scholarly journals A molecular rack and pinion actuates a cell-surface adhesin and enables bacterial gliding motility

2020 ◽  
Vol 6 (10) ◽  
pp. eaay6616 ◽  
Author(s):  
Abhishek Shrivastava ◽  
Howard C. Berg
Keyword(s):  
Cell Surface ◽  
Rotation Axis ◽  
Gliding Motility ◽  
Flavobacterium Johnsoniae ◽  
Viscous Shear ◽  
Shear Cells ◽  
A Cell ◽  
Solid Substratum ◽  
Gliding Bacterium ◽  
Rotary Motor

The gliding bacterium Flavobacterium johnsoniae is known to have an adhesin, SprB, that moves along the cell surface on a spiral track. Following viscous shear, cells can be tethered by the addition of an anti-SprB antibody, causing spinning at 3 Hz. Labeling the type 9 secretion system (T9SS) with a YFP fusion of GldL showed a yellow fluorescent spot near the rotation axis, indicating that the motor driving the motion is associated with the T9SS. The distance between the rotation axis and the track (90 nm) was determined after adding a Cy3 label for SprB. A rotary motor spinning a pinion of radius 90 nm at 3 Hz would cause a spot on its periphery to move at 1.5 μm/s, the gliding speed. We suggest the pinion drives a flexible tread that carries SprB along a track fixed to the cell surface. Cells glide when this adhesin adheres to the solid substratum.

scholarly journals A molecular rack and pinion actuates a cell-surface adhesin and enables bacterial gliding motility

2018 ◽  
Author(s):  
Abhishek Shrivastava ◽  
Howard C. Berg
Keyword(s):  
Cell Surface ◽  
Fluorescent Protein ◽  
Rotation Axis ◽  
Yellow Fluorescent Protein ◽  
Gliding Motility ◽  
Flavobacterium Johnsoniae ◽  
A Cell ◽  
Solid Substratum ◽  
Gliding Bacterium ◽  
Rotary Motor

AbstractThe mechanism for bacterial gliding is not understood. The gliding bacteriumFlavobacterium johnsoniaeis known to have an adhesin, SprB, that moves along the cell surface on a spiral track. When cells are sheared by passage of a suspension through thin tubing, they stop gliding but can be tethered by addition of an anti-SprB antibody. Tethered cells spin about 3 Hz. We labeled the Type 9 secretion system (T9SS) with a yellow-fluorescent-protein (YFP) fusion of GldL. When labeled cells were tethered, a yellow fluorescent spot was found near the rotation axis, which shows that the motor that drives the rotation localizes with the T9SS. The spiral track was labeled by following the motion of Cy3 attached to SprB via an antibody. The distance between the rotation axis and the track was determined by a measurement involving both labels, YFP and Cy3, yielding 90 nm. If a rotary motor spins a pinion of radius 90 nm 3 Hz, a spot on its periphery will move 1.5 μm/s, the speed at which cells glide. We suggest that the pinion drives a flexible tread that carries SprB along a track fixed to the cell surface. Cells glide when such an adhesin adheres to the solid substratum.

scholarly journals SprB Is a Cell Surface Component of the Flavobacterium johnsoniae Gliding Motility Machinery

2008 ◽  
Vol 190 (8) ◽  
pp. 2851-2857 ◽  
Author(s):  
Shawn S. Nelson ◽  
Sreelekha Bollampalli ◽  
Mark J. McBride
Keyword(s):  
Cell Surface ◽  
Surface Protein ◽  
Gliding Motility ◽  
Wild Type ◽  
Polystyrene Microspheres ◽  
Flavobacterium Johnsoniae ◽  
A Cell ◽  
Transposon Insertions ◽  
Gliding Bacterium ◽  
Surface Adhesins

ABSTRACT Cells of the gliding bacterium Flavobacterium johnsoniae move rapidly over surfaces by an unknown mechanism. Transposon insertions in sprB resulted in cells that were defective in gliding. SprB is a highly repetitive 669-kDa cell surface protein, and antibodies against SprB inhibited the motility of wild-type cells. Polystyrene microspheres coated with antibodies against SprB attached to and were rapidly propelled along the cell surface, suggesting that SprB is one of the outermost components of the motility machinery. The movement of SprB along the cell surface supports a model of gliding motility in which motors anchored to the cell wall rapidly propel cell surface adhesins.

