Control of septum thickness by the curvature of sepf polymers

Michaela Wenzel; Ilkay N. Celik Gulsoy; Yongqiang Gao; Zihao Teng; Joost Willemse; Martijn Middelkamp; Mariska G.M. van Rosmalen; Per W.B. Larsen; Nicole N. van der Wel; Gijs J.L. Wuite; Wouter H. Roos; Leendert W. Hamoen

doi:10.1073/pnas.2002635118

Control of septum thickness by the curvature of sepf polymers

Michaela Wenzel, Ilkay N. Celik Gulsoy, Yongqiang Gao, Zihao Teng, Joost Willemse, Martijn Middelkamp, Mariska G.M. van Rosmalen, Per W.B. Larsen, Nicole N. van der Wel, Gijs J.L. Wuite, Wouter H. Roos, Leendert W. Hamoen^*

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

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Abstract

Gram-positive bacteria divide by forming a thick cross wall. How the thickness of this septal wall is controlled is unknown. In this type of bacteria, the key cell division protein FtsZ is anchored to the cell membrane by two proteins, FtsA and/or SepF. We have isolated SepF homologs from different bacterial species and found that they all polymerize into large protein rings with diameters varying from 19 to 44 nm. Interestingly, these values correlated well with the thickness of their septa. To test whether ring diameter determines septal thickness, we tried to construct different SepF chimeras with the purpose to manipulate the diameter of the SepF protein ring. This was indeed possible and confirmed that the conserved core domain of SepF regulates ring diameter. Importantly, when SepF chimeras with different diameters were expressed in the bacterial host Bacillus subtilis, the thickness of its septa changed accordingly. These results strongly support a model in which septal thickness is controlled by curved molecular clamps formed by SepF polymers attached to the leading edge of nascent septa. This also implies that the intrinsic shape of a protein polymer can function as a mold to shape the cell wall.

Original language	English
Article number	e2002635118
Pages (from-to)	1-9
Number of pages	9
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	118
Issue number	2
Early online date	21 Dec 2020
DOIs	https://doi.org/10.1073/pnas.2002635118
Publication status	Published - 12 Jan 2021

Funding

ACKNOWLEDGMENTS. We thank Zehui Zhang and Daniel Antwi-berko for help with sample preparation, Wiep Klaas Smits for help with growing strains, Marien P. Dekker and Jan R. T. van Weering for support with TEM, Sourav Maity for help with HS-AFM, and Gaurav Dugar for critically reading the manuscript. Electron microscopy was performed at the electron micro-sopy facility of the Free University Amsterdam and Free University Medical Center, supported by the Netherlands Organization for Scientific Research (NWO, middelgroot 91111009), and the Electron Microscopy Center Amsterdam. This work was financially supported by NWO STW-Vici 12128 (to L.W.H.) and NWO-Vidi and NWO Excellent Chemisch Onderzoek (ECHO) (W.H.R.). Y.G. and Z.T. were supported by PhD fellowships from the China Scholarship Council, and M.W. was supported by a postdoc stipend from the Amsterdam Infection and Immunity Institute.

Funders	Funder number
China Scholarship Council
Amsterdam Infection and Immunity Institute
NWO-VIDI
Nederlandse Organisatie voor Wetenschappelijk Onderzoek	STW-Vici 12128, 91111009, 12128

Keywords

Bacillus subtilis
Cell division
FtsZ
SepF

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10.1073/pnas.2002635118

Control of septum thickness by the curvature of sepf polymersFinal published version, 1.79 MBLicence: Article 25fa Dutch Copyright Act

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Wenzel, M., Celik Gulsoy, I. N., Gao, Y., Teng, Z., Willemse, J., Middelkamp, M., van Rosmalen, M. G. M., Larsen, P. W. B., van der Wel, N. N., Wuite, G. J. L., Roos, W. H., & Hamoen, L. W. (2021). Control of septum thickness by the curvature of sepf polymers. Proceedings of the National Academy of Sciences of the United States of America, 118(2), 1-9. Article e2002635118. https://doi.org/10.1073/pnas.2002635118

