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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Autores principales:	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
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	DNA binding proteins bacterial division biochemical reconstruction division site selection protein-membrane interaction Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/17924910d19642edb417b06562cd1cc4
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spelling	oai:doaj.org-article:17924910d19642edb417b06562cd1cc42021-11-15T15:55:25ZThe Bacterial DNA Binding Protein MatP Involved in Linking the Nucleoid Terminal Domain to the Divisome at Midcell Interacts with Lipid Membranes10.1128/mBio.00376-192150-7511https://doaj.org/article/17924910d19642edb417b06562cd1cc42019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00376-19https://doaj.org/toc/2150-7511ABSTRACT 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.Begoña MonterrosoSilvia ZorrillaMarta Sobrinos-SanguinoMiguel Ángel Robles-RamosCarlos AlfonsoBill SöderströmNils Y. MeiresonneJolanda VerheulTanneke den BlaauwenGermán RivasAmerican Society for MicrobiologyarticleDNA binding proteinsbacterial divisionbiochemical reconstructiondivision site selectionprotein-membrane interactionMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	DNA binding proteins bacterial division biochemical reconstruction division site selection protein-membrane interaction Microbiology QR1-502
spellingShingle	DNA binding proteins bacterial division biochemical reconstruction division site selection protein-membrane interaction Microbiology QR1-502 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
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.
format	article
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
title	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_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_sort	bacterial dna binding protein matp involved in linking the nucleoid terminal domain to the divisome at midcell interacts with lipid membranes
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/17924910d19642edb417b06562cd1cc4
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The Bacterial DNA Binding Protein MatP Involved in Linking the Nucleoid Terminal Domain to the Divisome at Midcell Interacts with Lipid Membranes

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