Bacterial flagella disrupt host cell membranes and interact with cytoskeletal components

Wolfson, E; Elvidge, Johanna; Tahoun, Amin; Gillespie, Trudi; Mantell, Judith; McAteer, Sean P.; Rossez, Yannick; Paxton, Edith; Lane, Fiona M.; Shaw, Darren; Gill, Andrew C.; Steveni, Jo; Verkade, Paul; Blocker, Ariel; Mahajan, Aditya; Gally, David L.

doi:10.1101/2020.02.12.945204

Cited by 4 publications

(5 citation statements)

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“…EHEC O157:H7 TUV93-0 derived from strain EDL933 was used ( 67 ). The isogenic mutant Δ fliC and Δ motA strains were obtained as described previously ( 7 ). All strains were grown in lysogeny broth (LB) medium (1% [wt/vol] tryptone, 0.5% yeast extract, and 0.5% NaCl) overnight at 37°C and 100 rpm.…”

Section: Methodsmentioning

confidence: 99%

“…The persistence in their hosts, including humans, occurs through adhesion to tissues ( 4 ). EHEC adhere to the intestinal mucosa in a manner termed the attaching-and-effacing effect ( 5 ), but other mechanisms, involving flagella and pili, have been described but not fully characterized ( 6 , 7 ). The pili are the most described adhesins present at the bacterial surface ( 8 , 9 ).…”

Section: Introductionmentioning

confidence: 99%

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The Impact of Plasma Membrane Lipid Composition on Flagellum-Mediated Adhesion of Enterohemorrhagic Escherichia coli

Cazzola

Lemaire

Acket

et al. 2020

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Enterohemorrhagic Escherichia coli (EHEC) O157:H7 is a major cause of foodborne gastrointestinal illness. The adhesion of EHEC to host tissues is the first step enabling bacterial colonization. Adhesins such as fimbriae and flagella mediate this process. Here, we studied the interaction of the bacterial flagellum with the host cell’s plasma membrane using giant unilamellar vesicles (GUVs) as a biologically relevant model. Cultured cell lines contain many different molecular components, including proteins and glycoproteins. In contrast, with GUVs, we can characterize the bacterial mode of interaction solely with a defined lipid part of the cell membrane. Bacterial adhesion on GUVs was dependent on the presence of the flagellar filament and its motility. By testing different phospholipid head groups, the nature of the fatty acid chains, or the liposome curvature, we found that lipid packing is a key parameter to enable bacterial adhesion. Using HT-29 cells grown in the presence of polyunsaturated fatty acid (α-linolenic acid) or saturated fatty acid (palmitic acid), we found that α-linolenic acid reduced adhesion of wild-type EHEC but not of a nonflagellated mutant. Finally, our results reveal that the presence of flagella is advantageous for the bacteria to bind to lipid rafts. We speculate that polyunsaturated fatty acids prevent flagellar adhesion on membrane bilayers and play a clear role for optimal host colonization. Flagellum-mediated adhesion to plasma membranes has broad implications for host-pathogen interactions. IMPORTANCE Bacterial adhesion is a crucial step to allow bacteria to colonize their hosts, invade tissues, and form biofilm. Enterohemorrhagic Escherichia coli O157:H7 is a human pathogen and the causative agent of diarrhea and hemorrhagic colitis. Here, we use biomimetic membrane models and cell lines to decipher the impact of lipid content of the plasma membrane on enterohemorrhagic E. coli flagellum-mediated adhesion. Our findings provide evidence that polyunsaturated fatty acid (α-linolenic acid) inhibits E. coli flagellar adhesion to the plasma membrane in a mechanism separate from its antimicrobial and anti-inflammatory functions. In addition, we confirm that cholesterol-enriched lipid microdomains, often called lipid rafts, are important in bacterial adhesion. These findings demonstrate that plasma membrane adhesion via bacterial flagella play a significant role for an important human pathogen. This mechanism represents a promising target for the development of novel antiadhesion therapies.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The Impact of Plasma Membrane Lipid Composition on Flagellum-Mediated Adhesion of Enterohemorrhagic Escherichia coli

Cazzola

Lemaire

Acket

et al. 2020

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“…Bacteria growth and preparation. EHEC O157:H7 TUV93-0 derived from strain EDL933 was used (60).All The isogenic mutants ∆fliC and ∆motA were obtained as described (61). All strains were grown in lysogeny broth (LB) medium (1% w/v tryptone, 0.5% yeast extract and 0.5% NaCl) overnight at 37°C and 100 rpm.…”

