Modification of cell wall polysaccharide guides cell division in Streptococcus mutans

Svetlana Zamakhaeva; Catherine T. Chaton; Jeffrey S. Rush; Sowmya Ajay Castro; Cameron W. Kenner; Alexander E. Yarawsky; Andrew B. Herr; Nina M. van Sorge; Helge C. Dorfmueller; Gregory I. Frolenkov; Konstantin V. Korotkov; Natalia Korotkova

doi:10.1038/s41589-021-00803-9

Modification of cell wall polysaccharide guides cell division in Streptococcus mutans

Svetlana Zamakhaeva, Catherine T. Chaton, Jeffrey S. Rush, Sowmya Ajay Castro, Cameron W. Kenner, Alexander E. Yarawsky, Andrew B. Herr, Nina M. van Sorge, Helge C. Dorfmueller, Gregory I. Frolenkov, Konstantin V. Korotkov, Natalia Korotkova

Research output: Contribution to journal › Article › peer-review

14 Scopus citations

Abstract

In ovoid-shaped, Gram-positive bacteria, MapZ guides FtsZ-ring positioning at cell equators. The cell wall of the ovococcus Streptococcus mutans contains peptidoglycan decorated with serotype c carbohydrates (SCCs). In the present study, we identify the major cell separation autolysin AtlA as an SCC-binding protein. AtlA binding to SCC is attenuated by the glycerol phosphate (GroP) modification. Using fluorescently labeled AtlA constructs, we mapped SCC distribution on the streptococcal surface, revealing enrichment of GroP-deficient immature SCCs at the cell poles and equators. The immature SCCs co-localize with MapZ at the equatorial rings throughout the cell cycle. In GroP-deficient mutants, AtlA is mislocalized, resulting in dysregulated cellular autolysis. These mutants display morphological abnormalities associated with MapZ mislocalization, leading to FtsZ-ring misplacement. Altogether, our data support a model in which maturation of a cell wall polysaccharide provides the molecular cues for the recruitment of cell division machinery, ensuring proper daughter cell separation and FtsZ-ring positioning. [Figure not available: see fulltext.].

Original language	English
Pages (from-to)	878-887
Number of pages	10
Journal	Nature Chemical Biology
Volume	17
Issue number	8
DOIs	https://doi.org/10.1038/s41589-021-00803-9
State	Published - Aug 2021

Bibliographical note

Funding Information:
We thank S.-J. Ahn (University of Florida) for the kind gift of anti-AtlA antibodies, J. Abranches (University of Florida) for providing S. mutans serotype e, f and k strains; J. F. Timoney (University of Kentucky) and J. Huebner (von Hauner Children’s Hospital, LMU) for providing S. equi and E. faecalis, respectively; J. M. Bosken and E. D. Hall (University of Kentucky) for the use of the Thermo Fisher Scientific GC–MS instrument and C. Velez-Ortega (University of Kentucky) for access to a Leica SP8 confocal microscope. This work was supported by National Institutes of Health (NIH) grants (nos. R01 DE028916 from the National Institute of Dental and Craniofacial Research (NIDCR) and R01 AI143690 from the National Institute of Allergy and Infectious Diseases to N.K., R01 GM094363 from the National Institute of General Medical Sciences to A.B.H. and R01 DC014658 from the NIDCD to G.I.F.), Tenovus Scotland large research grant (no. T17/17) and University of Dundee Wellcome Fund (grant no. 105606/Z/14/Z) to S.A.C. and H.C.D., and the Wellcome and Royal Society grant (no. 109357/Z/15/Z) to H.C.D.. SEM was performed at the Electron Microscopy Center, which belongs to the National Science Foundation NNCI Kentucky Multiscale Manufacturing and Nano Integration Node, supported by ECCS-1542174. Carbohydrate composition analysis at the Complex Carbohydrate Research Center was supported by the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, US Department of Energy grant (no. DE-FG02-93ER20097). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Publisher Copyright:
© 2021, The Author(s), under exclusive licence to Springer Nature America, Inc.

