Biochemistry (Moscow)

, Volume 83, Supplement 1, pp S56–S61 | Cite as

Archaeal Flagella as Biotemplates for Nanomaterials with New Properties

  • S. N. Beznosov
  • M. G. Pyatibratov
  • O. V. FedorovEmail author


At the end of 1980s, regions of the polypeptide chain of bacterial flagella subunits (flagellins) responsible for different properties of these protein polymers were identified by structural studies. It was found that the N-and C-terminal regions are responsible for the polymerization properties of subunits, and the central region is responsible for antigenic properties of the flagellum. Soon after that, it was proposed to use variability of the central flagellin domain for directed modification to impart new properties to the flagellum surface. Such studies of flagella and other polymeric structures of bacterial origin thrived. However bacterial polymers have some shortcomings, mainly their instability to dissociating effects. This shortcoming is absent in archaeal flagella. A limiting factor was the lack of the three-dimensional structure of archaeal flagellins. A method was developed that allowed modifying flagella of the halophilic archaeon Halobacterium salinarum in a peptide that connects positively charged ions. Later, corresponding procedures were used that allowed preparing the anode material for a lithiumion battery whose characteristics 4-5-fold exceeded those of batteries commonly used in industrial production. We describe other advantages of archaeal flagella over bacterial analogs when used in nanotechnology.


