Motility modes of <i>Spiroplasma melliferum</i> BC3: a helical, wall‐less bacterium driven by a linear motor

Gilad, Rami; Porat, Asher; Trachtenberg, Shlomo

doi:10.1046/j.1365-2958.2003.03200.x

Cited by 45 publications

(63 citation statements)

References 64 publications

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“…As noted earlier, the closest resemblance between the motility of T. brucei and that of other microorganisms is the prokaryote Spiroplasma (21,31,32). A comparison between these two widely divergent organisms is instructive.…”

Section: Discussionmentioning

confidence: 84%

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

Rodríguez¹,

López²,

Thayer³

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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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 righthanded 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.millisecond differential interference-contrast microscopy ͉ Trypanosoma brucei ͉ cilium ͉ flagellum T he protozoan parasite Trypanosoma brucei is the causative pathogen of African sleeping sickness, a fatal disease indigenous to subSaharan Africa where 60 million people are at risk of infection (1, 2). T. brucei is transmitted between human hosts by a tsetse fly vector, and parasite motility is important in both hosts. In the tsetse fly, procyclic-form (PCF) parasites colonize the midgut and then migrate through the alimentary canal to the salivary glands, where maturation into human infectious forms occurs (3, 4). From the salivary gland, mature parasites can be injected into the blood of a mammalian host that has been bitten by the fly. In the mammalian host, migration of bloodstream-form (BSF) parasites through the blood-brain barrier initiates onset of the fatal course of the disease (5, 6). T. brucei is extracellular at all stages of infection and depends on its own flagellum-mediated motility for dissemination. Flagellar motility of T. brucei in various environments is believed to be central not only to host-parasite interaction, but also to cell division, morphogenesis, and development (3, 6-15).The T. brucei cell body is roughly 20-m long, with a relatively large posterior section tapering off into a long, narrow anterior section. It has a single flagellum, with the classic ''9 ϩ 2'' microtubule axoneme architecture that is attached to the cell body along its length. Based on microscopy studies, it is believed that propulsion of T. brucei proceeds by left-hand (LH) helical waves propagating along the flagellum, from tip to base, driving the cell forward in a drill-like motion (see Fig. 1A) (15-17). The genus name of the parasite actually derives from this distinctive motility (from the Greek trypanon or auger, and soma or body), first described in 1843 (18). Here, we use millisecond resolution differential interferencecontrast (DIC) microscopy, combined with other microscopy methods, to provide a quantitative analysis of T. brucei cell propulsion. Our results reveal that T. brucei ...

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Section: Discussionmentioning

confidence: 84%

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

Rodríguez¹,

López²,

Thayer³

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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“…These filaments have been implicated in gliding motility, and recent experiments suggest that they are responsible for morphological changes, such as twisted forms, in actively gliding myxobacteria; these twisted morphologies are not observed in non-motile mutants [Lunsdorf and Schairer, 2001]. Dynamic oscillatory morphology changes have been shown to drive motility in wall-less mollicute bacteria [Miyata and Uenoyama, 2002;Gilad et al, 2003;Trachtenberg et al, 2003]. A similar mechanism could also drive motility in myxobacteria through a slime ratchet-type mechanism [Wolgemuth et al, 2003].…”

Section: The Slime Ratchetmentioning

confidence: 99%

The Junctional Pore Complex and the Propulsion of Bacterial Cells

Wolgemuth

Oster

2004

Microb Physiol

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Gliding motility is defined as translocation in the direction of the long axis of the bacterium while in contact with a surface. This definition leaves unspecified any mechanism and, indeed, it appears that there is more than one physiological system underlying the same type of motion. Currently, two distinct mechanisms have been discovered in myxobacteria. One requires the extension, attachment, and retraction of type IV pili to pull the cell forwards. Recent experimental evidence suggests that a second mechanism for gliding motility involves the extrusion of slime from an organelle called the ‘junctional pore complex’. This review discusses the role of slime extrusion and the junctional pore complex in the gliding motility of both cyanobacteria and myxobacteria.

