Polar Localization of the Serine Chemoreceptor of Escherichia coli Is Nucleoid Exclusion-Dependent

Neeli-Venkata, Ramakanth; Startceva, Sofia; Annila, Teppo; Ribeiro, André S.

doi:10.1016/j.bpj.2016.10.024

Cited by 17 publications

(20 citation statements)

References 63 publications

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“…In a recent report it was suggested that the serine MCP Tsr of E. coli is driven to cell poles by the ‘volume exclusion’ effect of the nucleoid (17). To examine whether nucleoids influence the distribution of Tar, we stained the cephalexin treated cells with the fluorescence DNA dye DAPI to visualize the nucleoids (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Pulldown experiments have suggested a direct interaction between TolA and chemoreceptors. However, a recent study questioned the role of the Tol-Pal complex in chemoreceptor localization (17). To verify this, we expressed the Tar-mGFP fusion in a pal deletion mutant.…”

Section: Resultsmentioning

confidence: 99%

“…The trans-envelope Tol-Pal complex is a widely conserved component of the cell envelope of Gram-negative bacteria, and is involved in several processes among which cell division (15, 16). In contrast to this, another recent study showed that, at least for the serine chemoreceptor Tsr, the Tol-Pal complex is not required for polar localization, and that nucleoid exclusion is the driving force for polar localization of MCPs (17). Here, we evaluated the different polar localization models in E. coli using the aspartate chemoreceptor Tar.…”

Section: Introductionmentioning

confidence: 92%

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Membrane curvature and the Tol-Pal complex determine polar localization of the chemoreceptor Tar inE. coli

Saaki

Strahl

Hamoen

2017

Preprint

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18Chemoreceptors are localized at the cell poles of Escherichia coli and other rod-shaped 19 bacteria. Over the years different mechanisms have been put forward to explain this polar 20 localization; from stochastic clustering, membrane curvature driven localization, interactions 21 with the Tol-Pal complex, to nucleoid exclusion. To evaluate these mechanisms, we monitored 22 the cellular localization of the aspartate chemoreceptor Tar in different deletion mutants. We 23 did not find any indication for either stochastic cluster formation or nucleoid exclusion. 24However, the presence of a functional Tol-Pal complex appeared to be essential to retain Tar 25 at cell poles. This finding also implies that the curvature of cell poles does not attract 26 chemoreceptor complexes. Interestingly, Tar still accumulated at midcell in tol and in pal 27 deletion mutants. In these mutants, the protein appears to gather at the base of division septa, 28 a region characterised by strong membrane curvature. Chemoreceptors, like Tar, form trimer-29 of-dimers that bend the cell membrane due to a rigid tripod structure with an estimated 30 curvature of approximately 37 nm. This curvature approaches the curvature of the cell 31 membrane generated during cell division, and localization of chemoreceptor tripods at curved 32 membrane areas is therefore energetically favourable as it lowers membrane tension. Indeed, 33 when we introduced mutations in Tar that abolish the rigid tripod structure, the protein was no 34 longer able to accumulate at midcell or cell poles. These findings favour a model where 35 chemoreceptor localization in E. coli is driven by strong membrane curvature and association 36 with the Tol-Pal complex. 37 38 Importance 39 Bacteria have exquisite mechanisms to sense and to adapt to the environment they live in.40 One such mechanism involves the chemotaxis signal transduction pathway, in which 41 chemoreceptors specifically bind certain attracting or repelling molecules and transduce the 42 signals to the cell. In different rod-shaped bacteria, these chemoreceptors localize specifically 43 to cell poles. Here, we examined the polar localization of the aspartate chemoreceptor Tar in 44 3 E. coli, and found that membrane curvature at cell division sites and interaction with the Tal-45 pol protein complex, localize Tar at cell division sites, the future cell poles. This study shows 46 how membrane curvature can guide localization of proteins in a cell. 47 65 future division sites. This model is referred to as the 'stochastic nucleation model' (5-7). 66Another theory postulated that MCPs preferably assemble at the curved membrane of cell 67 poles (8). Chemoreceptors form membrane spanning trimers-of-dimers that interact at their 68 cytoplasmic domain at a slight angle thereby forming a tripod-like configuration (9). 69Consequently, the trimer of dimers prefer bend membrane areas due to the reduced curvature 70 mismatch. (10, 11). This model was recently supported by mechanically bending of whole E. 71coli cells in curve...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 92%

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Membrane curvature and the Tol-Pal complex determine polar localization of the chemoreceptor Tar inE. coli

Saaki

Strahl

Hamoen

2017

Preprint

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“…Chemotaxis proteins localize to distinct regions within a bacterial cell – this localization can vary depending on if it is a random or ordered process. A variety of mechanisms have been proposed including membrane curvature, stochastic nucleation, nuclear exclusion and interaction with the Tol-Pal complex [25–29]. These different mechanisms may not be exclusive of each other as these studies focus on different bacteria such as E. coli and Bacillus subtilis , as well as different MCPs within the same species.…”

Section: Discussionmentioning

confidence: 99%

Partitioning protein ParP directly links chemotaxis to biofilm dispersal in Pseudomonas aeruginosa

