Asymmetrical flagellar rotation in
            <i>Borrelia burgdorferi</i>
            nonchemotactic mutants

Li, Chunhao; Bakker, Richard G.; Motaleb, M. A.; Sartakova, Marina L.; Cabello, Felipe C.; Charon, Nyles W.

doi:10.1073/pnas.092010499

Cited by 79 publications

(249 citation statements)

References 42 publications

(55 reference statements)

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“…Monoclonal antibodies to FlaB (H9724), FlaA, and DnaK were provided by A. Barbour (University of California, Irvine), B. Johnson (Centers for Disease Control and Prevention, Atlanta, GA), and J. Benach (State University of New York, Stony Brook), respectively. Polyclonal anti-FliI, anti-CheA2, anti-CheX, and anti-CheY3 were described previously (22,37,48). Polyclonal anti-recombinant CheW3 was provided by C. Li (unpublished data).…”

Section: Methodsmentioning

confidence: 99%

Borrelia burgdorferi Uniquely Regulates Its Motility Genes and Has an Intricate Flagellar Hook-Basal Body Structure

et al. 2008

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Borrelia burgdorferi is a flat-wave, motile spirochete that causes Lyme disease. Motility is provided by periplasmic flagella (PFs) located between the cell cylinder and an outer membrane sheath. The structure of these PFs, which are composed of a basal body, a hook, and a filament, is similar to the structure of flagella of other bacteria. To determine if hook formation influences flagellin gene transcription in B. burgdorferi, we inactivated the hook structural gene flgE by targeted mutagenesis. In many bacteria, completion of the hook structure serves as a checkpoint for transcriptional control of flagellum synthesis and other chemotaxis and motility genes. Specifically, the hook allows secretion of the anti-sigma factor FlgM and concomitant late gene transcription promoted by 28 . However, the control of B. burgdorferi PF synthesis differs from the control of flagellum synthesis in other bacteria; the gene encoding 28 is not present in the genome of B. burgdorferi, nor are any 28 promoter recognition sequences associated with the motility genes. We found that B. burgdorferi flgE mutants lacked PFs, were rod shaped, and were nonmotile, which substantiates previous evidence that PFs are involved in both cell morphology and motility. Although most motility and chemotaxis gene products accumulated at wild-type levels in the absence of FlgE, mutant cells had markedly decreased levels of the flagellar filament proteins FlaA and FlaB. Further analyses showed that the reduction in the levels of flagellin proteins in the spirochetes lacking FlgE was mediated at the posttranscriptional level. Taken together, our results indicate that in B. burgdorferi, the completion of the hook does not serve as a checkpoint for transcriptional regulation of flagellum synthesis. In addition, we also present evidence that the hook protein in B. burgdorferi forms a high-molecular-weight complex and that formation of this complex occurs in the periplasmic space.Borrelia burgdorferi, the causative agent of Lyme disease, is a spirochete with a characteristic flat-wave morphology (24, 25; for a review, see reference 12). As a result of their unusual morphology, B. burgdorferi and other spirochete species have a highly specialized ability that allows them to traverse viscous gellike media (8). This unique swimming ability enables these bacteria to penetrate into specific host connective tissues and ecological niches (43). The importance of motility as a virulence factor has been implicated in several spirochete species, including Treponema denticola (42), Brachyspira hyodysenteriae (54), Borrelia garinii (60), and B. burgdorferi (10, 56).Motility in B. burgdorferi is provided by bundles of between 7 and 11 periplasmic flagella (PFs) that are subterminally attached near the cell ends. These PFs extend inward along the cell cylinder beneath an outer membrane sheath (6,24,28,46). B. burgdorferi PFs have a structure similar to that of flagella of other bacteria; a PF is composed of a basal body, a hook, and a filament containing a single major ...

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Section: Methodsmentioning

confidence: 99%

Borrelia burgdorferi Uniquely Regulates Its Motility Genes and Has an Intricate Flagellar Hook-Basal Body Structure

et al. 2008

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“…A previously described method was used to construct a BB0569 deletion mutant (25). Briefly, a part of the BB0569 gene (1,559 bp) was PCR amplified with primer pair P 1 /P 2 , and the resultant PCR product was cloned into the pGEM-T Easy vector (Promega, Madison, WI).…”

Section: Methodsmentioning

confidence: 99%

“…A high-passage-number Borrelia burgdorferi sensu stricto strain, B31A (wild type) (29), and its isogenic mutants were grown either in Barbour-Stoenner-Kelly II (BSK-II) liquid medium supplemented with 6% rabbit serum or on semisolid agar plates in a humidified incubator at 34°C in the presence of ϳ3 to 5% CO 2 , as previously described (25).…”

Section: Methodsmentioning

confidence: 99%

“…Recent studies revealed that all of the chemotaxis genes in the flaA operon that have been examined are essential for chemotaxis of B. burgdorferi (e.g., cheA 2 , cheW 3 , and cheY 3 mutants never reverse, and the cheX mutant constantly flexes). All of these mutants are nonchemotactic to attractants (25)(26)(27)(28). In contrast to the flaA operon, most genes studied to date in the cheW 2 operon are not required for chemotaxis (e.g., cheA 1 , cheW 2 , and cheY 2 mutants have swimming behaviors similar to those of the parental wildtype strain) (27,28).…”

