Bacterial mechanosensing: the force will be with you, always

Gordon, Vernita; Wang, Liyun

doi:10.1242/jcs.227694

Cited by 81 publications

(61 citation statements)

References 92 publications

(133 reference statements)

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“…In E. coli and P. mirabilis with the variation in viscosity of their fluid environment, mechanical load varies which ultimately results in obstruction or inhibition of their flagellar rotation ( Chawla et al, 2017 ). Similar results were observed with B. subtilis , Caulobacter crescentus and Vibrio parahaemolyticus in case of contact with surfaces, which provided evidence for the role of flagella in mechanism associated with surface-sensing and initiation of surface-dependent behavior ( Lele et al, 2013 ; Gordon and Wang, 2019 ). This provides evidence that flagella are the main surface sensor in various bacteria and thus play an important role in pathogen-host interaction.…”

Section: Surface Appendages In Bacteriasupporting

confidence: 78%

“…It comprises of a membrane-bound histidine kinase and a cytoplasmic response regulator to sense the stimulus and thus mediate the cellular response, respectively. For example in E. coli the major systems involved in sensing physicochemical changes and thus resulting in downstream regulation for biofilm formation are CpxAR, EnvZ/OmpR and RcsCDB (Gordon and Wang, 2019;Kimkes and Heinemann, 2020).…”

Section: Contact-dependent Mechanosensingmentioning

confidence: 99%

“…Next to this occurs the adhesion of bacterial cell appendages to the surface. Studies suggest that bacterial motility appendages such as type-IV pili, flagella and even the envelope proteins are likely to be the potential mechanosensory elements involved in adhesion (Gordon and Wang, 2019). As the bacterium attaches its appendages to the surface, due to the change in mechanical properties of bacterium's environment, biological responses such as phenotypic changes are observed.…”

Section: Contact-dependent Mechanosensingmentioning

confidence: 99%

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Role of Bacterial Cytoskeleton and Other Apparatuses in Cell Communication

Singhi

Srivastava

2020

Front. Mol. Biosci.

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The bacterial cytoskeleton is crucial for sensing the external environment and plays a major role in cell to cell communication. There are several other apparatuses such as conjugation tubes, membrane vesicles, and nanotubes used by bacterial cells for communication. The present review article describes the various bacterial cytoskeletal proteins and other apparatuses, the physical structures they form and their role in sensing environmental stress. The implications of this cellular communication in pathogenicity are discussed.

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Section: Surface Appendages In Bacteriasupporting

confidence: 78%

Section: Contact-dependent Mechanosensingmentioning

confidence: 99%

Section: Contact-dependent Mechanosensingmentioning

confidence: 99%

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Role of Bacterial Cytoskeleton and Other Apparatuses in Cell Communication

Singhi

Srivastava

2020

Front. Mol. Biosci.

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“…This variation in responses to medium type suggests that use of multiple media in characterizing mutant strains may aid in determining the universal or conditional role of that gene in filamentation and other biofilm-related phenotypes. In addition, recent work highlighting the role of mechanosensing and agar density on microbial invasion and adherence suggests substrate composition may also play a role in Candida biofilm formation [64][65][66] .…”

Section: Discussionmentioning

confidence: 99%

Automated quantification of Candida albicans biofilm-related phenotypes reveals additive contributions to biofilm production

