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Biochemistry (Moscow)

, Volume 79, Issue 13, pp 1470–1482 | Cite as

Flagella of halophilic archaea: Differences in supramolecular organization

  • A. S. Syutkin
  • M. G. PyatibratovEmail author
  • O. V. FedorovEmail author
Review

Abstract

Archaeal flagella are similar functionally to bacterial flagella, but structurally they are completely different. Helical archaeal flagellar filaments are formed of protein subunits called flagellins (archaellins). Notwithstanding progress in studies of archaeal flagella achieved in recent years, many problems in this area are still unsolved. In this review, we analyze the formation of these supramolecular structures by the example of flagellar filaments of halophilic archaea. Recent data on the structure of the flagellar filaments demonstrate that their supramolecular organization differs considerably in different haloarchaeal species.

Key words

archaea flagella archaella flagellin supramolecular structure halophilic 

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References

  1. 1.
    Woese, C. R., and Fox, G. E. (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms, Proc. Natl. Acad. Sci. USA, 74, 5088–5090.PubMedCentralPubMedCrossRefGoogle Scholar
  2. 2.
    Vorob’eva, L. I. (2007) Archaea [in Russian], Akademkniga, Moscow.Google Scholar
  3. 3.
    Jarrell, K. F., and Albers, S. V. (2012) The archaellum: an old motility structure with a new name, Trends Microbiol., 20, 307–312.PubMedCrossRefGoogle Scholar
  4. 4.
    Fedorov, O. V. (1998) Protein co-assembly folding as a mechanism of supramolecular structure formation, Uspekhi Biol. Khim., 38, 239–256.Google Scholar
  5. 5.
    Calladine, C. R. (1978) Change of waveform in bacterial flagella: the role of mechanics at the molecular level, J. Mol. Biol., 118, 457–479.CrossRefGoogle Scholar
  6. 6.
    Faulds-Pain, A., Birchall, C., Aldridge, C., Smith, W. D., Grimaldi, G., Nakamura, S., Miyata, T., Gray, J., Li, G., Tang, J. X., Namba, K., Minamino, T., and Aldridge, P. D. (2011) Flagellin redundancy in Caulobacter crescentus and its implications for flagellar filament assembly, J. Bacteriol., 193, 2695–2707.PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Silverman, M., Zieg, J., Hilmen, M., and Simon, M. (1979) Phase variation in Salmonella: genetic analysis of a recombinational switch, Proc. Natl. Acad. Sci. USA, 76, 391–395.PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Alam, M., and Oesterhelt, D. (1984) Morphology, function and isolation of halobacterial flagella, J. Mol. Biol., 176, 459–475.PubMedCrossRefGoogle Scholar
  9. 9.
    Wirth, R. (2012) Response to Jarrell and Albers: seven letters less does not say more, Trends Microbiol., 20, 511–512.PubMedCrossRefGoogle Scholar
  10. 10.
    Tripepi, M., Esquivel, R. N., Wirth, R., and Pohlschroder, M. (2013) Haloferax volcanii cells lacking the flagellin FlgA2 are hypermotile, Microbiology, 159, 2249–2258.PubMedCentralPubMedCrossRefGoogle Scholar
  11. 11.
    Herzog, B., and Wirth, R. (2012) Swimming behavior of selected species of Archaea, Appl. Environ. Microb., 78, 1670–1674.CrossRefGoogle Scholar
  12. 12.
    Nather, D. J., Rachel, R., Wanner, G., and Wirth, R. (2006) Flagella of Pyrococcus furiosus: multifunctional organelles, made for swimming, adhesion to various surfaces, and cell-cell contacts, J. Bacteriol., 188, 6915–6923.PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Jarrell, K. F., Ding, Y., Nair, D. B., and Siu, S. (2013) Surface appendages of archaea: structure, function, genetics and assembly, Life, 3, 86–117.PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Patenge, N., Berendes, A., Engelhardt, H., Schuster, S. C., and Oesterhelt, D. (2001) The fla gene cluster is involved in the biogenesis of flagella in Halobacterium salinarum, Mol. Microbiol., 41, 653–663.PubMedCrossRefGoogle Scholar