scholarly journals Novel Features of the Polysaccharide-Digesting Gliding Bacterium Flavobacterium johnsoniae as Revealed by Genome Sequence Analysis

2009 ◽  
Vol 75 (21) ◽  
pp. 6864-6875 ◽  
Author(s):  
Mark J. McBride ◽  
Gary Xie ◽  
Eric C. Martens ◽  
Alla Lapidus ◽  
Bernard Henrissat ◽  
...  
Keyword(s):  
Gene Regulation ◽  
Cell Surface ◽  
Outer Membrane ◽  
Genome Sequence ◽  
Genome Analysis ◽  
Genetic Manipulation ◽  
Gliding Motility ◽  
Glycoside Hydrolases ◽  
Flavobacterium Johnsoniae ◽  
Gliding Bacterium

ABSTRACT The 6.10-Mb genome sequence of the aerobic chitin-digesting gliding bacterium Flavobacterium johnsoniae (phylum Bacteroidetes) is presented. F. johnsoniae is a model organism for studies of bacteroidete gliding motility, gene regulation, and biochemistry. The mechanism of F. johnsoniae gliding is novel, and genome analysis confirms that it does not involve well-studied motility organelles, such as flagella or type IV pili. The motility machinery is composed of Gld proteins in the cell envelope that are thought to comprise the “motor” and SprB, which is thought to function as a cell surface adhesin that is propelled by the motor. Analysis of the genome identified genes related to sprB that may encode alternative adhesins used for movement over different surfaces. Comparative genome analysis revealed that some of the gld and spr genes are found in nongliding bacteroidetes and may encode components of a novel protein secretion system. F. johnsoniae digests proteins, and 125 predicted peptidases were identified. F. johnsoniae also digests numerous polysaccharides, and 138 glycoside hydrolases, 9 polysaccharide lyases, and 17 carbohydrate esterases were predicted. The unexpected ability of F. johnsoniae to digest hemicelluloses, such as xylans, mannans, and xyloglucans, was predicted based on the genome analysis and confirmed experimentally. Numerous predicted cell surface proteins related to Bacteroides thetaiotaomicron SusC and SusD, which are likely involved in binding of oligosaccharides and transport across the outer membrane, were also identified. Genes required for synthesis of the novel outer membrane flexirubin pigments were identified by a combination of genome analysis and genetic experiments. Genes predicted to encode components of a multienzyme nonribosomal peptide synthetase were identified, as were novel aspects of gene regulation. The availability of techniques for genetic manipulation allows rapid exploration of the features identified for the polysaccharide-digesting gliding bacteroidete F. johnsoniae.

scholarly journals Flavobacterium johnsoniae SprA Is a Cell Surface Protein Involved in Gliding Motility

2007 ◽  
Vol 189 (19) ◽  
pp. 7145-7150 ◽  
Author(s):  
Shawn S. Nelson ◽  
Padden P. Glocka ◽  
Sarika Agarwal ◽  
David P. Grimm ◽  
Mark J. McBride
Keyword(s):  
Cell Surface ◽  
Surface Protein ◽  
Gliding Motility ◽  
Proteinase K ◽  
Cell Surface Protein ◽  
Intact Cells ◽  
Unknown Mechanism ◽  
Flavobacterium Johnsoniae ◽  
A Cell

ABSTRACT Flavobacterium johnsoniae cells glide rapidly over surfaces by an unknown mechanism. Transposon-induced sprA mutants formed nonspreading colonies on agar, and the cells examined in wet mounts were deficient in attachment to surfaces and were almost completely nonmotile. Exposure of intact cells to proteinase K cleaved the 270-kDa SprA into several large peptides, suggesting that it is partially exposed on the cell surface.

scholarly journals Colony spreading of the gliding bacterium Flavobacterium johnsoniae in the absence of the motility adhesin SprB

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Keiko Sato ◽  
Masami Naya ◽  
Yuri Hatano ◽  
Yoshio Kondo ◽  
Mari Sato ◽  
...  
Keyword(s):  
Soft Agar ◽  
Gliding Motility ◽  
Wild Type ◽  
Initial Cell ◽  
Flavobacterium Johnsoniae ◽  
Seeking Behavior ◽  
Colony Spreading ◽  
Gliding Bacterium ◽  
Mutant Cells ◽  
Scanning Electron

