Bacterial Wheel Locks: Extracellular Polysaccharide Inhibits Flagellar Rotation

Waters, Christopher M.

doi:10.1128/jb.02147-12

Cited by 6 publications

(8 citation statements)

References 12 publications

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“…3B). Interestingly, both PilZ and FlgZ were previously shown to be involved in the repression of swarming motility on agar surfaces in a P. aeruginosa strain that had high levels of c-di-GMP due to the absence of a phosphodiesterase; furthermore, FlgZ regulates flagellar motility in other species (29,30,56,57). Our data indicated that PilZ and FlgZ play either independent or partially functionally redundant roles in motility repression by ethanol.…”

Section: Resultsmentioning

confidence: 59%

“…In pseudomonads and other bacteria, motility repression occurs in multiple ways, including (i) obstruction of the flagellum by exopolysaccharides (30,31), (ii) transcriptional downregulation of flagellar gene expression (32,33), (iii) loss of flagellar rotation by c-di-GMP-bound effector proteins and their interactions with flagellum motor components (32,34,35), (iv) sequestration of flagellar motor proteins by c-di-GMPbound effectors (29,36,37), and (v) inhibition of flagellar rotation switching (clockwise versus counterclockwise) (38)(39)(40). In most Gram-negative bacteria, the flagellar motor is composed of two structures, the rotor (FliG, FliM, and FliN), which determines clockwise or counterclockwise rotation (the switch complex), and the stator (MotA and MotB), which generates torque for flagellar rotation powered by proton motive force (41)(42)(43).…”

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confidence: 99%

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Ethanol Decreases Pseudomonas aeruginosa Flagellar Motility through the Regulation of Flagellar Stators

et al. 2019

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Pseudomonas aeruginosa frequently encounters microbes that produce ethanol. Low concentrations of ethanol reduced P. aeruginosa swim zone area by up to 45% in soft agar. The reduction of swimming by ethanol required the flagellar motor proteins MotAB and two PilZ domain proteins (FlgZ and PilZ). PilY1 and the type 4 pilus alignment complex (comprising PilMNOP) were previously implicated in MotAB regulation in surface-associated cells and were required for ethanol-dependent motility repression. As FlgZ requires the second messenger bis-(3′-5′)-cyclic dimeric GMP (c-di-GMP) to represses motility, we screened mutants lacking genes involved in c-di-GMP metabolism and found that mutants lacking diguanylate cyclases SadC and GcbA were less responsive to ethanol. The double mutant was resistant to its effects. As published previously, ethanol also represses swarming motility, and the same genes required for ethanol effects on swimming motility were required for its regulation of swarming. Microscopic analysis of single cells in soft agar revealed that ethanol effects on swim zone area correlated with ethanol effects on the portion of cells that paused or stopped during the time interval analyzed. Ethanol increased c-di-GMP in planktonic wild-type cells but not in ΔmotAB or ΔsadC ΔgcbA mutants, suggesting c-di-GMP plays a role in the response to ethanol in planktonic cells. We propose that ethanol produced by other microbes induces a regulated decrease in P. aeruginosa motility, thereby promoting P. aeruginosa colocalization with ethanol-producing microbes. Furthermore, some of the same factors involved in the response to surface contact are involved in the response to ethanol. IMPORTANCE Ethanol is an important biologically active molecule produced by many bacteria and fungi. It has also been identified as a potential marker for disease state in cystic fibrosis. In line with previous data showing that ethanol promotes biofilm formation by Pseudomonas aeruginosa, here we report that ethanol reduces swimming motility using some of the same proteins involved in surface sensing. We propose that these data may provide insight into how microbes, via their metabolic byproducts, can influence P. aeruginosa colocalization in the context of infection and in other polymicrobial settings.

