The Bacterial DNA Binding Protein MatP Involved in Linking the Nucleoid Terminal Domain to the Divisome at Midcell Interacts with Lipid Membranes
ABSTRACT Division ring formation at midcell is controlled by various mechanisms in Escherichia coli, one of them being the linkage between the chromosomal Ter macrodomain and the Z-ring mediated by MatP, a DNA binding protein that organizes this macrodomain and contributes to the prevention of prema...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2019-06-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.00376-19 |
| _version_ | 1818997494086893568 |
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| author | Begoña Monterroso Silvia Zorrilla Marta Sobrinos-Sanguino Miguel Ángel Robles-Ramos Carlos Alfonso Bill Söderström Nils Y. Meiresonne Jolanda Verheul Tanneke den Blaauwen Germán Rivas |
| author_facet | Begoña Monterroso Silvia Zorrilla Marta Sobrinos-Sanguino Miguel Ángel Robles-Ramos Carlos Alfonso Bill Söderström Nils Y. Meiresonne Jolanda Verheul Tanneke den Blaauwen Germán Rivas |
| author_sort | Begoña Monterroso |
| collection | DOAJ |
| description | ABSTRACT Division ring formation at midcell is controlled by various mechanisms in Escherichia coli, one of them being the linkage between the chromosomal Ter macrodomain and the Z-ring mediated by MatP, a DNA binding protein that organizes this macrodomain and contributes to the prevention of premature chromosome segregation. Here we show that, during cell division, just before splitting the daughter cells, MatP seems to localize close to the cytoplasmic membrane, suggesting that this protein might interact with lipids. To test this hypothesis, we investigated MatP interaction with lipids in vitro. We found that, when encapsulated inside vesicles and microdroplets generated by microfluidics, MatP accumulates at phospholipid bilayers and monolayers matching the lipid composition in the E. coli inner membrane. MatP binding to lipids was independently confirmed using lipid-coated microbeads and biolayer interferometry assays, which suggested that the recognition is mainly hydrophobic. Interaction of MatP with the lipid membranes also occurs in the presence of the DNA sequences specifically targeted by the protein, but there is no evidence of ternary membrane/protein/DNA complexes. We propose that the association of MatP with lipids may modulate its spatiotemporal localization and its recognition of other ligands. IMPORTANCE The division of an E. coli cell into two daughter cells with equal genomic information and similar size requires duplication and segregation of the chromosome and subsequent scission of the envelope by a protein ring, the Z-ring. MatP is a DNA binding protein that contributes both to the positioning of the Z-ring at midcell and the temporal control of nucleoid segregation. Our integrated in vivo and in vitro analysis provides evidence that MatP can interact with lipid membranes reproducing the phospholipid mixture in the E. coli inner membrane, without concomitant recruitment of the short DNA sequences specifically targeted by MatP. This observation strongly suggests that the membrane may play a role in the regulation of the function and localization of MatP, which could be relevant for the coordination of the two fundamental processes in which this protein participates, nucleoid segregation and cell division. |
| first_indexed | 2024-12-20T21:46:31Z |
| format | Article |
| id | doaj.art-17924910d19642edb417b06562cd1cc4 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-20T21:46:31Z |
| publishDate | 2019-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-17924910d19642edb417b06562cd1cc42022-12-21T19:25:40ZengAmerican Society for MicrobiologymBio2150-75112019-06-0110310.1128/mBio.00376-19The Bacterial DNA Binding Protein MatP Involved in Linking the Nucleoid Terminal Domain to the Divisome at Midcell Interacts with Lipid MembranesBegoña Monterroso0Silvia Zorrilla1Marta Sobrinos-Sanguino2Miguel Ángel Robles-Ramos3Carlos Alfonso4Bill Söderström5Nils Y. Meiresonne6Jolanda Verheul7Tanneke den Blaauwen8Germán Rivas9Centro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas (CSIC), Madrid, SpainCentro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas (CSIC), Madrid, SpainCentro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas (CSIC), Madrid, SpainCentro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas (CSIC), Madrid, SpainCentro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas (CSIC), Madrid, SpainStructural Cellular Biology