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...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Miguel Ángel Robles-Ramos, William Margolin, Marta Sobrinos-Sanguino, Carlos Alfonso, Germán Rivas, Begoña Monterroso, Silvia Zorrilla
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	E. coli FtsZ SlmA fluorescence microscopy lipid membranes membrane binding Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/1ad526da53d244e29f5949ef4bc4e51a
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:1ad526da53d244e29f5949ef4bc4e51a
record_format	dspace
spelling	oai:doaj.org-article:1ad526da53d244e29f5949ef4bc4e51a2021-11-15T16:19:08ZThe Nucleoid Occlusion Protein SlmA Binds to Lipid Membranes10.1128/mBio.02094-202150-7511https://doaj.org/article/1ad526da53d244e29f5949ef4bc4e51a2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02094-20https://doaj.org/toc/2150-7511ABSTRACT 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.Miguel Ángel Robles-RamosWilliam MargolinMarta Sobrinos-SanguinoCarlos AlfonsoGermán RivasBegoña MonterrosoSilvia ZorrillaAmerican Society for MicrobiologyarticleE. coliFtsZSlmAfluorescence microscopylipid membranesmembrane bindingMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	E. coli FtsZ SlmA fluorescence microscopy lipid membranes membrane binding Microbiology QR1-502
spellingShingle	E. coli FtsZ SlmA fluorescence microscopy lipid membranes membrane binding Microbiology QR1-502 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
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.
format	article
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
title	The Nucleoid Occlusion Protein SlmA Binds to Lipid Membranes
title_short	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_sort	nucleoid occlusion protein slma binds to lipid membranes
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/1ad526da53d244e29f5949ef4bc4e51a
work_keys_str_mv	AT miguelangelroblesramos thenucleoidocclusionproteinslmabindstolipidmembranes AT williammargolin thenucleoidocclusionproteinslmabindstolipidmembranes AT martasobrinossanguino thenucleoidocclusionproteinslmabindstolipidmembranes AT carlosalfonso thenucleoidocclusionproteinslmabindstolipidmembranes AT germanrivas thenucleoidocclusionproteinslmabindstolipidmembranes AT begonamonterroso thenucleoidocclusionproteinslmabindstolipidmembranes AT silviazorrilla thenucleoidocclusionproteinslmabindstolipidmembranes AT miguelangelroblesramos nucleoidocclusionproteinslmabindstolipidmembranes AT williammargolin nucleoidocclusionproteinslmabindstolipidmembranes AT martasobrinossanguino nucleoidocclusionproteinslmabindstolipidmembranes AT carlosalfonso nucleoidocclusionproteinslmabindstolipidmembranes AT germanrivas nucleoidocclusionproteinslmabindstolipidmembranes AT begonamonterroso nucleoidocclusionproteinslmabindstolipidmembranes AT silviazorrilla nucleoidocclusionproteinslmabindstolipidmembranes
_version_	1718426951089127424

The Nucleoid Occlusion Protein SlmA Binds to Lipid Membranes

Ejemplares similares