The Nucleoid Occlusion Protein SlmA Binds to Lipid Membranes
ABSTRACT Protection of the chromosome from scission by the division machinery during cytokinesis is critical for bacterial survival and fitness. This is achieved by nucleoid occlusion, which, in conjunction with other mechanisms, ensures formation of the division ring at midcell. In Escherichia coli...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2020-10-01
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| Series: | mBio |
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| Online Access: | https://journals.asm.org/doi/10.1128/mBio.02094-20 |
| _version_ | 1818434409251995648 |
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| author | Miguel Ángel Robles-Ramos William Margolin Marta Sobrinos-Sanguino Carlos Alfonso Germán Rivas Begoña Monterroso Silvia Zorrilla |
| author_facet | Miguel Ángel Robles-Ramos William Margolin Marta Sobrinos-Sanguino Carlos Alfonso Germán Rivas Begoña Monterroso Silvia Zorrilla |
| author_sort | Miguel Ángel Robles-Ramos |
| collection | DOAJ |
| description | ABSTRACT Protection of the chromosome from scission by the division machinery during cytokinesis is critical for bacterial survival and fitness. This is achieved by nucleoid occlusion, which, in conjunction with other mechanisms, ensures formation of the division ring at midcell. In Escherichia coli, this mechanism is mediated by SlmA, a specific DNA binding protein that antagonizes assembly of the central division protein FtsZ into a productive ring in the vicinity of the chromosome. Here, we provide evidence supporting direct interaction of SlmA with lipid membranes, tuned by its binding partners FtsZ and SlmA binding sites (SBS) on chromosomal DNA. Reconstructions in minimal membrane systems that mimic cellular environments show that SlmA binds to lipid-coated microbeads or locates at the edge of microfluidic-generated microdroplets, inside which the protein is encapsulated. DNA fragments containing SBS sequences do not seem to be recruited to the membrane by SlmA but instead compete with SlmA’s ability to bind lipids. The interaction of SlmA with FtsZ modulates this behavior, ultimately triggering membrane localization of the SBS sequences alongside the two proteins. The ability of SlmA to bind lipids uncovered in this work extends the interaction network of this multivalent regulator beyond its well-known protein and nucleic acid recognition, which may have implications in the overall spatiotemporal control of division ring assembly. IMPORTANCE Successful bacterial proliferation relies on the spatial and temporal precision of cytokinesis and its regulation by systems that protect the integrity of the nucleoid. In Escherichia coli, one of these protectors is SlmA protein, which binds to specific DNA sites around the nucleoid and helps to shield the nucleoid from inappropriate bisection by the cell division septum. Here, we discovered that SlmA not only interacts with the nucleoid and septum-associated cell division proteins but also binds directly to cytomimetic lipid membranes, adding a novel putative mechanism for regulating the local activity of these cell division proteins. We find that interaction between SlmA and lipid membranes is regulated by SlmA’s DNA binding sites and protein binding partners as well as chemical conditions, suggesting that the SlmA-membrane interactions are important for fine-tuning the regulation of nucleoid integrity during cytokinesis. |
| first_indexed | 2024-12-14T16:36:32Z |
| format | Article |
| id | doaj.art-1ad526da53d244e29f5949ef4bc4e51a |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-14T16:36:32Z |