Unit, Okinawa Institute of Science and Technology, Okinawa, JapanBacterial Cell Biology & Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, the NetherlandsBacterial Cell Biology & Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, the NetherlandsBacterial Cell Biology & Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, the NetherlandsCentro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas (CSIC), Madrid, SpainABSTRACT Division ring formation at midcell is controlled by various mechanisms in Escherichia coli, one of them being the linkage between the chromosomal Ter macrodomain and the Z-ring mediated by MatP, a DNA binding protein that organizes this macrodomain and contributes to the prevention of premature chromosome segregation. Here we show that, during cell division, just before splitting the daughter cells, MatP seems to localize close to the cytoplasmic membrane, suggesting that this protein might interact with lipids. To test this hypothesis, we investigated MatP interaction with lipids in vitro. We found that, when encapsulated inside vesicles and microdroplets generated by microfluidics, MatP accumulates at phospholipid bilayers and monolayers matching the lipid composition in the E. coli inner membrane. MatP binding to lipids was independently confirmed using lipid-coated microbeads and biolayer interferometry assays, which suggested that the recognition is mainly hydrophobic. Interaction of MatP with the lipid membranes also occurs in the presence of the DNA sequences specifically targeted by the protein, but there is no evidence of ternary membrane/protein/DNA complexes. We propose that the association of MatP with lipids may modulate its spatiotemporal localization and its recognition of other ligands. IMPORTANCE The division of an E. coli cell into two daughter cells with equal genomic information and similar size requires duplication and segregation of the chromosome and subsequent scission of the envelope by a protein ring, the Z-ring. MatP is a DNA binding protein that contributes both to the positioning of the Z-ring at midcell and the temporal control of nucleoid segregation. Our integrated in vivo and in vitro analysis provides evidence that MatP can interact with lipid membranes reproducing the phospholipid mixture in the E. coli inner membrane, without concomitant recruitment of the short DNA sequences specifically targeted by MatP. This observation strongly suggests that the membrane may play a role in the regulation of the function and localization of MatP, which could be relevant for the coordination of the two fundamental processes in which this protein participates, nucleoid segregation and cell division.https://journals.asm.org/doi/10.1128/mBio.00376-19DNA binding proteinsbacterial divisionbiochemical reconstructiondivision site selectionprotein-membrane interaction |
| spellingShingle | Begoña Monterroso Silvia Zorrilla Marta Sobrinos-Sanguino Miguel Ángel Robles-Ramos Carlos Alfonso Bill Söderström Nils Y. Meiresonne Jolanda Verheul Tanneke den Blaauwen Germán Rivas The Bacterial DNA Binding Protein MatP Involved in Linking the Nucleoid Terminal Domain to the Divisome at Midcell Interacts with Lipid Membranes mBio DNA binding proteins bacterial division biochemical reconstruction division site selection protein-membrane interaction |
| title | The Bacterial DNA Binding Protein MatP Involved in Linking the Nucleoid Terminal Domain to the Divisome at Midcell Interacts with Lipid Membranes |
| title_full | The Bacterial DNA Binding Protein MatP Involved in Linking the Nucleoid Terminal Domain to the Divisome at Midcell Interacts with Lipid Membranes |
| title_fullStr | The Bacterial DNA Binding Protein MatP Involved in Linking the Nucleoid Terminal Domain to the Divisome at Midcell Interacts with Lipid Membranes |
| title_full_unstemmed | The Bacterial DNA Binding Protein MatP Involved in Linking the Nucleoid Terminal Domain to the Divisome at Midcell Interacts with Lipid Membranes |
| title_short | The Bacterial DNA Binding Protein MatP Involved in Linking the Nucleoid Terminal Domain to the Divisome at Midcell Interacts with Lipid Membranes |
| title_sort | bacterial dna binding protein matp involved in linking the nucleoid terminal domain to the divisome at midcell interacts with lipid membranes |
| topic | DNA binding proteins bacterial division biochemical reconstruction division site selection protein-membrane interaction |
| url | https://journals.asm.org/doi/10.1128/mBio.00376-19 |
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