  15. 15.
    Chaban, B., Ng, S. Y., Kanbe, M., Saltzman, I., Nimmo, G., Aizawa, S. I., and Jarrell, K. F. (2007) Systematic deletion analyses of the fla genes in the flagella operon identify several genes essential for proper assembly and function of flagella in the archaeon, Methanococcus maripaludis, Mol. Microbiol., 66, 596–609.PubMedCrossRefGoogle Scholar
  16. 16.
    Lassak, K., Neiner, T., Ghosh, A., Klingl, A., Wirth, R., and Albers, S. (2012) Molecular analysis of the crenarchaeal flagellum, Mol. Microbiol., 83, 110–124.PubMedCrossRefGoogle Scholar
  17. 17.
    Schlesner, M., Miller, A., Streif, S., Staudinger, W. F., Muller, J., Scheffer, B., and Oesterhelt, D. (2009) Identification of Archaea-specific chemotaxis proteins which interact with the flagellar apparatus, BMC Microbiol., 9, 56.PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Ghosh, A., and Albers, S. V. (2011) Assembly and function of the archaeal flagellum, Biochem. Soc. Transact., 39, 64–69.CrossRefGoogle Scholar
  19. 19.
    Banerjee, A., Ghosh, A., Mills, D. J., Kahnt, J., Vonck, J., and Albers, S. V. (2012) FlaX, a unique component of the crenarchaeal archaellum, forms oligomeric ring-shaped structures and interacts with the motor ATPase FlaI, J. Biol. Chem., 287, 43322–43330.PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Thomas, N. A., and Jarrell, K. F. (2001) Characterization of flagellum gene families of methanogenic archaea and localization of novel flagellum accessory proteins, J. Bacteriol., 183, 7154–7164.PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.
    Ghosh, A., Hartung, S., van der Does, C., Tainer, J. A., and Albers, S. V. (2011) Archaeal flagellar ATPase motor shows ATP-dependent hexameric assembly and activity stimulation by specific lipid binding, Biochem. J., 437, 43–52.PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Kalmokoff, M. L., and Jarrell, K. F. (1991) Cloning and sequencing of a multigene family encoding the flagellins of Methanococcus voltae, J. Bacteriol., 173, 7113–7125.PubMedCentralPubMedGoogle Scholar
  23. 23.
    Bardy, S. L., and Jarrell, K. F. (2002) FlaK of the archaeon Methanococcus maripaludis possesses preflagellin peptidase activity, FEMS Microbiol. Lett., 208, 53–59.PubMedCrossRefGoogle Scholar
  24. 24.
    Bardy, S. L., and Jarrell, K. F. (2003) Cleavage of preflagellins by an aspartic acid signal peptidase is essential for flagellation in the archaeon Methanococcus voltae, Mol. Microbiol., 50, 1339–1347.PubMedCrossRefGoogle Scholar
  25. 25.
    Szabo, Z., Albers, S. V., and Driessen, A. J. M. (2006) Active-site residues in the type IV prepilin peptidase homologue PibD from the archaeon Sulfolobus solfataricus, J. Bacteriol., 188, 1437–1443.PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Ng, S. Y., Chaban, B., and Jarrell, K. F. (2006) Archaeal flagella, bacterial flagella and type IV pili: a comparison of genes and posttranslational modifications, J. Mol. Microbiol. Biotechnol., 11, 167–191.PubMedCrossRefGoogle Scholar
  27. 27.
