The Impact of Plasma Membrane Lipid Composition on Flagellum-Mediated Adhesion of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content>
ABSTRACT 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...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2020-10-01
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| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSphere.00702-20 |
| _version_ | 1819005601598930944 |
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| author | Hélène Cazzola Laurine Lemaire Sébastien Acket Elise Prost Luminita Duma Marc Erhardt Petra Čechová Patrick Trouillas Fady Mohareb Claire Rossi Yannick Rossez |
| author_facet | Hélène Cazzola Laurine Lemaire Sébastien Acket Elise Prost Luminita Duma Marc Erhardt Petra Čechová Patrick Trouillas Fady Mohareb Claire Rossi Yannick Rossez |
| author_sort | Hélène Cazzola |
| collection | DOAJ |
| description | ABSTRACT 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. |
| first_indexed | 2024-12-20T23:55:23Z |
| format | Article |
| id | doaj.art-aacf7a96bbcc4d109dd691887f0f6cbb |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-12-20T23:55:23Z |
| publishDate | 2020-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-aacf7a96bbcc4d109dd691887f0f6cbb2022-12-21T19:22:44ZengAmerican Society for MicrobiologymSphere2379-50422020-10-015510.1128/mSphere.00702-20The Impact of Plasma Membrane Lipid Composition on Flagellum-Mediated Adhesion of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content>Hélène Cazzola0Laurine Lemaire1Sébastien Acket2Elise Prost3Luminita Duma4Marc Erhardt5Petra Čechová6Patrick Trouillas7Fady Mohareb8Claire Rossi9Yannick Rossez10Université de Technologie de Compiègne, UPJV, UMR CNRS 7025, Enzyme and Cell Engineering, Centre de recherche Royallieu, Compiègne, FranceUniversité de Technologie de Compiègne, UPJV, UMR CNRS 7025, Enzyme and Cell Engineering, Centre de recherche Royallieu, Compiègne, FranceUniversité de Technologie de Compiègne, UPJV, UMR CNRS 7025, Enzyme and Cell Engineering, Centre de recherche Royallieu, Compiègne, FranceUniversité de Technologie de Compiègne, UPJV, UMR CNRS 7025, Enzyme and Cell Engineering, Centre de recherche Royallieu, Compiègne, FranceUniversité de Technologie de Compiègne, UPJV, UMR CNRS 7025, Enzyme and Cell Engineering, Centre de recherche Royallieu, Compiègne, FranceInstitute for Biology–Bacterial Physiology, Humboldt—Universität zu Berlin, Berlin, GermanyRCPTM, Palacký University Olomouc, Olomouc, Czech RepublicRCPTM, Palacký University Olomouc, Olomouc, Czech RepublicThe Bioinformatics Group, School of Water, Energy and Environment, Cranfield University, Cranfield, United KingdomUniversité de Technologie de Compiègne, UPJV, UMR CNRS 7025, Enzyme and Cell Engineering, Centre de recherche Royallieu, Compiègne, FranceUniversité de Technologie de Compiègne, UPJV, UMR CNRS 7025, Enzyme and Cell Engineering, Centre de recherche Royallieu, Compiègne, FranceABSTRACT 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.https://journals.asm.org/doi/10.1128/mSphere.00702-20adhesinsflagellalipid raftsphospholipids |
| spellingShingle | Hélène Cazzola Laurine Lemaire Sébastien Acket Elise Prost Luminita Duma Marc Erhardt Petra Čechová Patrick Trouillas Fady Mohareb Claire Rossi Yannick Rossez The Impact of Plasma Membrane Lipid Composition on Flagellum-Mediated Adhesion of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> mSphere adhesins flagella lipid rafts phospholipids |
| title | The Impact of Plasma Membrane Lipid Composition on Flagellum-Mediated Adhesion of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> |
| title_full | The Impact of Plasma Membrane Lipid Composition on Flagellum-Mediated Adhesion of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> |
| title_fullStr | The Impact of Plasma Membrane Lipid Composition on Flagellum-Mediated Adhesion of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> |
| title_full_unstemmed | The Impact of Plasma Membrane Lipid Composition on Flagellum-Mediated Adhesion of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> |
| title_short | The Impact of Plasma Membrane Lipid Composition on Flagellum-Mediated Adhesion of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> |
| title_sort | impact of plasma membrane lipid composition on flagellum mediated adhesion of enterohemorrhagic named content content type genus species escherichia coli named content |
| topic | adhesins flagella lipid rafts phospholipids |
| url | https://journals.asm.org/doi/10.1128/mSphere.00702-20 |
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