchaeal diversity in 23, 121 and 419 MYA salts. Geobiology 7:1–9CrossRefGoogle Scholar
  66. Popescu G, Dumitru L (2009) Biosorption of some heavy metals from media with high salt concentrations by halophilic Archaea. Biotechnol Biotechnol Eq 23:791–795Google Scholar
  67. Rees CH, Grant DW, Jones EB, Heaphy S (2004) Diversity of Kenyan soda lake alkaliphiles assessed by molecular methods. Extremophiles 8:63–71PubMedCrossRefGoogle Scholar
  68. Rodriguez-Valera F (1992) Biotechnological potential of halobacteria. Biochem Soc Symp 58:135–147PubMedGoogle Scholar
  69. Rodriguez-Valera F, Ruiz-Berraquero F, Ramos-Cormenzana A (1979) Isolation of extreme halophiles from seawater. Appl Environ Microbiol 38:164–165PubMedGoogle Scholar
  70. Rodriguez-Valera F, Juez G, Kushner DJ (1982) Halocins: salt-dependent bacteriocins produced by extremely halophilic rods. Can J Microbiol 28:151–154CrossRefGoogle Scholar
  71. Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487–491PubMedCrossRefGoogle Scholar
  72. Schuster B, Sleytr UB (2000) S-layer-supported lipid membranes. Rev Mol Biotechnol 74:233–254CrossRefGoogle Scholar
  73. Schuster B, Györvary E, Pum D, Sleytr UB (2005) Nanotechnology with S-layer protein. In: Vo-Dinh T (ed) Methods in molecular biology. vol 300: Protein nanotechnology, protocols, instrumentation and applications. Humana Press Inc., Totowa, NJ, pp 101–123Google Scholar
  74. Sencu V (1968) Salt Mount from Slănic Prahova (in Romanian). Ocrot Nat 12:167–179Google Scholar
  75. Shimane Y, Hatada Y, Minegishi H, Mizuki T, Echigo A, Miyazaki M, Ohta Y, Usami R, Grant WDGoogle Scholar
  76. Horikoshi K (2010) Natronoarchaeum mannanilyticum gen. nov., sp. nov., an aerobic, extremely halophilic member of the Archaea isolated from commercial salt made in Niigata, Japan. Int J Syst Evol Microbiol (in press). DOI: 10.1099/ijs.0.016600-0Google Scholar
  77. Simyonka YM (1989) Some particular features of infections and inflammatory processes, and immune status in patients with infection-dependent bronchial asthma during speleotherapy in salt-mine microclimate (in Russian). In: Bronchial asthma. Leningrad, pp 136–140Google Scholar
  78. Sleytr UB, Sara M (1997) Bacterial and archaeal S-layer proteins: structure-function relationships and their biotechnological applications. Trends Biotechnol 15:20–26PubMedCrossRefGoogle Scholar
  79. Sleytr UB, Messner P, Pum D, Sara M (1999) Crystalline bacterial cell surface layers (S-layers): from supramolecular cell structure to biomimetics and nanotechnology. Angew Chem 38:1034–1054CrossRefGoogle Scholar
  80. Stan-Lotter H, Radax C, Gruber C, Legat A, Pfaffenhuemer M, Wieland H, Leuko S, Weidler G, Kömle N, Kargle G (2003) Astrobiology with haloarchaea from Permo-Triassic rock salt. Int J Astrobiol 1:271–284CrossRefGoogle Scholar
  81. Teodosiu G, Dumitru L, Faghi AM (1999) The dynamic of the halophilic microorganisms growth at different values of pH and temperature. II. Extremely halophilic archaea. Proc Inst Biol 2: 163–168Google Scholar
  82. Thongthai C, McGenity TJ, Suntinanalert P, Grant WD (1992) Isolation and characterization of an extremely halophilic archaebacterium from traditionally fermented Thai fish sauce (nam-pla). Lett Appl Microbiol 14:111–114CrossRefGoogle Scholar
  83. Tindall BJ, Mills AA, Grant WD (1980) An alkalophilic red halophilic bacterium with low magnesium requirement from a Kenyan soda lake. J Gen Microbiol 116:257–260Google Scholar