Reinhardt

Bardy

2018

Preprint

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11The recent characterization of partitioning proteins in the localization of chemotaxis 12 signal transduction systems was proposed to have broad implications for polarly-flagellated non-13 enterobacteriaceae gamma-proteobacteria. These studies showed that the loss of either 14 partitioning protein resulted in equivalent reductions in swimming motility and chemotaxis 15 protein localization and inheritance. However, the role of these chemotaxis partitioning proteins 16 outside of Vibrio spp. remains untested. Our studies on the chemotaxis partitioning proteins in 17 Pseudomonas aeruginosa revealed an unexpected role for the partitioning protein ParP. While 18 the P. aeruginosa ParC and ParP homologs are needed for wild type swimming motility, the loss 19 of ParP results in a greater swimming defect compared to the parC mutant. Our studies revealed 20 that the Par-like proteins directly interact with each other and the chemotaxis system, and ParP 21 interacts with DipA. Deletion of dipA results in a similar defect in swimming motility as the 22 parP mutant. ParP has an interdependence for polar cluster formation, but not localization, with 23 both CheA and DipA, and CheA cluster formation is partially dependent on ParP. Due to the 24 direct interactions and interdependence of cluster formation of ParP and DipA, and the similar 25 phenotypes of the parP and dipA mutants, further investigation into the role of ParP in biofilm 26 dispersion is warranted. 27 Importance 28 Impaired chemotaxis protein cluster formation or inheritance reduces chemotaxis which 29 can have an impact on of the virulence of a bacterium. In some gamma-proteobacteria there are 30 systems in place to ensure that chemotaxis proteins, like chromosomes and plasmids, are 31 localized for optimal chemotaxis and that daughter cells inherit their own clusters for use after 32 cell division. Par-like proteins have been implicated in the partitioning and localization of 33 3 chemotaxis proteins and the chemotactic ability of Vibrio spp. and Rhodobacter sphaeroides [1-34 3].We propose that Par-like proteins can do more than localize chemotaxis proteins to the poles 35 of the cells. In P. aeruginosa, they bring together other key proteins involved in regulating 36 flagellar-based motility, and we propose they function as a critical link between biofilm dispersal 37 and motility. 38 Introduction 39Spatial organization within bacterial cells results in the arrangement of proteins in distinct 40 subcellular locations. This organization is not always static, and in some instances, can change in 41 response to external cues or different stages within the bacterial lifecycle [4, 5]. There are a 42 significant number of cellular processes that are affected by spatial organization and polarity, 43 including signal transduction and motility. Bacterial chemotaxis is mediated by a two-component 44 chemosensory system wherein a motile bacterium senses chemo-effectors in its environment and 45 responds by moving towards favorable or away from unfavo...

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“…In a phosphorylated form, CheY binds to a flagellar motor, which increases the probability of clockwise rotation leading to reorientation of the swimming direction (4). The serine chemoreceptor Tsr in Escherichia coli is one of the best studied MCPs and it serves as a model for elucidating signal transduction by various experimental and computational approaches (5)(6)(7)(8)(9)(10)(11). Similarly to other chemoreceptors, the Tsr structural unit is a homodimer, where each protomer contains a periplasmic ligand-binding domain, two transmembrane helices, a HAMP domain, and an intracellular signaling domain ( Fig.…”

Section: Introductionmentioning

confidence: 99%

Interdimer “zipping” in the chemoreceptor signaling domain revealed by molecular dynamics simulations

Petukh

Ortega

Baudry

et al. 2019

Preprint

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Chemoreceptors are principal components of the bacterial sensory system that modulates cellular motility. They detect changes in the environment and transmit information to CheA histidine kinase, which ultimately controls cellular flagellar motors. The prototypical Tsr chemoreceptor in E. coli is a homodimer containing two principal functional modules: (i) a periplasmic ligand-binding domain and (ii) a cytoplasmic signaling domain. Chemoreceptor dimers are arranged into a trimer of dimers at the tip of the signaling domain comprising a minimal physical unit essential for enhancing the CheA activity several hundredfold. Trimers of dimers are arranged into highly ordered hexagon arrays at the cell pole; however, the mechanism underlying the trimer-of-dimer and higher order array formation remains unclear.Furthermore, molecular mechanisms of signal transduction that are likely to involve inter-dimer interactions are not fully understood. Here we apply all-atom, microsecond-time scale molecular dynamics simulations of the Tsr trimer of dimers atomic model in order to obtain further insight into potential interactions within the chemoreceptor signaling unit. We show extensive interactions between homodimers at the hairpin tip of the signaling domain, where strong hydrophobic interactions maintain binding. A subsequent zipping of homodimers is facilitated by electrostatic interactions, in particular by polar solvation energy and salt bridges that stabilize the final compact structure, which extends beyond the kinase interacting subdomain. Our study provides evidence that interdimer interactions within the chemoreceptor signaling domain are more complex than previously thought.

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Polar Localization of the Serine Chemoreceptor of Escherichia coli Is Nucleoid Exclusion-Dependent

Cited by 17 publications

References 63 publications

Membrane curvature and the Tol-Pal complex determine polar localization of the chemoreceptor Tar inE. coli

Membrane curvature and the Tol-Pal complex determine polar localization of the chemoreceptor Tar inE. coli

Partitioning protein ParP directly links chemotaxis to biofilm dispersal in Pseudomonas aeruginosa

Interdimer “zipping” in the chemoreceptor signaling domain revealed by molecular dynamics simulations

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