The chemotaxis system, but not chemotaxis, is essential for swarming motility in
            <i>Escherichia coli</i>

Burkart, Mark; Toguchi, Adam; Harshey, Rasika M.

doi:10.1073/pnas.95.5.2568

Cited by 133 publications

(142 citation statements)

References 42 publications

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“…In E. coli, the signal transduction system is essential for swarming motility but traditional chemotaxis is not (44). Recently, it has been proposed that the twitching motility of P. aeruginosa and the social gliding motility of Myxococcus xanthus are essentially the same type IV pili-based process (45).…”

Section: Discussionmentioning

confidence: 99%

Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa

Rashid

Kornberg

2000

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

739

598

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Polyphosphate kinase (PPK), encoded by the ppk gene, is the principal enzyme in many bacteria for the synthesis of inorganic polyphosphate (poly P) from ATP. A knockout mutant in the ppk gene of Pseudomonas aeruginosa PAO1 is impaired in flagellar swimming motility on semisolid agar plates. The mutant is deficient in type IV pili-mediated twitching motility and in a ''swarming motility'' previously unobserved in P. aeruginosa. In swarming cultures, the polar monotrichous bacteria have differentiated into elongated and polar multitrichous cells that navigate the surface of solid media. All of the motility defects in the ppk mutant could be complemented by a plasmid harboring the ppk gene. Because bacterial motility is often crucial for their survival in a natural environment and for systemic infection inside a host, the dependence for motility on PPK reveals important roles for poly P in diverse processes such as biofilm formation, symbiosis, and virulence.I norganic polyphosphate (poly P) is a linear chain of tens or many hundreds of phosphate residues linked by high-energy phosphoanhydride bonds. It is found in every cell in nature: bacterial, archaeal, fungal, protozoan, plant, and animal (1, 2). Poly P has numerous and varied biological functions depending on where it is (species, cell, or subcellular compartment) and when it is needed. Among these functions are substitution for ATP in kinase reactions; reservoir of phosphate; chelation of divalent metals; capsule of bacteria; and regulatory roles in growth, development, stress, and deprivation (1, 2). In our studies of Escherichia coli, the most significant function observed thus far is its regulatory role in adapting to nutritional stringencies and environmental stresses, and for survival in the stationary phase of growth (3). This role has been inferred from the behavior of mutant cells lacking polyphosphate kinase (PPK), the enzyme responsible for the synthesis of poly P from ATP (4).Motility is arguably one of the most impressive features in microbial physiology. Movement in aqueous environments by swimming or along surfaces by using different modes of translocation has been classified into several distinct forms (5). Swimming on a surface takes place when the fluid film is sufficiently thick and the micromorphological pattern is unorganized. When the fluid layer on a surface is relatively thin, the swimming bacteria become elongated and hyperflagellated and move in a coordinated manner known as ''swarming'' (5-7). Twitching motility is another form of translocation on a solid surface in which the micromorphological pattern is less organized than in swarming (5, 8). Among these three modes of surface translocation, swimming and swarming depend on flagella, whereas twitching depends on type IV pili (5).These various forms of surface motility enable bacteria to establish symbiotic and pathogenic associations with plants and animals (9-11). Potential benefits of motility include increased efficiency of nutrient acquisition, avoidance of toxic substances, ab...

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Section: Discussionmentioning

confidence: 99%

Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa

Rashid

Kornberg

2000

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

739

598

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“…As described in the introduction to this report, M. xanthus is one of the best-studied gliding bacteria. Swarming motility is widespread among eubacteria (16,17) and has been extensively studied in Vibrio parahaemolyticus, Proteus mirabilis (1,7,24), and recently in Serratia liquefaciens, Escherichia coli, and Salmonella typhimurium (8,15,16). On appropriate surfaces, these bacteria undergo a series of changes and transform from "swimmer" cells to differentiated "swarmer" cells.…”

Section: Discussionmentioning

confidence: 99%

Myxococcus xanthus dif Genes Are Required for Biogenesis of Cell Surface Fibrils Essential for Social Gliding Motility

et al. 2000

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Myxococcus xanthus social (S) gliding motility has been previously reported by us to require the chemotaxis homologues encoded by the dif genes. In addition, two cell surface structures, type IV pili and extracellular matrix fibrils, are also critical to M. xanthus S motility. We have demonstrated here that M. xanthus dif genes are required for the biogenesis of fibrils but not for that of type IV pili. Furthermore, the developmental defects of dif mutants can be partially rescued by the addition of isolated fibril materials. Along with the chemotaxis genes of various swarming bacteria and the pilGHIJ genes of the twitching bacterium Pseudomonas aeruginosa, the M. xanthus dif genes belong to a unique class of bacterial chemotaxis genes or homologues implicated in the biogenesis of structures required for bacterial surface locomotion. Genetic studies indicate that the dif genes are linked to the M. xanthus dsp region, a locus known to be crucial for M. xanthus fibril biogenesis and S gliding.