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confidence: 99%

“…In contrast, the Lyme disease spirochete Borrelia burgdorferi has multiple homologs of its chemotaxis genes, including two cheA (cheA 1 and cheA 2 ), three cheY (cheY 1 , cheY 2 , and cheY 3 ), three cheW (cheW 1 , cheW 2 , and cheW 3 ), two cheB (cheB 1 and cheB 2 ), and two cheR (cheR 1 and cheR 2 ) genes (21)(22)(23). Many of these chemotaxis genes are located within the flaA operon or the cheW 2 operon (24,25). The flaA operon contains flaA, cheA 2 , cheW 3 , cheX, and cheY 3 .…”

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Hypothetical Protein BB0569 Is Essential for Chemotaxis of the Lyme Disease Spirochete Borrelia burgdorferi

Zhang

Li²,

Charon

et al. 2016

J Bacteriol

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The Lyme disease spirochete Borrelia burgdorferi has five putative methyl-accepting chemotaxis proteins (MCPs). In this report, we provide evidence that a hypothetical protein, BB0569, is essential for the chemotaxis of B. burgdorferi. While BB0569 lacks significant homology to the canonical MCPs, it contains a conserved domain (spanning residues 110 to 170) that is often evident in membrane-bound MCPs such as Tar and Tsr of Escherichia coli. Unlike Tar and Tsr, BB0569 lacks transmembrane regions and recognizable HAMP and methylation domains and is similar to TlpC, a cytoplasmic chemoreceptor of Rhodobacter sphaeroides. An isogenic mutant of BB0569 constantly runs in one direction and fails to respond to attractants, indicating that BB0569 is essential for chemotaxis. Immunofluorescence, green fluorescent protein (GFP) fusion, and cryo-electron tomography analyses demonstrate that BB0569 localizes at the cell poles and is required for chemoreceptor clustering at the cell poles. Protein cross-linking studies reveal that BB0569 forms large protein complexes with MCP3, indicative of its interactions with other MCPs. Interestingly, analysis of B. burgdorferi mcp mutants shows that inactivation of either mcp 2 or mcp 3 reduces the level of BB0569 substantially and that such a reduction is caused by protein turnover. Collectively, these results demonstrate that the domain composition and function of BB0569 are similar in some respects to those of TlpC but that these proteins are different in their cellular locations, further highlighting that the chemotaxis of B. burgdorferi is unique and different from the Escherichia coli and Salmonella enterica paradigm. IMPORTANCESpirochete chemotaxis differs substantially from the Escherichia coli and Salmonella enterica paradigm, and the basis for controlling the rotation of the bundles of periplasmic flagella at each end of the cell is unknown. In recent years, Borrelia burgdorferi, the causative agent of Lyme disease, has been used as a model organism to understand spirochete chemotaxis and its role in infectious processes of the disease. In this report, BB0569, a hypothetical protein of B. burgdorferi, has been investigated by using an approach of genetic, biochemistry, and cryo-electron tomography analyses. The results indicate that BB0569 has a distinct role in chemotaxis that may be unique to spirochetes and represents a novel paradigm. Chemotaxis allows bacteria to swim toward favorable environments or away from harmful ones by modulation of their swimming behavior (1, 2). The molecular mechanisms involved in bacterial chemotaxis have been extensively studied in two prototype organisms, Escherichia coli and Salmonella enterica (for recent reviews, see references 3-5). The chemotaxis signaling apparatus works as a supramolecular unit that is composed of three major components: methyl-accepting chemotaxis proteins (MCPs), the histidine kinase CheA, and the response regulator CheY (6, 7). MCPs sense various environmental and intracellular signals and control the acti...

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Borrelia

Wang¹,

Schwartz²

2015

Bergey's Manual of Systematics of Archaea and Bacteria

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Bor.re'li.a. N.L. fem. n. Borrelia named after Amedée Borrel (1867–1936). Spirochaetes / Spirochaetia / Spirochaetales / Spirochaetaceae / Borrelia Helical cells are 0.2–0.5 mm by 3–30 mm, composed of 3–10 loose coils . The cells are surrounded by a surface layer, an outer membrane, periplasmic flagella, and a protoplasmic cylinder (Figure 1). Typically, 15–20 periplasmic flagella (which also have been termed endoflagella , axial fibrils, or periplasmic fibrils) originate at each end of the cell and wind about the protoplasmic cylinder to overlap in the middle of the cell. The protoplasmic cylinder consists of a peptidoglycan layer and an inner membrane which encloses the internal components of the cells. The cells are actively motile with frequent reversal of the direction of translational movement. Gram‐stain‐negative. Stain well with Giemsa stain. Species which have been grown in vitro are microaerophilic . Nutritional requirements for in vitro growth are complex. Arthropod‐borne pathogens of man, other mammals, and birds. The causative agents of tick‐borne Lyme disease and relapsing fever and louse‐borne relapsing fever in man . DNA G + C content ( mol %): 27–32. Type species : Borrelia anserina (Sakharoff 1891) Bergey, Harrison, Breed, Hammer and Huntoon 1925, 435 AL .

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Asymmetrical flagellar rotation in Borrelia burgdorferi nonchemotactic mutants

Cited by 79 publications

References 42 publications

Borrelia burgdorferi Uniquely Regulates Its Motility Genes and Has an Intricate Flagellar Hook-Basal Body Structure

Borrelia burgdorferi Uniquely Regulates Its Motility Genes and Has an Intricate Flagellar Hook-Basal Body Structure

Hypothetical Protein BB0569 Is Essential for Chemotaxis of the Lyme Disease Spirochete Borrelia burgdorferi

Borrelia

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