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Section: Resultsmentioning

confidence: 59%

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confidence: 99%

Ethanol Decreases Pseudomonas aeruginosa Flagellar Motility through the Regulation of Flagellar Stators

et al. 2019

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“…The use of c-di-GMP insensitive ycgR mutants demonstrated that BC produced by neighboring cells did not affect motility. Waters (2013) suggested that inhibition of motility is due to a flagellar “wheel lock,” wherein BC is secreted in close proximity to a cell’s own flagella, mechanically binding it and consequently preventing its rotation. Motility was recovered when the putative endoglucanase gene bcsZ was over-produced in the ycgR mutants, indicating BC can be hydrolyzed as a quick release mechanism to regain motility ( Zorraquino et al, 2013 ).…”

Section: Animal–bacteria Interactions Of Bc Producersmentioning

confidence: 99%

Establishing a Role for Bacterial Cellulose in Environmental Interactions: Lessons Learned from Diverse Biofilm-Producing Proteobacteria

2015

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Bacterial cellulose (BC) serves as a molecular glue to facilitate intra- and inter-domain interactions in nature. Biosynthesis of BC-containing biofilms occurs in a variety of Proteobacteria that inhabit diverse ecological niches. The enzymatic and regulatory systems responsible for the polymerization, exportation, and regulation of BC are equally as diverse. Though the magnitude and environmental consequences of BC production are species-specific, the common role of BC-containing biofilms is to establish close contact with a preferred host to facilitate efficient host–bacteria interactions. Universally, BC aids in attachment, adherence, and subsequent colonization of a substrate. Bi-directional interactions influence host physiology, bacterial physiology, and regulation of BC biosynthesis, primarily through modulation of intracellular bis-(3′→5′)-cyclic diguanylate (c-di-GMP) levels. Depending on the circumstance, BC producers exhibit a pathogenic or symbiotic relationship with plant, animal, or fungal hosts. Rhizobiaceae species colonize plant roots, Pseudomonadaceae inhabit the phyllosphere, Acetobacteriaceae associate with sugar-loving insects and inhabit the carposphere, Enterobacteriaceae use fresh produce as vehicles to infect animal hosts, and Vibrionaceae, particularly Aliivibrio fischeri, colonize the light organ of squid. This review will highlight the diversity of the biosynthesis and regulation of BC in nature by discussing various examples of Proteobacteria that use BC-containing biofilms to facilitate host–bacteria interactions. Through discussion of current data we will establish new directions for the elucidation of BC biosynthesis, its regulation and its ecophysiological roles.

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“…3B). Interestingly, both PilZ and FlgZ were shown previously to be involved in the repression of swarming motility on agar surfaces in a P. aeruginosa strain that had high levels of c-di-GMP due to the absence of a phosphodiesterase, and to regulate flagellar motility in other species (22, 27, 49, 50). Together, these data indicated that PilZ and FlgZ play partially redundant roles in ethanol-dependent motility repression.…”

Section: Resultsmentioning

confidence: 99%

“…One of the roles of high c-di-GMP in P. aeruginosa is the down-regulation of flagellar motility (5, 7, 22–26). In pseudomonads and other bacteria, motility repression occurs in multiple ways, including (i) obstruction of the flagellum by exopolysaccharides (27, 28), (ii) transcriptional down-regulation of flagellar gene expression (26, 29), (iii) loss of flagellar rotation by c-di-GMP-bound effector proteins and their interactions with flagellum motor components (26, 30, 31), (iv) sequestration of flagellar motor proteins by c-di-GMP-bound effectors (22, 24), and (v) inhibition of flagellar rotation switching (clockwise vs. counterclockwise) (25, 32, 33). In Gram-negative bacteria, the flagellar motor is composed of two structures, the rotor (FliG, FliM, and FliN), which determines clockwise or counterclockwise rotation (the switch complex), and the stator (MotA and MotB), which generates torque for flagellar rotation powered by proton motive force (34–36).…”

Section: Introductionmentioning

confidence: 99%

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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Bacterial Wheel Locks: Extracellular Polysaccharide Inhibits Flagellar Rotation

Cited by 6 publications

References 12 publications

Ethanol Decreases Pseudomonas aeruginosa Flagellar Motility through the Regulation of Flagellar Stators

Ethanol Decreases Pseudomonas aeruginosa Flagellar Motility through the Regulation of Flagellar Stators

Establishing a Role for Bacterial Cellulose in Environmental Interactions: Lessons Learned from Diverse Biofilm-Producing Proteobacteria

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

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