  84. Tindall BJ, Ross HNM, Grant WD (1984) Natronobacterium gen. nov. and Natronococcus gen. nov., two new genera of haloalkaliphilic archaebacteria. Syst Appl Microbiol 5:41–57CrossRefGoogle Scholar
  85. Torreblanca M, Rodriguez-Valera F, Juez G, Ventosa A, Kamekura M, Kates M (1986) Classification of non-alkaliphilic halobacteria based on numerical taxonomy and polar lipid composition, and description of Haloarcula gen. nov. and Haloferax gen. nov. Syst Appl Microbiol 8:89–99CrossRefGoogle Scholar
  86. Torreblanca M, Meseguer I, Ventosa A (1994) Production of halocin is a practically universal feature of archaea halophilic rods. Lett Appl Microbiol 19:201–205CrossRefGoogle Scholar
  87. Trachtenberg S, Pinnick B, Kessel M (2000) The cell surface glycoprotein layer of the extreme halophile Halobacterium salinarum and its relation with Haloferax volcanii: cryo-electron tomography of freeze-substituted cells and projection studies of negatively stained envelopes. J Struct Biol 130:10–26PubMedCrossRefGoogle Scholar
  88. Vellieux F, Madern D, Zaccai G, Ebel C (2007) Molecular adaptation to high salt. In: Gerday C, Glansdorff N (eds) Physiology and biochemistry of extremophiles. ASM Press, Washington, DC, pp 240–253Google Scholar
  89. Ventosa A (2004) Halophilic microorganisms. Springer-Verlag, Berlin, HeidelbergGoogle Scholar
  90. Ventosa A, Nieto JJ, Oren A (1998) Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 62:504–544PubMedGoogle Scholar
  91. Ventosa A, Sanchez-Porro C, Martin S, Mellado E (2005) Halophilic archaea and bacteria as a source of extracellular hydrolytic enzymes. In: Gunde-Cimerman N, Oren A, Plemenitas A (eds) Adaptation to life at high salt concentrations in archaea, bacteria, and eukarya. Springer, Dordrecht, pp 337–354CrossRefGoogle Scholar
  92. Ventosa A, Mellado E, Sanchez-Porro C, Marquez MC (2008) Halophilic and halotolerant microorganism from soils. In: Dion P, Nautiyal CS (eds) Microbiology of extreme soils. Springer-Verlag, Berlin, Heidelberg, pp 87–115CrossRefGoogle Scholar
  93. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703PubMedGoogle Scholar
  94. Williams WD (1998) Guidelines of lake management, vol 6: Management of inland saline waters. In: International lake environment committee foundation and the United Nations environment programme, Kusatsu, JapanGoogle Scholar
  95. Xue Y, Fan H, Ventosa A, Grant WD, Jones BE, Cowan DA, Ma Y (2005) Halalkalicoccus tibetensis gen. nov., sp. nov., representing a novel genus of haloalkaliphilic archaea. Int J Syst Evol Microbiol 55:2501–2505PubMedCrossRefGoogle Scholar
  96. Yamamura A, Ichimura T, Kamekura M, Mizuki T, Usami R, Makino T, Ohtsuka J, Miyazono K, Okai M, Nagata K, Tanokura M (2009) Molecular mechanism of distinct salt-dependent enzyme activity of two halophilic nucleoside diphosphate kinases. Biophys J 96:4692–4700PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag/Wien 2012

Authors and Affiliations

  • Madalin Enache
    • 1
  • Gabriela Popescu
    • 1
  • Takashi Itoh
    • 2
  • Masahiro Kamekura
    • 3
  1. 1.Institute of Biology of the Romanian AcademyBucharestRomania
  2. 2.Japan Collection of MicroorganismsRIKEN BioResource CenterSaitamaJapan
  3. 3.Halophiles Research InstituteNodaJapan

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