    Tripepi, M., Imam, S., and Pohlschroder, M. (2010) Haloferax volcanii flagella are required for motility but are not involved in PibD-dependent surface adhesion, J. Bacteriol., 192, 3093–3102.PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Mukhopadhyay, B., Johnson, E. F., and Wolfe, R. S. (2000) A novel pH2 control on the expression of flagella in the hyperthermophilic strictly hydrogenotrophic methanarchaeaon Methanococcus jannaschii, Proc. Natl. Acad. Sci. USA, 97, 11522–11527.PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Hendrickson, E. L., Liu, Y., Rosas-Sandoval, G., Porat, I., Soll, D., Whitman, W. B., and Leigh, J. A. (2008) Global responses of Methanococcus maripaludis to specific nutrient limitations and growth rate, J. Bacteriol., 190, 2198–2205.PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Szabo, Z., Sani, M., Groeneveld, M., Zolghadr, B., Schelert, J., Albers, S. V., and Driessen, A. J. (2007) Flagellar motility and structure in the hyperthermoacidophilic archaeon Sulfolobus solfataricus, J. Bacteriol., 189, 4305–4309.PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    Reimann, J., Lassak, K., Khadouma, S., Ettema, T. J., Yang, N., Driessen, A. J., Klingl, A., and Albers, S. V. (2012) Regulation of archaella expression by the FHA and von Willebrand domain-containing proteins ArnA and ArnB in Sulfolobus acidocaldarius, Mol. Microbiol., 86, 24–36.PubMedCrossRefGoogle Scholar
  32. 32.
    Lassak, K., Peeters, E., Wrobel, S., and Albers, S. V. (2013) The one-component system ArnR: a membrane-bound activator of the crenarchaeal archaellum, Mol. Microbiol., 88, 125–139.PubMedCrossRefGoogle Scholar
  33. 33.
    Thomas, A. N., Bardy, B. L., and Jarrell, K. F. (2001) The archaeal flagellum: a different kind of prokaryotic motility structure, FEMS Microbiol. Rev., 25, 147–174.PubMedCrossRefGoogle Scholar
  34. 34.
    Kalmokoff, M. L., Jarrell, K. F., and Koval, S. F. (1988) Isolation of flagella from the archaebacterium Methanococcus voltae by phase separation with Triton X-114, J. Bacteriol., 170, 1752–1758.PubMedCentralPubMedGoogle Scholar
  35. 35.
    Cruden, D., Sparling, R., and Markovetz, A. J. (1989) Isolation and ultrastructure of the flagella of Methanococcus thermolithotrophicus and Methanospirillum hungatei, Appl. Environ. Microbiol., 55, 1414–1419.PubMedCentralPubMedGoogle Scholar
  36. 36.
    Kupper, J., Marwan, W., Typke, D., Grunberg, H., Uwer, U., Gluch, M., and Oesterhelt, D. (1994) The flagellar bundle of Halobacterium salinarium is inserted into a distinct polar cap structure, J. Bacteriol., 176, 5184–5187.PubMedCentralPubMedGoogle Scholar
  37. 37.
    Bakeeva, L. E., Metlina, A. L., Novikova, T. M., and Speransky, V. V. (1992) The ultrastructure of the flagellar apparatus of Halobacterium salinarium, Doklady Akad. Nauk, 326, 914–915.Google Scholar
  38. 38.
    Metlina, A. L. (2001) Prokaryotic flagella as biological motility system, Uspekhi Biol. Khim., 41, 229–282.Google Scholar
  39. 39.
    Metlina, A. L. (2004) Bacterial and archaeal flagella as prokaryotic motility organelles, Biochemistry (Moscow), 69, 1203–1212.CrossRefGoogle Scholar
  40. 40.
    Streif, S., Staudinger, W. F., Marwan, W., and Oesterhelt, D. (2008) Flagellar rotation in the archaeon Halobacterium salinarum depends on ATP, J. Mol. Biol., 384, 1–8.PubMedCrossRefGoogle Scholar
  41. 41.
    Reindl, S., Ghosh, A., Williams, G. J., Lassak, K., Neiner, T., Henche, A. L., Albers, S. V., and Tainer, J. A. (2013) Insights into FlaI functions in archaeal motor assembly and motility from structures, conformations, and genetics, Mol. Cell, 49, 1069–1082.PubMedCentralPubMedCrossRefGoogle Scholar
  42. 42.
    Banerjee, A., Neiner, T., Tripp, P., and Albers, S. V. (2013) Insights into subunit interactions in the Sulfolobus acidocaldarius archaellum cytoplasmic complex, FEBS J., 280, 6141–6149.PubMedCrossRefGoogle Scholar
  43. 43.