Archaea flagella archaella protein modification biotemplated nanomaterials 


  1. 1.
    Nam, K. T., Kim, D., Yoo, P. J., Chiang, C., Meethong, N., Hammond, P. T., Chiang, Y., and Belcher, A. M. (2006) Virus-enabled synthesis and assembly of nanowires for lithium ion battery electrodes, Science, 312, 885–888.CrossRefPubMedGoogle Scholar
  2. 2.
    Audette, G. F., and Hazes, B. (2007) Development of protein nanotubes from a multipurpose biological structure, J. Nanosci. Nanotechnol., 7, 2222–2229.CrossRefPubMedGoogle Scholar
  3. 3.
    Gazit, E. (2007) Use of biomolecular templates for the fabrication of metal nanowires, FEBS J., 274, 317–322.CrossRefPubMedGoogle Scholar
  4. 4.
    Kumara, M. T., Tripp, B. C., and Muralidharan, S. (2007) Self-assembly of metal nanoparticles and nanotubes on bioengineered flagella scaffolds, Chem. Mater., 19, 2056–2064.CrossRefGoogle Scholar
  5. 5.
    Yu, B., Giltner, C. L., Schaik, E. J., Bautista, D. L., Hodges, R. S., Audette, G. F., Li, D. Y., and Irvin, R. T. (2007) A novel biometallic interface: high affinity tipassociated binding by pilinderived protein nanotubes, J. Bionanosci., 1, 73–83.CrossRefGoogle Scholar
  6. 6.
    Atabekov, J. G. (2008) Using viral structures as nanotechnology instruments, Nanotechnologies in Russia, 3, 128–137.Google Scholar
  7. 7.
    Lee, Y. J., Yi, H., Kim, W., Kang, K., Yun, D. S., Strano, M. S., Ceder, G., and Belcher, A. M. (2009) Fabricating genetically engineered high-power lithium ion batteries using multiple virus genes, Science, 324, 1051–1055.PubMedGoogle Scholar
  8. 8.
    Ghosh, D., Lee, Y., Thomas, S., Kohli, A. G., Yun, D. S., Belcher, A. M., and Kelly, K. A. (2012) M13-templated magnetic nanoparticles for targeted in vivo imaging of prostate cancer, Nat. Nanotechnol., 10, 677–682.CrossRefGoogle Scholar
  9. 9.
    Fedorov, O. V., and Efimov, A. V. (1990) Flagellin as an object for supramolecular engineering, Prot. Eng., 3, 411–413.CrossRefGoogle Scholar
  10. 10.
    Jarrell, K. F., Bayley, D. P., and Faguy, D. M. (1993) Structure, molecular sequence analysis and genetics of the flagella of the domain Archaea: comparison with bacterial flagella, Curr. Top. Mol. Genet., 1, 15–31.Google Scholar
  11. 11.
    Fedorov, O. V., Pyatibratov, M. G., Kostyukova, A. S., Osina, N. K., and Tarasov, V. Y. (1994) Protofilament as a structural element of flagella of haloalkaliphilic archaebacteria, Can. J. Microbiol., 40, 45–53.CrossRefGoogle Scholar
  12. 12.
    Jarrell, K. F., and Albers, S. V. (2012) The archaellum: an old motility structure with a new name, Trends Microbiol., 20, 307–312.CrossRefPubMedGoogle Scholar
  13. 13.
    Wang, Q., Suzuki, A., Mariconda, S., Porwollik, S., and Harshey, R. M. (2005) Sensing wetness: a new role for the bacterial flagellum, EMBO J., 24, 2034–2042.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    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.PubMedGoogle Scholar
  15. 15.
    Haiko, J., and Westerlund-Wikstrom, B. (2013) The role of the bacterial flagellum in adhesion and virulence, Biology, 2, 1242–1267.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Friedlander, R. S., Vogel, N., and Aizenberg, J. (2015) Role of flagella in adhesion of Escherichia coli to abiotic surfaces, Langmuir, 31, 6137–6144.CrossRefPubMedGoogle Scholar
  17. 17.
    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, Cent. Eur. J. Biol., 8, 828–834.Google Scholar
  18. 18.
    Beznosov, S. N., Veluri, P. S., Pyatibratov, M. G., Chatterjee, A., MacFarlane, D. R., Fedorov, O. V., and Mitra, S. (2015) Flagellar filament biotemplated inorganic oxide materials–towards an efficient lithium battery anode, Sci. Rep., 5, 7736.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Poweleit, N., Ge, P., Nguyen, H. H., Loo, R. R. O., Gunsalus, R. P., and Zhou, Z. H. (2016) CryoEM structure of the Methanospirillum hungatei archaellum reveals structural features distinct from the bacterial flagellum and type IV pilus, Nat. Microbiol., 2, 16222.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Fedorov, O. V., Kostyukova, A. S., and Pyatibratov, M. G. (1988) Architectonics of a bacterial flagellin filament subunit, FEBS Lett., 241, 145–148.CrossRefPubMedGoogle Scholar
  21. 21.
    Kumara, M. T., Tripp, B. C., and Muralidharan, S. (2007) Layer-by-layer assembly of bioengineered flagella protein nanotubes, Biomacromolecules, 8, 3718–3722.CrossRefPubMedGoogle Scholar
  22. 22.
    Thai, C. K., Dai, H., Sastry, M. S., Sarikaya, M., Schwartz, D. T., and Baneyx, F. (2004) Identification and characterization of Cu2O-and ZnO-binding polypeptides by Escherichia coli cell surface display: toward an understanding of metal oxide binding, Biotechnol. Bioeng., 87, 129–137.CrossRefPubMedGoogle Scholar
  23. 23.
    Kumara, M. T., Srividya, N., Muralidharan, S., and Tripp, B. C. (2006) Bioengineered flagella protein nanotubes with cysteine loops: self-assembly and manipulation in an optical trap, Nano Lett., 6, 2121–2129.CrossRefPubMedGoogle Scholar
  24. 24.
    Woods, R. D., Takahashi, N., Aslam, A., Pleass, R. J., Aizawa, S., and Sockett, R. E. (2007) Bifunctional nanotube scaffolds for diverse ligands are purified simply from Escherichia coli strains coexpressing two functionalized flagellar genes, Nano Lett., 7, 1809–1816.CrossRefPubMedGoogle Scholar
