The Unique Paradigm of Spirochete Motility and Chemotaxis

Nyles W. Charon; Andrew Cockburn; Chunhao Li; Jun Liu; Kelly A. Miller; Michael R. Miller; Md. A. Motaleb; Charles W. Wolgemuth

doi:10.1146/annurev-micro-092611-150145

The Unique Paradigm of Spirochete Motility and Chemotaxis

Nyles W. Charon¹, Andrew Cockburn¹, Chunhao Li³, Jun Liu⁴, Kelly A. Miller¹, Michael R. Miller², Md. A. Motaleb⁵ and Charles W. Wolgemuth⁶
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¹Department of Microbiology, Immunology, and Cell Biology, ²Department of Biochemistry, West Virginia University, Health Sciences Center, Morgantown, West Virginia 26506-9177; email: [email protected], [email protected], [email protected], [email protected] ³Department of Oral Biology, The State University of New York at Buffalo, New York 14214-3092; email: [email protected] ⁴The University of Texas–Houston Medical School, Department of Pathology and Laboratory Medicine, Houston, Texas 77030; email: [email protected] ⁵Department of Microbiology and Immunology, Brody School of Medicine, East Carolina University, Greenville, North Carolina 27834; email: [email protected] ⁶Department of Cell Biology and Center for Cell Analysis and Modeling, University of Connecticut Health Center, Farmington, Connecticut 06030-3505; email: [email protected]
Vol. 66:349-370 (Volume publication date October 2012) https://doi.org/10.1146/annurev-micro-092611-150145
© Annual Reviews

Abstract

Spirochete motility is enigmatic: It differs from the motility of most other bacteria in that the entire bacterium is involved in translocation in the absence of external appendages. Using the Lyme disease spirochete Borrelia burgdorferi (Bb) as a model system, we explore the current research on spirochete motility and chemotaxis. Bb has periplasmic flagella (PFs) subterminally attached to each end of the protoplasmic cell cylinder, and surrounding the cell is an outer membrane. These internal helix-shaped PFs allow the spirochete to swim by generating backward-moving waves by rotation. Exciting advances using cryoelectron tomography are presented with respect to in situ analysis of cell, PF, and motor structure. In addition, advances in the dynamics of motility, chemotaxis, gene regulation, and the role of motility and chemotaxis in the life cycle of Bb are summarized. The results indicate that the motility paradigms of flagellated bacteria do not apply to these unique bacteria.

Keyword(s): Borrelia, flagella, Lyme disease, motor

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2012-10-13

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The Unique Paradigm of Spirochete Motility and Chemotaxis

Annual Review of Microbiology 66, 349 (2012); https://doi.org/10.1146/annurev-micro-092611-150145

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Supplementary Data

Download Supplemental Figures and Table as a PDF. Contains: Supplemental Figure 1 (also reproduced below), Supplemental Figure 2 (also reproduced below), Supplemental Table 1, and links to Supplemental Movies 1-4 (videos embedded below)

Supplemental Figure 1: Differentiation of a flat wave vs. a helical wave. The plane of focus yields different images depending on whether the cell is (a) a flat wave with an axial twist or (b) a helical wave (5). Supplemental movie 1 indicates that Bb is a flat-wave.

Supplemental Figure 2: Genetic map of Bb chromosome. Genes are identified as those that are potentially involved, or have been shown to be involved, in motility and chemotaxis. The direction of transcription is indicated by the arrows, and the σ⁷⁰ promoters that have been identified by primer extension or 5'RACE analysis. Blue denotes chemotaxis genes, and dark green motility genes. Red indicates regulatory genes (1, 2, 6).

Supplemental Movie 1: Tethered cell of Bb swimming in 0.5% methylcellulose recorded first at real time then played back in slow motion (5). Download movie file (AVI)

Supplemental Movie 2: 3D reconstruction of the Bb motor (11). J. Liu, unpublished. Download movie file (AVI)

Supplemental Movie 3: Phase microscopy movie of swimming wild-type followed by cheA2 mutant cells of Bb in 1% methylcellulose. Note that the wild-type cell runs, flexes, and runs, whereas the cheA2 mutant only runs in one direction (9). Download movie file (AVI)

Supplemental Movie 4: Animated model of swimming Bb. For simplification, only one PF attached at each end is shown, and the OM is not presented. In this model, The PFs from the two ends overlap and are shown to form a continuous filament from one end to the other (4). Download movie file (AVI)