Chemotactic motility is required for invasion of the host by the fish pathogen <i>Vibrio anguillarum</i>

O'Toole, Ronan; Milton, Debra L.; Wolf‐Watz, Hans

doi:10.1046/j.1365-2958.1996.412927.x

Cited by 158 publications

(140 citation statements)

References 55 publications

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“…Consistent with the abnormal function of flagella caused by improper chemotaxis and the reduced virulence in S. typhimurium, Vibrio anguillarum, and Campylobacter jejuni (51)(52)(53), the ppk mutant of P. aeruginosa has been found to be avirulent in a burned-mouse pathogenesis model (A. N. Hamood, personal communication), even though the mutant possesses normal flagella and pili.…”

Section: Discussionmentioning

confidence: 84%

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

Rashid

Kornberg

2000

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

738

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: 84%

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

Rashid

Kornberg

2000

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

738

598

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“…The marine environment is a heterogeneous landscape at the microscale and a bacterium's ability to accurately navigate gradients of nutrients and infochemicals may provide it with a competitive advantage (Taylor and Stocker 2012). Chemotaxis is found governing bacteria − phytoplankton interactions (Bell and Mitchell 1972;Blackburn et al, 1998;Stocker and Seymour 2012), facilitating symbioses such as that between Vibrio fischeri and squid (Mandel et al, 2012), implicated in the onset of disease (Otoole et al, 1996;Banin et al, 2001;Rosenberg and Falkovitz 2004;Larsen et al, 2004;Meron et al, 2009) and common throughout coral reefs (Tout et al, 2015b). Within this framework, reef-building corals are becoming a focal system for studying the role of motility in bacteria-host interactions in the ocean.…”

Section: Discussionmentioning

confidence: 99%

Temperature-induced behavioral switches in a bacterial coral pathogen

et al. 2015

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Evidence to date indicates that elevated seawater temperatures increase the occurrence of coral disease, which is frequently microbial in origin. Microbial behaviors such as motility and chemotaxis are often implicated in coral colonization and infection, yet little is known about the effect of warming temperatures on these behaviors. Here we present data demonstrating that increasing water temperatures induce two behavioral switches in the coral pathogen Vibrio coralliilyticus that considerably augment the bacterium's performance in tracking the chemical signals of its coral host, Pocillopora damicornis. Coupling field-based heat-stress manipulations with laboratory-based observations in microfluidic devices, we recorded the swimming behavior of thousands of individual pathogen cells at different temperatures, associated with current and future climate scenarios. When temperature reached ⩾ 23°C, we found that the pathogen's chemotactic ability toward coral mucus increased by 460%, denoting an enhanced capability to track host-derived chemical cues. Raising the temperature further, to 30°C, increased the pathogen's chemokinetic ability by 457%, denoting an enhanced capability of cells to accelerate in favorable, mucus-rich chemical conditions. This work demonstrates that increasing temperature can have strong, multifarious effects that enhance the motile behaviors and host-seeking efficiency of a marine bacterial pathogen.

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“…However, rpoN is often found to control multiple functions, including flagellar synthesis and nitrogen utilization (41,50,60). Moreover, P. syringae pathovars produce a number of toxins, including syringomycins, tabtoxin, phaseolotoxin, tagetitoxin, and coronatine (6), and we have found that rpoN is required for the expression of coronatine (32).…”

mentioning

confidence: 97%

The Alternative Sigma Factor RpoN Is Required for hrp Activity in Pseudomonas syringae pv. Maculicola and Acts at the Level of hrpL Transcription

2000

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␤-Glucuronidase (uidA) reporter gene fusions were constructed for the hrpZ, hrpL, and hrpS genes from the phytopathogen Pseudomonas syringae pv. maculicola strain ES4326. These reporters, as well as an avrRpt2-uidA fusion, were used to measure transcriptional activity in ES4326 and a ES4326 rpoN mutant. rpoN was required for the expression of avrRpt2, hrpZ, and hrpL in vitro in minimal media and in vivo when infiltrated into Arabidopsis thaliana leaves. In contrast, the expression of hrpS was essentially the same in wild-type and rpoN mutant strains. Constitutive expression of hrpL in an rpoN mutant restored hrpZ transcription to wild-type levels, restored the hypersensitive response when infiltrated into tobacco (Nicotiana tobacum), and partially restored the elicitation of virulence-related symptoms but not growth when infiltrated into Arabidopsis leaves. These data indicate that rpoN-mediated control of hrp gene expression acts at the level of hrpL and that in planta growth of P. syringae is not required for the elicitation of disease symptoms.In gram-negative bacteria, transcriptional activation in response to external stimuli often involves the alternative sigma factor 54 (1, 50). 54 , which is encoded by rpoN, works in conjunction with members of the NtrC superfamily of transcriptional activators (1, 50). Among the different enzymatic pathways under 54 control are those responsible for nitrogen utilization, dicarboxylate transport, xylene degradation, and hydrogen utilization (8,39,47,79).In the case of some phytopathogenic bacterial species, rpoN has been implicated indirectly as a regulator of a large cluster of pathogenicity-related genes known as the hrp gene cluster (17,27). For example, Pseudomonas syringae pv. syringae strain 61 contains a 25-kb hrp cluster consisting of 27 genes arranged as follows : hrpKL, hrpJ, hrcV, hrpQ, hrcN, hrpOP, hrcQRSTU, hrpVT, hrcC, hrpGF, hrpED, hrcJ, hrpBZA, and hrpSR (11,33). The acronym hrp stands for hypersensitive response and pathogenicity. The genes within the hrp cluster are required not only for pathogenicity but also for elicitation of the plant resistance reaction known as the hypersensitive response (HR) (44, 45). The HR involves rapid, localized plant cell death, which is triggered by a gene-for-gene interaction between a particular avirulence (avr) gene in the pathogen and a corresponding resistance gene in the host (21, 56). The widely conserved members of the hrp cluster, designated hrc, show significant homology to members of the Yersinia type III secretory pathway and in the new simplified nomenclature bear the letter designation of the corresponding Yersinia gene (9). (The exception is hrcV, which is homologous to the Yersinia lcrD genes.)Sequence analysis of the hrp cluster in P. syringae pv. phaseolicola suggested that 54 would be required for hrp gene expression in conjunction with the hrpRS genes, which are required for expression of the remaining hrp genes in the cluster (17, 27). hrpR and hrpS encode proteins that contain the domain conserved ...

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Chemotactic motility is required for invasion of the host by the fish pathogen Vibrio anguillarum

Cited by 158 publications

References 55 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

Temperature-induced behavioral switches in a bacterial coral pathogen

The Alternative Sigma Factor RpoN Is Required for hrp Activity in Pseudomonas syringae pv. Maculicola and Acts at the Level of hrpL Transcription

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