AbstractColony spreading of Flavobacterium johnsoniae is shown to include gliding motility using the cell surface adhesin SprB, and is drastically affected by agar and glucose concentrations. Wild-type (WT) and ΔsprB mutant cells formed nonspreading colonies on soft agar, but spreading dendritic colonies on soft agar containing glucose. In the presence of glucose, an initial cell growth-dependent phase was followed by a secondary SprB-independent, gliding motility-dependent phase. The branching pattern of a ΔsprB colony was less complex than the pattern formed by the WT. Mesoscopic and microstructural information was obtained by atmospheric scanning electron microscopy (ASEM) and transmission EM, respectively. In the growth-dependent phase of WT colonies, dendritic tips spread rapidly by the movement of individual cells. In the following SprB-independent phase, leading tips were extended outwards by the movement of dynamic windmill-like rolling centers, and the lipoproteins were expressed more abundantly. Dark spots in WT cells during the growth-dependent spreading phase were not observed in the SprB-independent phase. Various mutations showed that the lipoproteins and the motility machinery were necessary for SprB-independent spreading. Overall, SprB-independent colony spreading is influenced by the lipoproteins, some of which are involved in the gliding machinery, and medium conditions, which together determine the nutrient-seeking behavior.

scholarly journals Cell Surface Filaments of the Gliding Bacterium Flavobacterium johnsoniae Revealed by Cryo-Electron Tomography

2007 ◽  
Vol 189 (20) ◽  
pp. 7503-7506 ◽  
Author(s):  
Jun Liu ◽  
Mark J. McBride ◽  
Sriram Subramaniam
Keyword(s):  
Cell Surface ◽  
Outer Membrane ◽  
Electron Tomography ◽  
Wild Type ◽  
Unknown Mechanism ◽  
Flavobacterium Johnsoniae ◽  
Atp Binding Cassette Transporter ◽  
Cryo Electron Tomography ◽  
Inner Surface ◽  
Gliding Bacterium

ABSTRACT Flavobacterium johnsoniae cells glide rapidly over surfaces by an as-yet-unknown mechanism. Using cryo-electron tomography, we show that wild-type cells display tufts of ∼5-nm-wide cell surface filaments that appear to be anchored to the inner surface of the outer membrane. These filaments are absent in cells of a nonmotile gldF mutant but are restored upon expression of plasmid-encoded GldF, a component of a putative ATP-binding cassette transporter.

scholarly journals Genome Sequence of the Cellulolytic Gliding Bacterium Cytophaga hutchinsonii

2007 ◽  
Vol 73 (11) ◽  
pp. 3536-3546 ◽  
Author(s):  
Gary Xie ◽  
David C. Bruce ◽  
Jean F. Challacombe ◽  
Olga Chertkov ◽  
John C. Detter ◽  
...  
Keyword(s):  
Gliding Motility ◽  
Open Reading Frames ◽  
Crystalline Cellulose ◽  
Cellulolytic Bacteria ◽  
Cytophaga Hutchinsonii ◽  
Type Iv ◽  
Flavobacterium Johnsoniae ◽  
Anchoring Proteins ◽  
Genes Encoding ◽  
Gliding Bacterium

ABSTRACT The complete DNA sequence of the aerobic cellulolytic soil bacterium Cytophaga hutchinsonii, which belongs to the phylum Bacteroidetes, is presented. The genome consists of a single, circular, 4.43-Mb chromosome containing 3,790 open reading frames, 1,986 of which have been assigned a tentative function. Two of the most striking characteristics of C. hutchinsonii are its rapid gliding motility over surfaces and its contact-dependent digestion of crystalline cellulose. The mechanism of C. hutchinsonii motility is not known, but its genome contains homologs for each of the gld genes that are required for gliding of the distantly related bacteroidete Flavobacterium johnsoniae. Cytophaga-Flavobacterium gliding appears to be novel and does not involve well-studied motility organelles such as flagella or type IV pili. Many genes thought to encode proteins involved in cellulose utilization were identified. These include candidate endo-β-1,4-glucanases and β-glucosidases. Surprisingly, obvious homologs of known cellobiohydrolases were not detected. Since such enzymes are needed for efficient cellulose digestion by well-studied cellulolytic bacteria, C. hutchinsonii either has novel cellobiohydrolases or has an unusual method of cellulose utilization. Genes encoding proteins with cohesin domains, which are characteristic of cellulosomes, were absent, but many proteins predicted to be involved in polysaccharide utilization had putative D5 domains, which are thought to be involved in anchoring proteins to the cell surface.