  25. 25.
    Deplanche, K., Woods, R. D., Mikheenko, I. P., Sockett, R. E., and Macaskie, L. E. (2008) Manufacture of stable palladium and gold nanoparticles on native and genetically engineered flagella scaffolds, Biotechnol. Bioeng., 101, 873–880.CrossRefPubMedGoogle Scholar
  26. 26.
    Westerlund-Wikstrom, B., Tanskanen, J., Virkola, R., Hacker, J., Lindberg, M., Skurnik, M., and Korhonen, T. K. (1997) Functional expression of adhesive peptides as fusions to Escherichia coli flagellin, Prot. Eng., 10, 1319–1326.CrossRefGoogle Scholar
  27. 27.
    Lee, Y., Kim, J., Yun, D. S., Nam, Y. S., Shao-Horn, Y., and Belcher, A. M. (2012) Virus-templated Au and Au–Pt core–shell nanowires and their electrocatalytic activities for fuel cell applications, Energy Environ. Sci., 5, 8328–8334.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Chen, P.-Y., Ladewski, R., Miller, R., Dang, X., Qi, J., Liau, F., Belcher, A. M., and Hammond, P. T. (2013) Layer-by-layer assembled porous photoanodes for efficient electron collection in dyesensitized solar cells, J. Mater. Chem. A, 1, 2217–2224.CrossRefGoogle Scholar
  29. 29.
    Mao, C., Solis, D. J., Reiss, B. D., Kottmann, S. T., Sweeney, R. Y., Hayhurst, A., Georgiou, G., Iverson, B., and Belcher, A. M. (2004) Virus-based toolkit for the directed synthesis of magnetic and semiconducting nanowires, Science, 303, 213–217.CrossRefPubMedGoogle Scholar
  30. 30.
    Petrov, A., Lombardo, S., and Audette, G. F. (2013) Fibrilmediated oligomerization of pilinderived protein nanotubes, J. Nanobiotechnol., 11,24.CrossRefGoogle Scholar
  31. 31.
    Rothemund, P. W. K. (2006) Folding DNA to create nanoscale shapes and patterns, Nature, 440, 297–302.CrossRefPubMedGoogle Scholar
  32. 32.
    Peng, L., Wu, C., You, M., Han, D., Chen, Y., Fu, T., Ye, M., and Tan, W. (2013) Engineering and applications of DNA-grafting polymer materials, Chem. Sci., 4, 1928–1938.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Yevdokimov, Y. M., and Sytchev, V. V. (2007) Nanotechnology and nucleic acids, Open Nanosci. J., 1, 19–31.CrossRefGoogle Scholar
  34. 34.
    Xiong, X., Wu, C., Zhou, C., Zhu, G., Chen, Z., and Tan, W. (2013) Responsive DNA-based hydrogels and their applications, Macromol. Rapid. Commun., 34, 1271–1283.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Sleytr, U. B., Pum, D., and Sara, M. (1997) Advances in Slayer nanotechnology and biomimetics, Adv. Biophys., 34, 71–79.CrossRefPubMedGoogle Scholar
  36. 36.
    Kovalenko, I., Zdyrko, B., Magasinski, A., Hertzberg, B., Milicev, Z., Burtovyy, R., Luzinov, I., and Yushin, G. (2011) A major constituent of brown algae for use in high-capacity Liion batteries, Science, 334, 75–79.CrossRefPubMedGoogle Scholar
  37. 37.
    Mashaghi, S., Jadidi, T., Koenderink, G., and Mashaghi, A. (2013) Lipid nanotechnology, Int. J. Mol. Sci., 14, 4242–4282.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Beznosov, S. N., Pyatibratov, M. G., and Fedorov, O. V. (2009) Archaeal flagella as matrices for new nanomaterials, Nanotechnologies in Russia, 4, 373–378.CrossRefGoogle Scholar
  39. 39.
    Tarasov, V. Yu., 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. Prot. Chem., 14, 27–31.CrossRefGoogle Scholar
  40. 40.
    Alam, M., and Oesterhelt, D. (1984) Morphology, function and isolation of halobacterial flagella, J. Mol. Biol., 176, 459–475.PubMedGoogle Scholar
  41. 41.
    Jarrell, K. F., Stark, M., Nair, D. B., and Chong, J. P. (2011) Flagella and pili are both necessary for efficient attachment of Methanococcus maripaludis to surfaces, FEMS Microbiol. Lett., 319, 44–50.CrossRefPubMedGoogle Scholar
  42. 42.
    Bardy, S. L., Mori, T., Komoriya, K., Aizawa, S., and Jarrell, K. F. (2002) Identification and localization of flagellins FlaA and FlaB3 within flagella of Methanococcus voltae, J. Bacteriol., 184, 5223–5233.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Sumper, M. (1987) Halobacterial glycoprotein biosynthesis, Biochim. Biophys. Acta, 906, 69–79.CrossRefPubMedGoogle Scholar
  44. 44.
    Yaroslavtsev, A. B., Kulova, T. L., and Skundin, A. M. (2015) Electrode nanomaterials for lithiumion batteries, Russ. Chem. Rev., 84, 826–852.CrossRefGoogle Scholar
  45. 45.
    Beznosov, S. N., Pyatibratov, M. G., Fedorov, O. V., Kulova, T. L., and Skundin, A. M. (2011) Electrochemical properties of nanostructured material based on modified flagella of halophilic archaea Halobacterium salinarum for negative electrode of lithiumion battery, Nanotechnologies in Russia, 6, 705–710.CrossRefGoogle Scholar
  46. 46.
    Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Cassarino, T. G., Bertoni, M., Bordoli, L., and Schwede, T. (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information, Nucleic Acids Res., 42, W252–W258.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Wu, C. H., Liu, I. J., Lu, R. M., and Wu, H. C. (2016) Advancement and applications of peptide phage display technology in biomedical science, J. Biomed. Sci., 23, 8.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • S. N. Beznosov
    • 1
  • M. G. Pyatibratov
    • 1
  • O. V. Fedorov
    • 1
    Email author
  1. 1.Institute of Protein ResearchRussian Academy of SciencesPushchinoRussia

Personalised recommendations