| publishDate | 2020-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-1ad526da53d244e29f5949ef4bc4e51a2022-12-21T22:54:26ZengAmerican Society for MicrobiologymBio2150-75112020-10-0111510.1128/mBio.02094-20The Nucleoid Occlusion Protein SlmA Binds to Lipid MembranesMiguel Ángel Robles-Ramos0William Margolin1Marta Sobrinos-Sanguino2Carlos Alfonso3Germán Rivas4Begoña Monterroso5Silvia Zorrilla6Centro de Investigaciones Biológicas Margarita Salas, Consejo Superior de Investigaciones Científicas (CSIC), Madrid, SpainDepartment of Microbiology and Molecular Genetics, McGovern Medical School, University of Texas, Houston, Texas, USACentro de Investigaciones Biológicas Margarita Salas, Consejo Superior de Investigaciones Científicas (CSIC), Madrid, SpainCentro de Investigaciones Biológicas Margarita Salas, Consejo Superior de Investigaciones Científicas (CSIC), Madrid, SpainCentro de Investigaciones Biológicas Margarita Salas, Consejo Superior de Investigaciones Científicas (CSIC), Madrid, SpainCentro de Investigaciones Biológicas Margarita Salas, Consejo Superior de Investigaciones Científicas (CSIC), Madrid, SpainCentro de Investigaciones Biológicas Margarita Salas, Consejo Superior de Investigaciones Científicas (CSIC), Madrid, SpainABSTRACT Protection of the chromosome from scission by the division machinery during cytokinesis is critical for bacterial survival and fitness. This is achieved by nucleoid occlusion, which, in conjunction with other mechanisms, ensures formation of the division ring at midcell. In Escherichia coli, this mechanism is mediated by SlmA, a specific DNA binding protein that antagonizes assembly of the central division protein FtsZ into a productive ring in the vicinity of the chromosome. Here, we provide evidence supporting direct interaction of SlmA with lipid membranes, tuned by its binding partners FtsZ and SlmA binding sites (SBS) on chromosomal DNA. Reconstructions in minimal membrane systems that mimic cellular environments show that SlmA binds to lipid-coated microbeads or locates at the edge of microfluidic-generated microdroplets, inside which the protein is encapsulated. DNA fragments containing SBS sequences do not seem to be recruited to the membrane by SlmA but instead compete with SlmA’s ability to bind lipids. The interaction of SlmA with FtsZ modulates this behavior, ultimately triggering membrane localization of the SBS sequences alongside the two proteins. The ability of SlmA to bind lipids uncovered in this work extends the interaction network of this multivalent regulator beyond its well-known protein and nucleic acid recognition, which may have implications in the overall spatiotemporal control of division ring assembly. IMPORTANCE Successful bacterial proliferation relies on the spatial and temporal precision of cytokinesis and its regulation by systems that protect the integrity of the nucleoid. In Escherichia coli, one of these protectors is SlmA protein, which binds to specific DNA sites around the nucleoid and helps to shield the nucleoid from inappropriate bisection by the cell division septum. Here, we discovered that SlmA not only interacts with the nucleoid and septum-associated cell division proteins but also binds directly to cytomimetic lipid membranes, adding a novel putative mechanism for regulating the local activity of these cell division proteins. We find that interaction between SlmA and lipid membranes is regulated by SlmA’s DNA binding sites and protein binding partners as well as chemical conditions, suggesting that the SlmA-membrane interactions are important for fine-tuning the regulation of nucleoid integrity during cytokinesis.https://journals.asm.org/doi/10.1128/mBio.02094-20E. coliFtsZSlmAfluorescence microscopylipid membranesmembrane binding |
| spellingShingle | Miguel Ángel Robles-Ramos William Margolin Marta Sobrinos-Sanguino Carlos Alfonso Germán Rivas Begoña Monterroso Silvia Zorrilla The Nucleoid Occlusion Protein SlmA Binds to Lipid Membranes mBio E. coli FtsZ SlmA fluorescence microscopy lipid membranes membrane binding |
| title | The Nucleoid Occlusion Protein SlmA Binds to Lipid Membranes |
| title_full | The Nucleoid Occlusion Protein SlmA Binds to Lipid Membranes |
| title_fullStr | The Nucleoid Occlusion Protein SlmA Binds to Lipid Membranes |
| title_full_unstemmed | The Nucleoid Occlusion Protein SlmA Binds to Lipid Membranes |
| title_short | The Nucleoid Occlusion Protein SlmA Binds to Lipid Membranes |
| title_sort | nucleoid occlusion protein slma binds to lipid membranes |
| topic | E. coli FtsZ SlmA fluorescence microscopy lipid membranes membrane binding |
| url | https://journals.asm.org/doi/10.1128/mBio.02094-20 |
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