Section: Methodsmentioning

confidence: 99%

The impact of plasma membrane lipid composition on flagella-mediated adhesion of enterohemorrhagicEscherichia coli

Cazzola

Lemaire

Acket

et al. 2020

Preprint

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AbstractEnterohemorrhagic Escherichia coli (EHEC) O157:H7 is a major cause of foodborne gastrointestinal illness. The adhesion of EHEC on host tissues is the first step enabling bacterial colonization. Adhesins like fimbriae and flagella mediate this mechanism. Here, we studied the interaction of the bacterial flagellum with the host cell’s plasma membrane using Giant Unilamellar Vesicles (GUVs) as a biologically relevant model. Cultured cell lines contain many different molecular components including proteins and glycoproteins. In contrast, with GUVs we can characterize the bacterial mode of interaction solely with a defined lipid part of the cell membrane. Bacterial adhesion on GUVs was dependent on the presence of the flagellar filament and its motility. By testing different phospholipid head groups, the nature of the fatty acid chains or the liposome curvature, we found that lipid packing is a key parameter to enable bacterial adhesion. Using HT-29 cells grown in the presence of polyunsaturated fatty acid (α-linolenic acid) or saturated fatty acid (palmitic acid), we found that α-linolenic acid reduced adhesion of wild type EHEC but not of a non-flagellated mutant. Finally, our results reveal that the presence of flagella is advantageous for the bacteria to bind to lipid rafts. We speculate that polyunsaturated fatty acids prevent flagellar adhesion on membrane bilayers and play a clear role for optimal host colonization. Flagella-mediated adhesion to plasma membranes has broad implications to host-pathogen interactions.ImportanceBacterial adhesion is a crucial step to allow bacteria to colonize their hosts, invade tissues and form biofilm. Enterohemorrhagic E. coli O157:H7 is a human pathogen and the causative agent of diarrhea and hemorrhagic colitis. Here, we use biomimetic membrane models and cell lines to decipher the impact of lipid content of the plasma membrane on enterohemorrhagic E. coli flagella-mediated adhesion. Our findings provide evidence that polyunsaturated fatty acid (α-linolenic acid) inhibits E. coli flagella adhesion to the plasma membrane in a mechanism separate from its antimicrobial and anti-inflammatory functions. In addition, we confirm that cholesterol-enriched lipid microdomains, often called lipid rafts are important in bacterial adhesion. These findings significantly strengthen plasma membrane adhesion via bacterial flagella in an important human pathogen. This mechanism represents a promising target for the development of novel anti-adhesion therapies.

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“…Flagellar lysine methylation, which increases the hydrophobicity of the flagellin, can further promote host attachment (Horstmann et al, 2020). Some flagellated pathogens, like S. enterica and E. coli , may use their flagella to mechanically disrupt the host membrane and actin cytoskeleton (Wolfson et al, 2020). In contrast, other bacteria, like Yersinia , downregulate flagella at host temperatures and instead induce the expression of the injectisome (Hoe and Goguen, 1993; Michiels et al, 1991; de Rouvroit et al, 1992; Skurnik et al, 1984).…”

Section: Reacting To External Conditions and Requirementsmentioning

confidence: 99%

Adaptivity and dynamics in type III secretion systems

Milne-Davies

Wimmi

Diepold

2020

Molecular Microbiology

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The type III secretion system is the common core of two bacterial molecular machines: the flagellum and the injectisome. The flagellum is the most widely distributed prokaryotic locomotion device, whereas the injectisome is a syringe‐like apparatus for inter‐kingdom protein translocation, which is essential for virulence in important human pathogens. The successful concept of the type III secretion system has been modified for different bacterial needs. It can be adapted to changing conditions, and was found to be a dynamic complex constantly exchanging components. In this review, we highlight the flexibility, adaptivity, and dynamic nature of the type III secretion system.

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Bacterial flagella disrupt host cell membranes and interact with cytoskeletal components

Cited by 4 publications

References 75 publications

The Impact of Plasma Membrane Lipid Composition on Flagellum-Mediated Adhesion of Enterohemorrhagic Escherichia coli

The Impact of Plasma Membrane Lipid Composition on Flagellum-Mediated Adhesion of Enterohemorrhagic Escherichia coli

The impact of plasma membrane lipid composition on flagella-mediated adhesion of enterohemorrhagicEscherichia coli

Adaptivity and dynamics in type III secretion systems

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