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“…Cholesterol, uncommon in bacteria, increases the rigidity of the membrane. The Mollicute cells are well defined in shape and exhibit a rich repertoire of cell movements and dynamic morphologies [for reviews, see Kirchhoff, 1992;Trachtenberg, 1998Trachtenberg, , 2003]. The Mycoplasmas glide [Miyata et al, 2002;Wolgemuth et al, 2003] and the Spiroplasmas are active polymorphic and chemotactic swimmers [Gilad et al, 2002;Berg, 2002;Wolgemuth et al, 2003].…”

Section: The Mollicutesmentioning

confidence: 99%

“…To swim, the cell has to deviate from helical symmetry and reciprocating movements. This is achieved through local dynamic deformations [see Gilad et al, 2003]. Trachtenberg Fig.…”

Section: The Underlying Helical Geometry Of Spiroplasmamentioning

confidence: 99%

“…Reciprocal shape changes in a low Reynolds number environment cannot generate net cell displacement [Purcell, 1977[Purcell, , 1997. Therefore, for a generation of directional motility and, equally important, direction changes (the combination of which underlies the chemotactic response), mechanisms of breaking helical symmetry have to be employed [Gilad et al, 2003;Trachtenberg and Geffen, unpubl. data].…”

Section: The Phenomenology Of Spiroplasma Swimming and Chemotaxismentioning

confidence: 99%

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Shaping and Moving a <i>Spiroplasma</i>

Trachtenberg

2004

Microb Physiol

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The Mollicutes (Spiroplasma, Mycoplasma and Acholeplasma) are the most minimal cells known to exist, being the smallest and simplest free-living and self-replicating forms of life. Phylogenetically, the Mollicutes are related to gram-positive bacteria and have evolved, by regressive evolution and genome reduction, from Clostridia. The smallest genome in this group (Mycoplasma genitalium – 5.77 × 10⁵ bp) is only twice that of a large virus (e.g., Entomopox viruses). The largest Mollicute genome (Spiroplasma LB12 – 2.2 × 10⁶ bp) is only about half that of, e.g., Escherichia coli. Structurally, the Mollicutes lack cell walls and flagella, but have internal cytoskeletons and are motile and chemotactic. Only a cholesterol-containing unit membrane envelops the cells. No analogs to the bacterial chemotactic and motility (che, mot, fla) genes, genes for a two-component signal transduction system, genes associated with gliding, or genomic homologs for the eukaryotic cytoskeleton and motor proteins were found in the Mollicutes. The Spiroplasmas are unique amongst the Mollicutes in having a well-defined basic helical cell geometry. In this respect, the Spiroplasma cell can, essentially, be viewed as a helical dynamic membranal tube (diameter ∼0.2 µm; equivalent to that of one eukaryotic flagellar axoneme or to a bacterial flagellar bundle). A flat cytoskeletal ribbon of parallel fibrils is attached to the inside of the cellular tube. Both tube and cytoskeleton are mutually coiled into a dynamic helix driven by differential length changes of the fibrils, which function as linear motors. The cytoskeletal ribbon follows the shortest (inner) helical line on the inner surface of the cellular tube. Being helical allows for further analytical reduction and consequent structural quantification of Spiroplasma. Of particular importance is the ability to correlate light and electron microscopy data and to calculate the fibril lengths (and corresponding molecular dimensions) in the helical and nonhelical dynamic states. The structural unit of the contractile cytoskeleton is a ∼50-Ångstrom-wide filament comprised of pairs of the 59-kD fib gene product. The monomers are arranged in pairs with opposite polarities allowing for a ∼100-Ångstrom-long axial repeat. The functional unit of the contractile cytoskeletal ribbon is a fibril comprised of an aligned pair of filaments. Neighboring repeats form a tetrameric ring with a lateral repeat of ∼100 Å. The axial length of the rings may shorten by ∼40%, driving the changes in the fibril lengths and, consequently, helical dynamics. Local length changes result in helical symmetry breaking and nonreciprocating cell movements allowing for net directional displacement. Flexing allows for changes in swimming direction.

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Motility modes of Spiroplasma melliferum BC3: a helical, wall‐less bacterium driven by a linear motor

Cited by 45 publications

References 64 publications

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

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

The Junctional Pore Complex and the Propulsion of Bacterial Cells

Shaping and Moving a <i>Spiroplasma</i>

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