Singly Flagellated Pseudomonas aeruginosa Chemotaxes Efficiently by Unbiased Motor Regulation

Cai, Qiuxian; Li, Zhaojun; Ouyang, Qi; Luo, Chunxiong; Gordon, Vernita

doi:10.1128/mbio.00013-16

Cited by 43 publications

(46 citation statements)

References 38 publications

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“…The opportunistic human pathogen Pseudomonas aeruginosa assembles a single polar flagellum that powers a run-and-reverse form of motility similar to that described for Vibrio spp. (17,18). Although core structural features of the flagellum are well conserved and flagellar gene expression is regulated in similar stepwise fashions in P. aeruginosa and E. coli (19,20), the P. aeruginosa flagellum appears to have several unusual features.…”

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In Situ Structures of Polar and Lateral Flagella Revealed by Cryo-Electron Tomography

et al. 2019

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The bacterial flagellum is a sophisticated self-assembling nanomachine responsible for motility in many bacterial pathogens, including Pseudomonas aeruginosa, Vibrio spp., and Salmonella enterica. The bacterial flagellum has been studied extensively in the model systems Escherichia coli and Salmonella enterica serovar Typhimurium, yet the range of variation in flagellar structure and assembly remains incompletely understood. Here, we used cryo-electron tomography and subtomogram averaging to determine in situ structures of polar flagella in P. aeruginosa and peritrichous flagella in S. Typhimurium, revealing notable differences between these two flagellar systems. Furthermore, we observed flagellar outer membrane complexes as well as many incomplete flagellar subassemblies, which provide additional insight into mechanisms underlying flagellar assembly and loss in both P. aeruginosa and S. Typhimurium. IMPORTANCE The bacterial flagellum has evolved as one of the most sophisticated self-assembled molecular machines, which confers locomotion and is often associated with virulence of bacterial pathogens. Variation in species-specific features of the flagellum, as well as in flagellar number and placement, results in structurally distinct flagella that appear to be adapted to the specific environments that bacteria encounter. Here, we used cutting-edge imaging techniques to determine high-resolution in situ structures of polar flagella in Pseudomonas aeruginosa and peritrichous flagella in Salmonella enterica serovar Typhimurium, demonstrating substantial variation between flagella in these organisms. Importantly, we observed novel flagellar subassemblies and provided additional insight into the structural basis of flagellar assembly and loss in both P. aeruginosa and S. Typhimurium.

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In Situ Structures of Polar and Lateral Flagella Revealed by Cryo-Electron Tomography

et al. 2019

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“…One type of motility is swimming motility, which uses flagellar rotation to move through aqueous environments using a reversible rotary machinery to propel the bacterium and the transmembrane proton gradient as an energy source (5). The direction and regulation of flagellar rotation enable bacteria to move toward favorable environments and away from unfavorable environments, a process termed chemotaxis (5,6). Twitching motility depends on the type IV pilus to enable movement on solid surfaces through extension and retraction of polar pili (7).…”

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Surfing Motility: a Conserved yet Diverse Adaptation among Motile Bacteria

2018

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Bacterial rapid surfing motility is a novel surface adaptation of in the presence of the glycoprotein mucin. Here, we show that other Gram-negative motile bacterial species, including, ,, , and, also exhibit the physical characteristics of surfing on the surface of agar plates containing 0.4% mucin, where surfing motility was generally more rapid and less dependent on medium viscosity than was swimming motility. As previously observed in , all surfing species exhibited some level of broad-spectrum adaptive resistance, although the antibiotics to which they demonstrated surfing-mediated resistance differed. Surfing motility in was found to be dependent on the quorum-sensing systems of this organism; however, this aspect was not conserved in other tested bacterial species, including and, as demonstrated by assaying specific quorum-sensing mutants. Thus, rapid surfing motility is a complex surface growth adaptation that is conserved in several motile bacteria, involves flagella, and leads to diverse broad-spectrum antibiotic resistance, but it is distinct in terms of dependence on quorum sensing. This study showed for the first time that surfing motility, a novel form of surface motility first discovered in under artificial cystic fibrosis conditions, including the presence of high mucin content, is conserved in other motile bacterial species known to be mucosa-associated, including, , and Here, we demonstrated that key characteristics of surfing, including the ability to adapt to various viscous environments and multidrug adaptive resistance, are also conserved. Using mutagenesis assays, we also identified the importance of all three known quorum-sensing systems, Las, Rhl, and Pqs, in in regulating surfing motility, and we also observed a conserved dependence of surfing on flagella in certain species.