Dunn

Fillinger

Anderson

et al. 2020

npj Biofilms Microbiomes

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Biofilms are organized communities of microbial cells that promote persistence among bacterial and fungal species. Biofilm formation by host-associated Candida species of fungi occurs on both tissue surfaces and implanted devices, contributing to host colonization and disease. In C. albicans, biofilms are built sequentially by adherence of yeast to a surface, invasion into the substrate, the formation of aerial hyphal projections, and the secretion of extracellular matrix. Measurement of these biofilm-related phenotypes remains highly qualitative and often subjective. Here, we designed an informatics pipeline for quantifying filamentation, adhesion, and invasion of Candida species on solid agar media and utilized this approach to determine the importance of these component phenotypes to C. albicans biofilm production. Characterization of 23 C. albicans clinical isolates across three media and two temperatures revealed a wide range of phenotypic responses among isolates in any single condition. Media profoundly altered all biofilm-related phenotypes among these isolates, whereas temperature minimally impacted these traits. Importantly, the extent of biofilm formation correlated significantly with the additive score for its component phenotypes under some conditions, experimentally linking the strength of each component to biofilm mass. In addition, the response of the genome reference strain, SC5314, across these conditions was an extreme outlier compared to all other strains, suggesting it may not be representative of the species. Taken together, development of a high-throughput, unbiased approach to quantifying Candida biofilm-related phenotypes linked variability in these phenotypes to biofilm production and can facilitate genetic dissection of these critical processes to pathogenesis in the host.

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“…Since the most apparent difference between growth in liquid and that in soft agar is the porous structure of agar, which interferes with flagellar rotation, we hypothesized that an increased mechanical load on the flagellar motor might signal flagellar gene expression in pathogenic E. coli. Such mechanosensing has indeed been described in several bacterial species (21,22), although its molecular mechanisms remain poorly understood. In E. coli, the load is known to cause posttranslational remodeling of the flagellar motor, increasing the number of force-generating stator units 23, but no gene-regulatory mechanosensing mediated by flagella has been reported so far.…”

Section: Z36mentioning

confidence: 99%

Flagellum-Mediated Mechanosensing and RflP Control Motility State of Pathogenic Escherichia coli

Laganenka

López

Colin

et al. 2020

mBio

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Bacterial flagellar motility plays an important role in many processes that occur at surfaces or in hydrogels, including adhesion, biofilm formation, and bacterium-host interactions. Consequently, expression of flagellar genes, as well as genes involved in biofilm formation and virulence, can be regulated by the surface contact. In a few bacterial species, flagella themselves are known to serve as mechanosensors, where an increased load on flagella experienced during surface contact or swimming in viscous media controls gene expression. In this study, we show that gene regulation by motility-dependent mechanosensing is common among pathogenic Escherichia coli strains. This regulatory mechanism requires flagellar rotation, and it enables pathogenic E. coli to repress flagellar genes at low loads in liquid culture, while activating motility in porous medium (soft agar) or upon surface contact. It also controls several other cellular functions, including metabolism and signaling. The mechanosensing response in pathogenic E. coli depends on the negative regulator of motility, RflP (YdiV), which inhibits basal expression of flagellar genes in liquid. While no conditional inhibition of flagellar gene expression in liquid and therefore no upregulation in porous medium was observed in the wild-type commensal or laboratory strains of E. coli, mechanosensitive regulation could be recovered by overexpression of RflP in the laboratory strain. We hypothesize that this conditional activation of flagellar genes in pathogenic E. coli reflects adaptation to the dual role played by flagella and motility during infection. IMPORTANCE Flagella and motility are widespread virulence factors among pathogenic bacteria. Motility enhances the initial host colonization, but the flagellum is a major antigen targeted by the host immune system. Here, we demonstrate that pathogenic E. coli strains employ a mechanosensory function of the flagellar motor to activate flagellar expression under high loads, while repressing it in liquid culture. We hypothesize that this mechanism allows pathogenic E. coli to regulate its motility dependent on the stage of infection, activating flagellar expression upon initial contact with the host epithelium, when motility is beneficial, but reducing it within the host to delay the immune response.

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Bacterial mechanosensing: the force will be with you, always

Cited by 81 publications

References 92 publications

Role of Bacterial Cytoskeleton and Other Apparatuses in Cell Communication

Role of Bacterial Cytoskeleton and Other Apparatuses in Cell Communication

Automated quantification of Candida albicans biofilm-related phenotypes reveals additive contributions to biofilm production

Flagellum-Mediated Mechanosensing and RflP Control Motility State of Pathogenic Escherichia coli

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