ASJC Scopus subject areas

Molecular Biology
Cell Biology

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Zamakhaeva, S., Chaton, C. T., Rush, J. S., Ajay Castro, S., Kenner, C. W., Yarawsky, A. E., Herr, A. B., van Sorge, N. M., Dorfmueller, H. C., Frolenkov, G. I., Korotkov, K. V., & Korotkova, N. (2021). Modification of cell wall polysaccharide guides cell division in Streptococcus mutans. Nature Chemical Biology, 17(8), 878-887. https://doi.org/10.1038/s41589-021-00803-9

@article{0df62edebda24127af454864a8baa0f9,

title = "Modification of cell wall polysaccharide guides cell division in Streptococcus mutans",

abstract = "In ovoid-shaped, Gram-positive bacteria, MapZ guides FtsZ-ring positioning at cell equators. The cell wall of the ovococcus Streptococcus mutans contains peptidoglycan decorated with serotype c carbohydrates (SCCs). In the present study, we identify the major cell separation autolysin AtlA as an SCC-binding protein. AtlA binding to SCC is attenuated by the glycerol phosphate (GroP) modification. Using fluorescently labeled AtlA constructs, we mapped SCC distribution on the streptococcal surface, revealing enrichment of GroP-deficient immature SCCs at the cell poles and equators. The immature SCCs co-localize with MapZ at the equatorial rings throughout the cell cycle. In GroP-deficient mutants, AtlA is mislocalized, resulting in dysregulated cellular autolysis. These mutants display morphological abnormalities associated with MapZ mislocalization, leading to FtsZ-ring misplacement. Altogether, our data support a model in which maturation of a cell wall polysaccharide provides the molecular cues for the recruitment of cell division machinery, ensuring proper daughter cell separation and FtsZ-ring positioning. [Figure not available: see fulltext.].",

author = "Svetlana Zamakhaeva and Chaton, {Catherine T.} and Rush, {Jeffrey S.} and {Ajay Castro}, Sowmya and Kenner, {Cameron W.} and Yarawsky, {Alexander E.} and Herr, {Andrew B.} and {van Sorge}, {Nina M.} and Dorfmueller, {Helge C.} and Frolenkov, {Gregory I.} and Korotkov, {Konstantin V.} and Natalia Korotkova",

note = "Funding Information: We thank S.-J. Ahn (University of Florida) for the kind gift of anti-AtlA antibodies, J. Abranches (University of Florida) for providing S. mutans serotype e, f and k strains; J. F. Timoney (University of Kentucky) and J. Huebner (von Hauner Children{\textquoteright}s Hospital, LMU) for providing S. equi and E. faecalis, respectively; J. M. Bosken and E. D. Hall (University of Kentucky) for the use of the Thermo Fisher Scientific GC–MS instrument and C. Velez-Ortega (University of Kentucky) for access to a Leica SP8 confocal microscope. This work was supported by National Institutes of Health (NIH) grants (nos. R01 DE028916 from the National Institute of Dental and Craniofacial Research (NIDCR) and R01 AI143690 from the National Institute of Allergy and Infectious Diseases to N.K., R01 GM094363 from the National Institute of General Medical Sciences to A.B.H. and R01 DC014658 from the NIDCD to G.I.F.), Tenovus Scotland large research grant (no. T17/17) and University of Dundee Wellcome Fund (grant no. 105606/Z/14/Z) to S.A.C. and H.C.D., and the Wellcome and Royal Society grant (no. 109357/Z/15/Z) to H.C.D.. SEM was performed at the Electron Microscopy Center, which belongs to the National Science Foundation NNCI Kentucky Multiscale Manufacturing and Nano Integration Node, supported by ECCS-1542174. Carbohydrate composition analysis at the Complex Carbohydrate Research Center was supported by the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, US Department of Energy grant (no. DE-FG02-93ER20097). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Publisher Copyright: {\textcopyright} 2021, The Author(s), under exclusive licence to Springer Nature America, Inc.",

year = "2021",

month = aug,

doi = "10.1038/s41589-021-00803-9",

language = "English",

volume = "17",

pages = "878--887",

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T1 - Modification of cell wall polysaccharide guides cell division in Streptococcus mutans

AU - Zamakhaeva, Svetlana

AU - Chaton, Catherine T.

AU - Rush, Jeffrey S.

AU - Ajay Castro, Sowmya

AU - Kenner, Cameron W.

AU - Yarawsky, Alexander E.

AU - Herr, Andrew B.

AU - van Sorge, Nina M.