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“…Bacterial cell elongation occurs after treatment with ␤-lactam antibiotics, such as cephalexin (13,24,28,30), from mutations in the cell division gene lonS (32), or upon differentiation to swarmer cells (3,6,9,15,25). We have previously reported that the MCPs of cephalexin-treated E. coli cells are localized not only to the cell poles but also at intervals along the length of the elongated cell (24).…”

mentioning

confidence: 99%

Evolutionary Conservation of Methyl-Accepting Chemotaxis Protein Location in Bacteria and Archaea

Gestwicki¹,

Lamanna²,

Harshey

et al. 2000

J Bacteriol

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The methyl-accepting chemotaxis proteins (MCPs) are concentrated at the cell poles in an evolutionarily diverse panel of bacteria and an archeon. In elongated cells, the MCPs are located both at the poles and at regions along the length of the cells. Together, these results suggest that MCP location is evolutionarily conserved.Prokaryotic processes, such as cell division and chemotaxis, often depend on the asymmetric or nonuniform distribution of proteins to subcellular locations (for a recent review on this subject, see reference 31). The methyl-accepting chemotaxis proteins (MCPs) are components of the chemotactic response system in Bacteria and Archaea (1,12,16,35). The subcellular location of MCPs has been determined for four prokaryotes: Caulobacter crescentus (2), Escherichia coli (23, 24), Bacillus subtilis (17), and Rhodobacter sphaeroides (14). In these species, the MCPs are concentrated primarily at the cell poles. The location of the MCPs may be involved in the regulation of E. coli chemotaxis (4,8,20), as MCP clustering has been implicated in regulating ligand binding and signaling in this bacterium (7,10,19,21,22,34). An understanding of MCP localization in a wide range of other bacteria and archaea could illuminate the relationship between MCP location and regulation of chemotaxis.Previous microscopy studies that have explored the subcellular location of MCPs have utilized anti-MCP antibodies raised against the MCP of the organism being studied (2,17,23,24). Hazelbauer and coworkers have reported that antibodies raised against Trg, an E. coli MCP, can be used in Western blottings to identify proteins antigenically related to the E. coli MCPs from a number of different organisms (1,26,27). These results suggest that anti-Trg antibodies could be used in fluorescence microscopy experiments as convenient reagents to visualize the subcellular location of MCPs in a variety of organisms.To explore the conservation of MCP location, we selected a representative panel of bacterial species and an archaeon. The species were chosen to represent chemotactically active strains that, relative to E. coli, are either evolutionarily (5, 18) similar (e.g., Vibrio furnissii [36]), divergent (e.g., Spirochaeta aurantia [11]), or highly divergent (e.g., Halobacterium salinarium [29,33]).Cells were grown in the following liquid media supplemented with 10 mM D-galactose: E. coli, Luria broth (LB) (1% tryptone, 0.5% yeast extract, 0.5% NaCl); V. furnissii, high-salt LB (1% tryptone, 0.5% yeast extract, 2% NaCl); S. aurantia, GTY (10 mM D-glucose, 4% tryptone, 2% yeast extract, 10 mM phosphate buffer [pH 7.0]); H. salinarium, complex medium (27 mM KCl, 166 mM MgSO 4 , 10 mM sodium citrate, 4.3 M NaCl, 1% peptone, 2 mM CaCl 2 ). We used anti-Trg antibodies to determine the location of MCPs by fluorescence microscopy (23, 24).As has been seen in investigations of C. crescentus (2), E. coli (10,23,24), B. subtilis (16), and R. sphaeroides (14), fluorescence is observed primarily at the poles of both V. furnissii and S. aurantia...

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The chemotaxis system, but not chemotaxis, is essential for swarming motility in Escherichia coli

Cited by 133 publications

References 42 publications

Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa

Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa

Myxococcus xanthus dif Genes Are Required for Biogenesis of Cell Surface Fibrils Essential for Social Gliding Motility

Evolutionary Conservation of Methyl-Accepting Chemotaxis Protein Location in Bacteria and Archaea

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