Spirochetes are a medically important and ecologically significant group of motile bacteria with a distinct morphology. Outermost is a membrane sheath, and within this sheath is the protoplasmic cell cylinder and subterminally attached periplasmic flagella. Here we address specific and unique aspects of their motility and chemotaxis. For spirochetes, translational motility requires asymmetrical rotation of the two internally located flagellar bundles. Consequently, they have swimming modalities that are more complex than the well-studied paradigms. In addition, coordinated flagellar rotation likely involves an efficient and novel signaling mechanism. This signal would be transmitted over the length of the cell, which in some cases is over 100-fold greater than the cell diameter. Finally, many spirochetes, including Treponema, Borrelia, and Leptospira, are highly invasive pathogens. Motility is likely to play a major role in the disease process. This review summarizes the progress in the genetics of motility and chemotaxis of spirochetes, and points to new directions for future experimentation.

Borrelia burgdorferi is a motile spirochete with multiple internal periplasmic flagella (PFs) attached near each end of the cell cylinder; these PFs overlap in the cell center. We analyzed the shape and motion of wild type and PF-deficient mutants using both photomicrography and video microscopy. We found that swimming cells resembled the dynamic movements of eukaryotic flagella. In contrast to helically shaped spirochetes, which propagate Spirochetes have several attributes that probably contribute to their ability to swim in gel-like media (1-6). Most-but not all (see below)-species are helical or have helical portions (4, 7); this morphology allows them to bore their way through these media in a corkscrew-like manner (1, 4). In addition, these bacteria have periplasmic flagella (PFs) between the outer membrane sheath and the cell cylinder (4, 7). Several lines of evidence indicate that the PFs are directly involved in motility (4,8), and recent results with protruding PFs indicate that the PFs rotate similarly to the external flagella of rod-shaped bacteria (9-11). During translation, the PFs and cell body interact with one another and probably form a more rigid propeller than external flagella alone (1, 11, 12).We report here that Borrelia burgdorferi, the causative agent of Lyme disease (13), swims by using helical PFs to produce a nonhelical cell shape. The PFs of B. burgdorferi are left-handed helices of defined helix pitch (1.48 ,um) and diameter (0.28 ,um) (10). Other spirochetes have been shown to have left-handed PFs but ofdifferent helix dimensions (10). B. burgdorferi has multiple PFs attached at each end that overlap in the cell center (13,14). However, whereas most other spirochetes have cell bodies that are clearly helical, we report here that swimming cells of B. burgdorferi are planar.Moreover, cell translation is accomplished by producing posteriorly propagating planar waves resembling those found in eukaryotic flagella. MATERIALS AND METHODSOrganisms and Culture Conditions. Strains HB19, B31, and both avirulent and fresh isolates of strain 297 (fewer than three in vitro passages from hamsters) ofB. burgdorferi were provided by R. C. Johnson (University of Minnesota, Minneapolis). The spontaneously occurring motility mutant of strain HB19 lacking PFs was provided by Alan Barbour (University of Texas, San Antonio) (8). Cells were grown in BSK medium at 350C (15).Light Microscopy. Approximately 5 jA of a cell suspension was placed on a slide and covered with a cover glass (22 X 22 mm) supported by a mixture of paraffin and Vaseline. For observations of cells swimming in methylcellulose, a drop of cells in culture medium was mixed on the slide with an approximately equal volume of 1% or 2% methylcellulose (2% = 4 N-s m-2 = 4000 cP; Matheson) in salts buffer (SB; 14.1 mM NaCl/12.6 mM NaHCO3/5.4 mM KCl/1.5 mM MgCl2/0.1 mM CaCl2/46 mM Na2HPO4/3.5 mM NaH2PO4, pH 7.7). For measurements of swim speeds in a pure liquid, cells were centrifuged for 10 min at -745 x g at 40C, rinsed twice in col...

Treponema denticola is an anaerobic, motile, oral spirochete associated with periodontal disease. We found that the periplasmic flagella (PFs), which are located between the outer membrane sheath and cell cylinder, influence its morphology in a unique manner. In addition, the protein composition of the PFs was found to be quite complex and similar to those of other spirochetes. Dark-field microscopy revealed that most wild-type cells had an irregular twisted morphology, with both planar and helical regions, and a minority of cells had a regular right-handed helical shape. High-voltage electron microscopy indicated that the PFs, especially in those regions of the cell which were planar, wrapped around the cell body axis in a right-handed sense. In those regions of the cell which were helical or irregular, the PFs tended to lie along the cell axis. The PFs caused the cell to form the irregular shape, as two nonmotile, PF-deficient mutants (JR1 and HL51) were no longer irregular but were right-handed helices. JR1 was isolated as a spontaneously occurring nonmotile mutant, and HL51 was isolated as a site-directed mutant in the flagellar hook gene flgE. Consistent with these results is the finding that wild-type cells with their outer membrane sheath removed were also right-handed helices similar in shape to JR1 and HL51. Purified PFs were analyzed by two-dimensional gel electrophoresis, and several protein species were identified. Western blot analysis using antisera to Treponema pallidum PF proteins along with N-terminal amino acid sequence analysis indicated T. denticola PFs are composed of one class A sheath protein of 38 kDa (FlaA) and three class B proteins of 35 kDa (FlaB1 and FlaB2) and one of 34 kDa (FlaB3). The N-terminal amino acid sequences of the FlaA and FlaB proteins of T. denticola were most similar to those of T. pallidum and Treponema phagedenis. Because these proteins were present in markedly reduced amounts or were absent in HL51, PF synthesis is likely to be regulated in a hierarchy similar to that found for flagellar synthesis in other bacteria.Spirochetes are recognized for their unique cell morphology and unusual means of motility (5, 48). In most spirochetes, the primary structural component of the cell body is a flexible yet semirigid helically shaped cell cylinder (5). Borrelia burgdorferi is an exception, since it has a rod-shaped cell cylinder (13, 15). Helical periplasmic flagella (PFs) are closely associated with the spirochetal protoplasmic cell cylinder (PC) and are embedded in the cytoplasmic membrane and cell wall near each end of the cell (5, 6, 17); each PF is inserted at only one end. Surrounding the entire cell is an outer membrane sheath (OS) (5). Genetic evidence indicates that the PFs are essential for the motility of several spirochete species (4,8,26,28,37,44). The PFs vary in number, length, and protein composition among the spirochete species. Depending on the species, the PFs may or may not overlap in the center of the cell (5, 8). PFs from most spirochete species are co...

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