AU - Dorfmueller, Helge C.

AU - Frolenkov, Gregory I.

AU - Korotkov, Konstantin V.

AU - Korotkova, Natalia

N1 - Funding Information: We thank S.-J. Ahn (University of Florida) for the kind gift of anti-AtlA antibodies, J. Abranches (University of Florida) for providing S. mutans serotype e, f and k strains; J. F. Timoney (University of Kentucky) and J. Huebner (von Hauner Children’s Hospital, LMU) for providing S. equi and E. faecalis, respectively; J. M. Bosken and E. D. Hall (University of Kentucky) for the use of the Thermo Fisher Scientific GC–MS instrument and C. Velez-Ortega (University of Kentucky) for access to a Leica SP8 confocal microscope. This work was supported by National Institutes of Health (NIH) grants (nos. R01 DE028916 from the National Institute of Dental and Craniofacial Research (NIDCR) and R01 AI143690 from the National Institute of Allergy and Infectious Diseases to N.K., R01 GM094363 from the National Institute of General Medical Sciences to A.B.H. and R01 DC014658 from the NIDCD to G.I.F.), Tenovus Scotland large research grant (no. T17/17) and University of Dundee Wellcome Fund (grant no. 105606/Z/14/Z) to S.A.C. and H.C.D., and the Wellcome and Royal Society grant (no. 109357/Z/15/Z) to H.C.D.. SEM was performed at the Electron Microscopy Center, which belongs to the National Science Foundation NNCI Kentucky Multiscale Manufacturing and Nano Integration Node, supported by ECCS-1542174. Carbohydrate composition analysis at the Complex Carbohydrate Research Center was supported by the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, US Department of Energy grant (no. DE-FG02-93ER20097). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Publisher Copyright: © 2021, The Author(s), under exclusive licence to Springer Nature America, Inc.

PY - 2021/8

Y1 - 2021/8

N2 - In ovoid-shaped, Gram-positive bacteria, MapZ guides FtsZ-ring positioning at cell equators. The cell wall of the ovococcus Streptococcus mutans contains peptidoglycan decorated with serotype c carbohydrates (SCCs). In the present study, we identify the major cell separation autolysin AtlA as an SCC-binding protein. AtlA binding to SCC is attenuated by the glycerol phosphate (GroP) modification. Using fluorescently labeled AtlA constructs, we mapped SCC distribution on the streptococcal surface, revealing enrichment of GroP-deficient immature SCCs at the cell poles and equators. The immature SCCs co-localize with MapZ at the equatorial rings throughout the cell cycle. In GroP-deficient mutants, AtlA is mislocalized, resulting in dysregulated cellular autolysis. These mutants display morphological abnormalities associated with MapZ mislocalization, leading to FtsZ-ring misplacement. Altogether, our data support a model in which maturation of a cell wall polysaccharide provides the molecular cues for the recruitment of cell division machinery, ensuring proper daughter cell separation and FtsZ-ring positioning. [Figure not available: see fulltext.].

AB - In ovoid-shaped, Gram-positive bacteria, MapZ guides FtsZ-ring positioning at cell equators. The cell wall of the ovococcus Streptococcus mutans contains peptidoglycan decorated with serotype c carbohydrates (SCCs). In the present study, we identify the major cell separation autolysin AtlA as an SCC-binding protein. AtlA binding to SCC is attenuated by the glycerol phosphate (GroP) modification. Using fluorescently labeled AtlA constructs, we mapped SCC distribution on the streptococcal surface, revealing enrichment of GroP-deficient immature SCCs at the cell poles and equators. The immature SCCs co-localize with MapZ at the equatorial rings throughout the cell cycle. In GroP-deficient mutants, AtlA is mislocalized, resulting in dysregulated cellular autolysis. These mutants display morphological abnormalities associated with MapZ mislocalization, leading to FtsZ-ring misplacement. Altogether, our data support a model in which maturation of a cell wall polysaccharide provides the molecular cues for the recruitment of cell division machinery, ensuring proper daughter cell separation and FtsZ-ring positioning. [Figure not available: see fulltext.].

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JO - Nature Chemical Biology

JF - Nature Chemical Biology

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ER -

Modification of cell wall polysaccharide guides cell division in Streptococcus mutans

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