    Cohen-Krausz, S., and Trachtenberg, S. (2002) The structure of the archeabacterial flagellar filament of the extreme halophile Halobacterium salinarum R1M1 and its relation to eubacterial flagellar filaments and type IV pili, J. Mol. Biol., 321, 383–395.PubMedCrossRefGoogle Scholar
  44. 44.
    Trachtenberg, S., Galkin, V. E., and Egelman, E. H. (2005) Refining the structure of the Halobacterium salinarum flagellar filament using the iterative helical real space reconstruction method: insights into polymorphism, J. Mol. Biol., 346, 665–676.PubMedCrossRefGoogle Scholar
  45. 45.
    Cohen-Krausz, S., and Trachtenberg, S. (2008) The flagellar filament structure of the extreme acidothermophile Sulfolobus shibatae B12 suggests that archeabacterial flagella have a unique and common symmetry and design, J. Mol. Biol., 375, 1113–1124.PubMedCrossRefGoogle Scholar
  46. 46.
    Kalmokoff, M. L., Karnauchow, T. M., and Jarrell, K. F. (1990) Conserved N-terminal sequences in the flagellins of archaebacterial, Biochem. Biophys. Res. Commun., 167, 154–160.PubMedCrossRefGoogle Scholar
  47. 47.
    Bardy, S. L., Eichler, J., and Jarrell, K. F. (2003) Archaeal signal peptides — a comparative survey at the genome level, Protein Sci., 12, 1833–1843.PubMedCentralPubMedCrossRefGoogle Scholar
  48. 48.
    Tarasov, V. Y., Kostyukova, A. S., Tiktopulo, E. I., Pyatibratov, M. G., and Fedorov, O. V. (1995) Unfolding of tertiary structure of Halobacterium halobium flagellins does not result in flagella destruction, J. Protein Chem., 14, 27–31.PubMedCrossRefGoogle Scholar
  49. 49.
    Pyatibratov, M. G., Kostyukova, A. S., Tarasov, V. Yu., and Fedorov, O. V. (1996) Some principles of formation of the haloalkaliphilic archaeal flagellar structure, Biochemistry (Moscow), 61, 1056–1062.Google Scholar
  50. 50.
    Calo, D., Kaminski, L., and Eichler, J. (2010) Protein glycosylation in Archaea: sweet and extreme, Glycobiology, 20, 1065–1076.PubMedCrossRefGoogle Scholar
  51. 51.
    Mescher, M. F., and Strominger, J. L. (1976) Purification and characterization of a prokaryotic glucoprotein from the cell envelope of Halobacterium salinarium, J. Biol. Chem., 251, 2005–2014.PubMedGoogle Scholar
  52. 52.
    Sumper, M. (1987) Halobacterial glycoprotein biosynthesis, Biochim. Biophys. Acta (BBA) — Rev. Biomembr., 906, 69–79.CrossRefGoogle Scholar
  53. 53.
    Tripepi, M., You, J., Temel, S., Onder, O., Brisson, D., and Pohlschroder, M. (2012) N-glycosylation of Haloferax volcanii flagellins requires known Agl proteins and is essential for biosynthesis of stable flagella, J. Bacteriol., 194, 4876–4887.PubMedCentralPubMedCrossRefGoogle Scholar
  54. 54.
    Meyer, B. H., and Albers, S. V. (2014) AglB catalyzing the oligosaccharyl transferase step of the archaeal N-glycosylation process is essential in the thermoacidophilic crenarchaeon Sulfolobus acidocaldarius, MicrobiologyOpen, 3, 531–543.PubMedCrossRefGoogle Scholar
  55. 55.
    Guan, Z., Naparstek, S., Calo, D., and Eichler, J. (2012) Protein glycosylation as an adaptive response in Archaea: growth at different salt concentrations leads to alterations in Haloferax volcanii S-layer glycoprotein N-glycosylation, Environ. Microbiol., 14, 743–753.PubMedCentralPubMedCrossRefGoogle Scholar
  56. 56.
    Wieland, F., Paul, G., and Sumper, M. (1985) Halobacterial flagellins are sulfated glycoproteins, J. Biol. Chem., 260, 15180–15185.PubMedGoogle Scholar
  57. 57.
    Voisin, S., Houliston, R. S., Kelly, J., Brisson, J. R., Watson, D., Bardy, S. L., Jarrell, K. F., and Logan, S. M. (2005) Identification and characterization of the unique N-linked glycan common to the flagellins and S-layer glycoprotein of Methanococcus voltae, J. Biol. Chem., 280, 16586–16593.PubMedCrossRefGoogle Scholar
  58. 58.