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“…P. aeruginosa is a monotrichous flagellated bacterium whose flagellar motility is governed by a run-reverse pattern (32, 57) rather than the run-tumble pattern in organisms with peritrichous flagella like E. coli (58). P. aeruginosa directional movement is due to a change in the flagellar rotation (clockwise or counterclockwise) and this rotation change is called a ‘reversal’.…”

Section: Resultsmentioning

confidence: 99%

“…P. aeruginosa directional movement is due to a change in the flagellar rotation (clockwise or counterclockwise) and this rotation change is called a ‘reversal’. The frequency of reversals can impact the area covered since P. aeruginosa must slow its normal speed from 40–55 µm/sec (38, 53, 57) to as low as 15 µm/sec immediately before a reversal (57). To determine if the decrease in swim zone diameter in ethanol was a result of a change in reversal frequencies, this parameter was measured in the absence and presence of 1% ethanol.…”

Section: Resultsmentioning

confidence: 99%

“…Additionally, P. aeruginosa and related bacteria that utilize a run-reverse-turn trajectory, spend equal time going clockwise or counterclockwise with variation in their pause duration in order to turn at different angles to maximize space exploration (32). Since chemotaxis involves the modulation of reversal frequencies (57), these data may suggest that ethanol also affect chemotaxis in P. aeruginosa . More work is required to determine if ethanol influences positive or negative chemotactic pathways.…”

Section: Discussionmentioning

confidence: 99%

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Ethanol decreases Pseudomonas aeruginosa flagellar motility through a cyclic-di-GMP- and stator-dependent pathway

Lewis

Baker

Chen

et al. 2018

Preprint

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22Pseudomonas aeruginosa frequently encounters microbes that produce bioactive metabolites 23 including ethanol. At concentrations that do not affect growth, we found that ethanol reduces P. 24 aeruginosa motility by 30% in a swim agar assay and this decrease is accompanied by a 2.5-25 fold increase in levels of cyclic diguanylate (c-di-GMP), a second messenger that represses 26 motility, in planktonic cells. A screen of mutants lacking genes involved in c-di-GMP metabolism 27identified SadC and GcbA as diguanylate cyclases involved in swim zone reduction by ethanol 28 and ethanol-induced c-di-GMP production. The reduction of swimming in response to ethanol 29 also required the stator set, MotAB, two PilZ-domain proteins (FlgZ and PilZ), PilY1-a proposed 30 surface-sensing protein, and PilMNOP, which comprises the pilus alignment complex and these 31 proteins have been previously implicated in the control of motility on agar surfaces. Microscopic 32 analysis of the fraction of quiescent cells in swim medium showed that ethanol decreased the 33 portion of motile cells in the wild type, but had opposite effects in the ∆pilY1, ∆pilMNOP, 34 ∆motAB, and ∆pilZ∆flgZ mutants. Together, these data indicate ethanol induces a regulated 35 change in motility in planktonic cells at concentrations similar to those produced by other 36 microbes. We propose that this ethanol-responsiveness may contribute to the co-localization of 37 P. aeruginosa with ethanol-producing microbes. 38 39 3 Importance 40Ethanol is an important, biologically active molecule produced by many bacteria and fungi. It 41 has also been identified as a potential marker for disease state in cystic fibrosis. In line with 42 previous data that show that ethanol promotes biofilm formation by Pseudomonas aeruginosa, 43 here we report that ethanol also induces cyclic-di-GMP levels in planktonic cells and reduces 44 swimming motility using some of the same proteins involved in surface sensing. We propose 45 that these data may provide insight into how microbes can influence P. aeruginosa localization 46 and surface association in the context of infection and in other polymicrobial settings. 47 49Ethanol, in addition to being a common fermentation product and a carbon source, can 50 also serve as a signaling molecule for many microbes. For example, fungal gardens formed as 51 part of a symbiosis between ambrosia beetles and their fungal symbionts, Ambrosiella and 52Raffaelea, are preferentially localized to sites with higher ethanol (1). In the parasite 53 Toxoplasma gondii, low concentrations of ethanol (<200 mM or 1.2%) facilitates an increase in 54 the second messenger inositol 1, 4, 5-triphosphate, resulting in increased intracellular calcium 55 and increased host colonization (2, 3). In Acinetobacter baumannii, a Gram-negative 56 opportunistic pathogen, ethanol causes an increase in virulence and an increase in 57 carbohydrate leading to biofilm formation and repression of motility through mechanisms not yet 58 described (4). In Pseudomonas aeruginosa, exogeno...

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Singly Flagellated Pseudomonas aeruginosa Chemotaxes Efficiently by Unbiased Motor Regulation

Cited by 43 publications

References 38 publications

In Situ Structures of Polar and Lateral Flagella Revealed by Cryo-Electron Tomography

In Situ Structures of Polar and Lateral Flagella Revealed by Cryo-Electron Tomography

Surfing Motility: a Conserved yet Diverse Adaptation among Motile Bacteria

Ethanol decreases Pseudomonas aeruginosa flagellar motility through a cyclic-di-GMP- and stator-dependent pathway

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