Under Elevated c-di-GMP in Escherichia coli, YcgR Alters Flagellar Motor Bias and Speed Sequentially, with Additional Negative Control of the Flagellar Regulon via the Adaptor Protein RssB

Nieto, Vincent; Partridge, Jonathan D.; Severin, Geoffrey B.; Lai, Run-Zhi; Waters, Christopher M.; Parkinson, John S.; Harshey, Rasika M.

doi:10.1128/jb.00578-19

Cited by 25 publications

(24 citation statements)

References 78 publications

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“…Further, the pathway is independent of the known sensory transduction pathway since the observed speed modulation also occurs in the absence of CheY (Fig 4F). Recent studies have shown that c-di-GMP effector YcgR can inhibit flagellar motility by interacting directly with the motor to modulate both its bias and speed [22,23,41]. While the aforementioned mechanism has been shown to inhibit motor speeds there is no evidence that the same can enhance motor speeds beyond pre-stimulus levels.…”

Section: Discussionmentioning

confidence: 99%

Ligand Sensing Enhances Bacterial Flagellar Motor Output via Stator Recruitment

Naaz

Agrawal

Chakraborty

et al. 2020

Preprint

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The phenomenon of chemotaxis in bacteria, where the cells migrate towards or away from chemicals, has been extensively studied in the past. For flagellated bacteria such as Escherichia coli, a change in chemical concentration in its environment is sensed by a chemoreceptor and communicated via a well-characterised signalling pathway to the flagellar motor. It has been widely accepted that the signals change the rotation bias of the motor without influencing the motor speed. Here, we obtain results to the contrary and show that the bacteria is also capable of modulating motor speed on merely sensing a ligand. The response of single bacterial flagellar motors to step changes in ligand concentration demonstrate the presence of a sophisticated signalling pathway that controls the motor speed via recruitment of stators. Swimming speeds measured at the population level also corroborate the above observation. Experiments performed with mutant strains delineate the role of metabolism and sensing in the modulation of motor speed and show how speed changes along with changes in bias can significantly enhance bacteria's response to changes in its environment.

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Section: Discussionmentioning

confidence: 99%

Ligand Sensing Enhances Bacterial Flagellar Motor Output via Stator Recruitment

Naaz

Agrawal

Chakraborty

et al. 2020

Preprint

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“…In contrast to c-di-GMP 0 strains of Salmonella Enteritidis and C. crescentus, which show a flagellar motility defect, the S. meliloti c-di-GMP 0 strain performs normally in swimming motility assays (Schäper et al 2016). Unlike E. coli and P. aeruginosa, whose flagellar gene expression is repressed in c-di-GMP-dependent manner (Hickman and Harwood 2008;Nieto et al 2019), no effect on flagellar gene transcript abundances was observed in S. meliloti overproducing DGC PleD (Schäper et al 2017). Artificial increase of c-di-GMP levels upon DGC overproduction in S. meliloti and the two related alpha-rhizobia Rhizobium etli and Rhizobium leguminosarum resulted in inhibition of swimming motility, consistent with the general paradigm (Schäper et al 2016;Perez-Mendoza et al 2014).…”

Section: C-di-gmp-mediated Regulation Of Motilitymentioning

confidence: 99%

Cyclic di-GMP signaling controlling the free-living lifestyle of alpha-proteobacterial rhizobia

Krol

Schäper

Becker

2020

Biological Chemistry

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Cyclic-di-GMP (c-di-GMP) is a ubiquitous bacterial second messenger which has been associated with a motile to sessile lifestyle switch in many bacteria. Here, we review recent insights into c-di-GMP regulated processes related to environmental adaptations in alphaproteobacterial rhizobia, which are diazotrophic bacteria capable of fixing nitrogen in symbiosis with their leguminous host plants. The review centers on Sinorhizobium meliloti, which in the recent years was intensively studied for its c-di-GMP regulatory network.

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“…The relationship between motility and biofilm formation is complex. Although it is widely understood that motility is crucial for biofilm formation 47,48 , it is also true that motility and curli production have an inverse relationship, where csgD directly represses fliE 69 and induces c-di-GMP synthesis through adrA, which reduces motility through ycgR [70][71][72] . This is often referred to as a lifestyle 'switch', where biofilm matrix production represses motility for a motile-to-sessile lifestyle transition 73 .…”

Section: Discussionmentioning

confidence: 99%

Massively parallel transposon mutagenesis identifies temporally essential genes for biofilm formation inEscherichia coli

Holden

Yasir

Turner

et al. 2020

Preprint

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Biofilms complete a life cycle where cells aggregate, grow and produce a structured community before dispersing to seed biofilms in new environments. Progression through this life cycle requires controlled temporal gene expression to maximise fitness at each stage. Previous studies have focused on the essential genome for the formation of a mature biofilm, but here we present an insight into the genes involved at different stages of biofilm formation. We used TraDIS-Xpress; a massively parallel transposon mutagenesis approach using transposon-located promoters to assay expression of all genes in the genome. We determined how gene essentiality and expression affects the fitness of E. coli growing as a biofilm on glass beads after 12, 24 and 48 hours. A selection of genes identified as important were then validated independently by assaying biofilm biomass, aggregation, curli biosynthesis and adhesion ability of defined mutants. We identified 48 genes that affected biofilm fitness including genes with known roles and those not previously implicated in biofilm formation. Regulation of type 1 fimbriae and motility were important at all time points. Adhesion and motility were important for the early biofilm, whereas matrix production and purine biosynthesis were only important as the biofilm matured. We found strong temporal contributions to biofilm fitness for some genes including some which were both beneficial and detrimental depending on the stage at which they are expressed, including dksA and dsbA. Novel genes implicated in biofilm formation included ychM and truA involved in cell division, crfC and maoP in DNA housekeeping and yigZ and ykgJ of unknown function. This work provides new insights into the requirements for successful biofilm formation through the biofilm life cycle and demonstrates the importance of understanding expression and fitness through time.

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Under Elevated c-di-GMP in Escherichia coli, YcgR Alters Flagellar Motor Bias and Speed Sequentially, with Additional Negative Control of the Flagellar Regulon via the Adaptor Protein RssB

Cited by 25 publications

References 78 publications

Ligand Sensing Enhances Bacterial Flagellar Motor Output via Stator Recruitment

Ligand Sensing Enhances Bacterial Flagellar Motor Output via Stator Recruitment

Cyclic di-GMP signaling controlling the free-living lifestyle of alpha-proteobacterial rhizobia

Massively parallel transposon mutagenesis identifies temporally essential genes for biofilm formation inEscherichia coli

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