    Kelly, J., Logan, S. M., Jarrell, K. F., Vandyke, D. J., and Vinogradov, E. (2009) A novel N-linked flagellar glycan from Methanococcus maripaludis, Carbohydr. Res., 344, 648–653.PubMedCrossRefGoogle Scholar
  59. 59.
    Chaban, B., Voisin, S., Kelly, J., Logan, S. M., and Jarrell, K. F. (2006) Identification of genes involved in the biosynthesis and attachment of Methanococcus voltae N-linked glycans: insight into N-linked glycosylation pathways in Archaea, Mol. Microbiol., 61, 259–268.PubMedCrossRefGoogle Scholar
  60. 60.
    Vandyke, D. J., Wu, J., Logan, S. M., Kelly, J. F., Mizuno, S., Aizawa, S. I., and Jarrell, K. F. (2009) Identification of genes involved in the assembly and attachment of a novel flagellin N-linked tetrasaccharide important for motility in the archaeon Methanococcus maripaludis, Mol. Microbiol., 72, 633–644.PubMedCrossRefGoogle Scholar
  61. 61.
    Gerl, L., and Sumper, M. (1988) Halobacterial flagellins are encoded by a multigene family. Characterization of five flagellin genes, J. Biol. Chem., 263, 13246–13251.PubMedGoogle Scholar
  62. 62.
    Gerl, L., Deutzmann, R., and Sumper, M. (1989) Halobacterial flagellins are encoded by a multigene family Identification of all five gene products, FEBS Lett., 244, 137–140.PubMedCrossRefGoogle Scholar
  63. 63.
    Tarasov, V. Y., Pyatibratov, M. G., Tang, S. L., Dyall-Smith, M., and Fedorov, O. V. (2000) Role of flagellins from A and B loci in flagella formation of Halobacterium salinarum, Mol. Microbiol., 35, 69–78.PubMedCrossRefGoogle Scholar
  64. 64.
    Tarasov, V. Y., Pyatibratov, M. G., Beznosov, S. N., and Fedorov, O. V. (2004) On the supramolecular organization of the flagellar filament in Archaea, Doklady Biochem. Biophys., 396, 203–205.CrossRefGoogle Scholar
  65. 65.
    Pyatibratov, M. G., Leonard, K., Tarasov, V. Y., and Fedorov, O. V. (2002) Two immunologically distinct types of protofilaments can be identified in Natrialba magadii flagella, FEMS Microbiol. Lett., 212, 23–27.PubMedCrossRefGoogle Scholar
  66. 66.
    Beznosov, S. N., Pyatibratov, M. G., and Fedorov, O. V. (2007) On the multicomponent nature of Halobacterium salinarum flagella, Microbiology (Moscow), 76, 435–441.CrossRefGoogle Scholar
  67. 67.
    Beznosov, S. N., Pyatibratov, M. G., and Fedorov, O. V. (2009) Archaeal flagella as matrices for new nanomaterials, Nanotechnol. Russia, 4, 373–378.CrossRefGoogle Scholar
  68. 68.
    Beznosov, S. N., Pyatibratov, M. G., Veluri, P. S., Mitra, S., and Fedorov, O. V. (2013) A way to identify archaellins in Halobacterium salinarum archaella by FLAG-tagging, Centr. Europ. J. Biol., 8, 828–834.CrossRefGoogle Scholar
  69. 69.
    Lewus, P., and Ford, R. M. (1999) Temperature-sensitive motility of Sulfolobus acidocaldarius influences population distribution in extreme environments, J. Bacteriol., 181, 4020–4025.PubMedCentralPubMedGoogle Scholar
  70. 70.
    Baliga, N. S., Bonneau, R., Facciotti, M. T., Pan, M., Glusman, G., Deutsch, E. W., and Ng, W. V. (2004) Genome sequence of Haloarcula marismortui: a halophilic archaeon from the Dead Sea, Genome Res., 14, 2221–2234.PubMedCentralPubMedCrossRefGoogle Scholar
  71. 71.
    Oren, A., Ginzburg, M., Ginzburg, B. Z., Hochstein, L. I., and Volcani, B. E. (1990) Haloarcula marismortui (Volcani) sp. nov., nom. rev., an extremely halophilic bacterium from the Dead Sea, Int. J. System. Bacteriol., 40, 209–210.CrossRefGoogle Scholar
  72. 72.
    Pyatibratov, M. G., Beznosov, S. N., Rachel, R., Tiktopulo, E. I., Surin, A. K., Syutkin, A. S., and Fedorov, O. V. (2008) Alternative flagellar filament types in the haloarchaeon Haloarcula marismortui, Canad. J. Microbiol., 54, 835–844.CrossRefGoogle Scholar
