Propulsion of African trypanosomes is driven by bihelical waves with alternating chirality separated by kinks

  1. Jose A. Rodrígueza,b,
  2. Miguel A. Lopezc,
  3. Michelle C. Thayerc,
  4. Yunzhe Zhaod,
  5. Michael Oberholzerc,
  6. Donald D. Changd,
  7. Neville K. Kisaluc,
  8. Manuel L. Penicheta,b,c,
  9. Gustavo Helguerab,
  10. Robijn Bruinsmad,
  11. Kent L. Hilla,c and
  12. Jianwei Miaod,1
  1. aMolecular Biology Institute,
  2. bDepartment of Surgery, Division of Surgical Oncology, and
  3. cDepartment of Microbiology Immunology and Molecular Genetics, The David Geffen School of Medicine, and
  4. dDepartment of Physics and Astronomy, University of California, Los Angeles, CA 90095
  1. Edited by Howard C. Berg, Harvard University, Cambridge, MA, and approved September 16, 2009 (received for review June 23, 2009)

Abstract

Trypanosoma brucei, a parasitic protist with a single flagellum, is the causative agent of African sleeping sickness. Propulsion of T. brucei was long believed to be by a drill-like, helical motion. Using millisecond differential interference-contrast microscopy and analyzing image sequences of cultured procyclic-form and bloodstream-form parasites, as well as bloodstream-form cells in infected mouse blood, we find that, instead, motility of T. brucei is by the propagation of kinks, separating left-handed and right-handed helical waves. Kink-driven motility, previously encountered in prokaryotes, permits T. brucei a helical propagation mechanism while avoiding the large viscous drag associated with a net rotation of the broad end of its tapering body. Our study demonstrates that millisecond differential interference-contrast microscopy can be a useful tool for uncovering important short-time features of microorganism locomotion.

Footnotes

  • 1To whom correspondence should be addressed. Email: miao{at}physics.ucla.edu
  • Author contributions: J.A.R., R.B., K.L.H., and J.M. designed research; J.A.R., M.A.L., M.C.T., Y.Z., M.O., D.D.C., N.K.K., and J.M. performed research; J.A.R., M.A.L., M.C.T., Y.Z., M.O., D.D.C., M.L.P., G.H., R.B., K.L.H., and J.M. analyzed data; and J.A.R., R.B., K.L.H., and J.M. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0907001106/DCSupplemental.

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