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title = "Control of septum thickness by the curvature of sepf polymers",

abstract = "Gram-positive bacteria divide by forming a thick cross wall. How the thickness of this septal wall is controlled is unknown. In this type of bacteria, the key cell division protein FtsZ is anchored to the cell membrane by two proteins, FtsA and/or SepF. We have isolated SepF homologs from different bacterial species and found that they all polymerize into large protein rings with diameters varying from 19 to 44 nm. Interestingly, these values correlated well with the thickness of their septa. To test whether ring diameter determines septal thickness, we tried to construct different SepF chimeras with the purpose to manipulate the diameter of the SepF protein ring. This was indeed possible and confirmed that the conserved core domain of SepF regulates ring diameter. Importantly, when SepF chimeras with different diameters were expressed in the bacterial host Bacillus subtilis, the thickness of its septa changed accordingly. These results strongly support a model in which septal thickness is controlled by curved molecular clamps formed by SepF polymers attached to the leading edge of nascent septa. This also implies that the intrinsic shape of a protein polymer can function as a mold to shape the cell wall.",

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author = "Michaela Wenzel and {Celik Gulsoy}, {Ilkay N.} and Yongqiang Gao and Zihao Teng and Joost Willemse and Martijn Middelkamp and {van Rosmalen}, {Mariska G.M.} and Larsen, {Per W.B.} and {van der Wel}, {Nicole N.} and Wuite, {Gijs J.L.} and Roos, {Wouter H.} and Hamoen, {Leendert W.}",

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Wenzel, M, Celik Gulsoy, IN, Gao, Y, Teng, Z, Willemse, J, Middelkamp, M, van Rosmalen, MGM, Larsen, PWB, van der Wel, NN, Wuite, GJL, Roos, WH & Hamoen, LW 2021, 'Control of septum thickness by the curvature of sepf polymers', Proceedings of the National Academy of Sciences of the United States of America, vol. 118, no. 2, e2002635118, pp. 1-9. https://doi.org/10.1073/pnas.2002635118

TY - JOUR

T1 - Control of septum thickness by the curvature of sepf polymers

AU - Wenzel, Michaela

AU - Celik Gulsoy, Ilkay N.

AU - Gao, Yongqiang

AU - Teng, Zihao

AU - Willemse, Joost

AU - Middelkamp, Martijn

AU - van Rosmalen, Mariska G.M.

AU - Larsen, Per W.B.

AU - van der Wel, Nicole N.

AU - Wuite, Gijs J.L.

AU - Roos, Wouter H.

AU - Hamoen, Leendert W.

PY - 2021/1/12

Y1 - 2021/1/12

N2 - Gram-positive bacteria divide by forming a thick cross wall. How the thickness of this septal wall is controlled is unknown. In this type of bacteria, the key cell division protein FtsZ is anchored to the cell membrane by two proteins, FtsA and/or SepF. We have isolated SepF homologs from different bacterial species and found that they all polymerize into large protein rings with diameters varying from 19 to 44 nm. Interestingly, these values correlated well with the thickness of their septa. To test whether ring diameter determines septal thickness, we tried to construct different SepF chimeras with the purpose to manipulate the diameter of the SepF protein ring. This was indeed possible and confirmed that the conserved core domain of SepF regulates ring diameter. Importantly, when SepF chimeras with different diameters were expressed in the bacterial host Bacillus subtilis, the thickness of its septa changed accordingly. These results strongly support a model in which septal thickness is controlled by curved molecular clamps formed by SepF polymers attached to the leading edge of nascent septa. This also implies that the intrinsic shape of a protein polymer can function as a mold to shape the cell wall.

AB - Gram-positive bacteria divide by forming a thick cross wall. How the thickness of this septal wall is controlled is unknown. In this type of bacteria, the key cell division protein FtsZ is anchored to the cell membrane by two proteins, FtsA and/or SepF. We have isolated SepF homologs from different bacterial species and found that they all polymerize into large protein rings with diameters varying from 19 to 44 nm. Interestingly, these values correlated well with the thickness of their septa. To test whether ring diameter determines septal thickness, we tried to construct different SepF chimeras with the purpose to manipulate the diameter of the SepF protein ring. This was indeed possible and confirmed that the conserved core domain of SepF regulates ring diameter. Importantly, when SepF chimeras with different diameters were expressed in the bacterial host Bacillus subtilis, the thickness of its septa changed accordingly. These results strongly support a model in which septal thickness is controlled by curved molecular clamps formed by SepF polymers attached to the leading edge of nascent septa. This also implies that the intrinsic shape of a protein polymer can function as a mold to shape the cell wall.

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ER -

Control of septum thickness by the curvature of sepf polymers

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