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Journal of Bacteriology, January 2009, p. 600-607, Vol. 191, No. 2
0021-9193/09/$08.00+0     doi:10.1128/JB.01288-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

The Flat-Ribbon Configuration of the Periplasmic Flagella of Borrelia burgdorferi and Its Relationship to Motility and Morphology {triangledown} ,{dagger}

Nyles W. Charon,1* Stuart F. Goldstein,2 Michael Marko,3 Chyongere Hsieh,3 Linda L. Gebhardt,4 M. Abdul Motaleb,1,5 Charles W. Wolgemuth,6 Ronald J. Limberger,4 and Nancy Rowe7

Department of Microbiology, Immunology and Cell Biology, Robert C. Byrd Health Sciences Center, West Virginia University, Morgantown, West Virginia 26506-9177,1 Department of Genetics, Cell Biology, and Development, 6-160 Jackson Hall, University of Minnesota, Minneapolis, Minnesota 55455,2 Resource for Visualization of Biological Complexity, Wadsworth Center, Empire State Plaza, Albany, New York 12201-0509,3 New York State Department of Health, Wadsworth Center, David Axelrod Institute, 120 New Scotland Avenue, Albany, New York 12208,4 Department of Microbiology and Immunology, Brody School of Medicine, East Carolina University, Greenville, North Carolina 27834,5 Department of Cell Biology, University of Connecticut Health Center, Farmington, Connecticut 06030-3505,6 Supercomputer Institute, 599 Walter Library, University of Minnesota, Minneapolis, Minnesota 554557

Received 14 September 2008/ Accepted 31 October 2008

Electron cryotomography was used to analyze the structure of the Lyme disease spirochete, Borrelia burgdorferi. This methodology offers a new means for studying the native architecture of bacteria by eliminating the chemical fixing, dehydration, and staining steps of conventional electron microscopy. Using electron cryotomography, we noted that membrane blebs formed at the ends of the cells. These blebs may be precursors to vesicles that are released from cells grown in vivo and in vitro. We found that the periplasmic space of B. burgdorferi was quite narrow (16.0 nm) compared to those of Escherichia coli and Pseudomonas aeruginosa. However, in the vicinity of the periplasmic flagella, this space was considerably wider (42.3 nm). In contrast to previous results, the periplasmic flagella did not form a bundle but rather formed a tight-fitting ribbon that wraps around the protoplasmic cell cylinder in a right-handed sense. We show how the ribbon configuration of the assembled periplasmic flagella is more advantageous than a bundle for both swimming and forming the flat-wave morphology. Previous results indicate that B. burgdorferi motility is dependent on the rotation of the periplasmic flagella in generating backward-moving waves along the length of the cell. This swimming requires that the rotation of the flagella exerts force on the cell cylinder. Accordingly, a ribbon is more beneficial than a bundle, as this configuration allows each periplasmic flagellum to have direct contact with the cell cylinder in order to exert that force, and it minimizes interference between the rotating filaments.


* Corresponding author. Mailing address: Department of Microbiology, Immunology and Cell Biology, Robert C. Byrd Health Sciences Center, West Virginia University, Morgantown, WV 26506-9177. Phone: (304) 293-4170. Fax: (304) 293-7823. E-mail: ncharon{at}hsc.wvu.edu

{triangledown} Published ahead of print on 14 November 2008.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.


Journal of Bacteriology, January 2009, p. 600-607, Vol. 191, No. 2
0021-9193/09/$08.00+0     doi:10.1128/JB.01288-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.




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