  73. 73.
    Matagne, A., Joris, B., and Frere, J. M. (1991) Anomalous behavior of a protein during SDS/PAGE corrected by chemical modification of carboxylic groups, Biochem. J., 280, 553–556.PubMedCentralPubMedGoogle Scholar
  74. 74.
    Ikeda, J. S., Schmitt, C. K., Darnell, S. C., Watson, P. R., Bispham, J., Wallis, T. S., and O’Brien, A. D. (2001) Flagellar phase variation of Salmonella enterica serovar Typhimurium contributes to virulence in the murine typhoid infection model but does not influence Salmonella-induced enteropathogenesis, Infect. Immun., 69, 3021–3030.PubMedCentralPubMedCrossRefGoogle Scholar
  75. 75.
    Syutkin, A. S., Pyatibratov, M. G., Galzitskaya, O. V., Rodriguez-Valera, F., and Fedorov, O. V. (2014) Haloarcula marismortui archaellin genes as ecoparalogs, Extremophiles, 18, 341–349.PubMedCrossRefGoogle Scholar
  76. 76.
    Syutkin, A. S., Pyatibratov, M. G., Beznosov, S. N., and Fedorov, O. V. (2012) Various mechanisms of flagella helicity formation in haloarchaea, Microbiology (Moscow), 81, 573–581.CrossRefGoogle Scholar
  77. 77.
    Valliere-Douglass, J. F., Eakin, C. M., Wallace, A., Ketchem, R. R., Wang, W., Treuheit, M. J., and Balland, A. (2010) Glutamine-linked and non-consensus asparagine-linked oligosaccharides present in human recombinant antibodies define novel protein glycosylation motifs, J. Biol. Chem., 285, 16012–16022.PubMedCentralPubMedCrossRefGoogle Scholar
  78. 78.
    Franzmann, P. D., Stackebrandt, E., Sanderson, K., Volkman, J. K., Cameron, D. E., Stevenson, P. L., and Burton, H. R. (1988) Halobacterium lacusprofundi sp. nov., a halophilic bacterium isolated from Deep Lake, Antarctica, System. Appl. Microbiol., 11, 20–27.CrossRefGoogle Scholar
  79. 79.
    Tu, D., Blaha, G., Moore, P. B., and Steitz, T. A. (2005) Gene replacement in Haloarcula marismortui: construction of a strain with two of its three chromosomal rRNA operons deleted, Extremophiles, 9, 427–435.PubMedCrossRefGoogle Scholar
  80. 80.
    Lopez-Lopez, A., Benlloch, S., Bonfa, M., Rodriguez-Valera, F., and Mira, A. (2007) Intragenomic 16S rDNA divergence in Haloarcula marismortui is an adaptation to different temperatures, J. Mol. Evol., 65, 687–696.PubMedCrossRefGoogle Scholar
  81. 81.
    Sanchez-Perez, G., Mira, A., Nyiro, G., Pasic, L., and Rodriguez-Valera, F. (2008) Adapting to environmental changes using specialized paralogs, Trends Genet., 24, 154–158.PubMedCrossRefGoogle Scholar
  82. 82.
    Bodaker, I., Sharon, I., Suzuki, M. T., Feingersch, R., Shmoish, M., Andreishcheva, E., Sogin, M. L., Rosenberg, M., Maguire, M. E., Belkin, S., Oren, A., and Beja, O. (2010) Comparative community genomics in the Dead Sea: an increasingly extreme environment, ISME J., 4, 399–407.PubMedCrossRefGoogle Scholar
  83. 83.
    Williams, D., Gogarten, J. P., and Papke, R. T. (2012) Quantifying homologous replacement of loci between haloarchaeal species, Genome Biol. Evol., 4, 1223–1244.PubMedCentralPubMedCrossRefGoogle Scholar
  84. 84.
    Allers, T., Barak, S., Liddell, S., Wardell, K., and Mevarech, M. (2010) Improved strains and plasmid vectors for conditional overexpression of His-tagged proteins in Haloferax volcanii, Appl. Environ. Microbiol., 76, 1759–1769.PubMedCentralPubMedCrossRefGoogle Scholar
  85. 85.
    Deutscher, L., Renner, L. D., and Cuniberti, G. (2014) Flagella — templates for the synthesis of metallic nanowires, IFMBE Proc., 41, 860–863.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2014

Authors and Affiliations

  1. 1.Institute of Protein ResearchRussian Academy of SciencesPushchino, Moscow RegionRussia

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