scholarly journals Flavobacterium johnsoniae gldN and gldO Are Partially Redundant Genes Required for Gliding Motility and Surface Localization of SprB

2009 ◽  
Vol 192 (5) ◽  
pp. 1201-1211 ◽  
Author(s):  
Ryan G. Rhodes ◽  
Mudiarasan Napoleon Samarasam ◽  
Abhishek Shrivastava ◽  
Jessica M. van Baaren ◽  
Soumya Pochiraju ◽  
...  
Keyword(s):  
Protein Secretion ◽  
Deletion Mutant ◽  
Gliding Motility ◽  
Selection Strategy ◽  
Wild Type ◽  
Flavobacterium Johnsoniae ◽  
Redundant Genes ◽  
Surface Localization ◽  
Gliding Bacterium ◽  
Mutant Cells

ABSTRACT Cells of the gliding bacterium Flavobacterium johnsoniae move rapidly over surfaces. Mutations in gldN cause a partial defect in gliding. A novel bacteriophage selection strategy was used to aid construction of a strain with a deletion spanning gldN and the closely related gene gldO in an otherwise wild-type F. johnsoniae UW101 background. Bacteriophage transduction was used to move a gldN mutation into F. johnsoniae UW101 to allow phenotypic comparison with the gldNO deletion mutant. Cells of the gldN mutant formed nonspreading colonies on agar but retained some ability to glide in wet mounts. In contrast, cells of the gldNO deletion mutant were completely nonmotile, indicating that cells require GldN, or the GldN-like protein GldO, to glide. Recent results suggest that Porphyromonas gingivalis PorN, which is similar in sequence to GldN, has a role in protein secretion across the outer membrane. Cells of the F. johnsoniae gldNO deletion mutant were defective in localization of the motility protein SprB to the cell surface, suggesting that GldN may be involved in secretion of components of the motility machinery. Cells of the gldNO deletion mutant were also deficient in chitin utilization and were resistant to infection by bacteriophages, phenotypes that may also be related to defects in protein secretion.

scholarly journals Social motility of biofilm-like microcolonies in a gliding bacterium

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Chao Li ◽  
Amanda Hurley ◽  
Wei Hu ◽  
Jay W. Warrick ◽  
Gabriel L. Lozano ◽  
...  
Keyword(s):  
Self Assembly ◽  
Microscopic Analysis ◽  
Extracellular Polysaccharide ◽  
Microfluidic System ◽  
Gliding Motility ◽  
Solid Surfaces ◽  
Swarming Motility ◽  
Collective Movement ◽  
Flavobacterium Johnsoniae ◽  
Gliding Bacterium

AbstractBacterial biofilms are aggregates of surface-associated cells embedded in an extracellular polysaccharide (EPS) matrix, and are typically stationary. Studies of bacterial collective movement have largely focused on swarming motility mediated by flagella or pili, in the absence of a biofilm. Here, we describe a unique mode of collective movement by a self-propelled, surface-associated biofilm-like multicellular structure. Flavobacterium johnsoniae cells, which move by gliding motility, self-assemble into spherical microcolonies with EPS cores when observed by an under-oil open microfluidic system. Small microcolonies merge, creating larger ones. Microscopic analysis and computer simulation indicate that microcolonies move by cells at the base of the structure, attached to the surface by one pole of the cell. Biochemical and mutant analyses show that an active process drives microcolony self-assembly and motility, which depend on the bacterial gliding apparatus. We hypothesize that this mode of collective bacterial movement on solid surfaces may play potential roles in biofilm dynamics, bacterial cargo transport, or microbial adaptation. However, whether this collective motility occurs on plant roots or soil particles, the native environment for F. johnsoniae, is unknown.

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