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Seven-transmembrane receptor protein RgsP and cell wall-binding protein RgsM promote unipolar growth in Rhizobiales

Members of the Rhizobiales (class of α-proteobacteria) display zonal peptidoglycan cell wall growth at one cell pole, contrasting with the dispersed mode of cell wall growth along the sidewalls of many other rod-shaped bacteria. Here we show that the seven-transmembrane receptor (7TMR) protein RgsP...

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Autores principales: Schäper, Simon, Yau, Hamish C. L., Krol, Elizaveta, Skotnicka, Dorota, Heimerl, Thomas, Gray, Joe, Kaever, Volkhard, Søgaard-Andersen, Lotte, Vollmer, Waldemar, Becker, Anke
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6107284/
https://www.ncbi.nlm.nih.gov/pubmed/30102748
http://dx.doi.org/10.1371/journal.pgen.1007594
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author Schäper, Simon
Yau, Hamish C. L.
Krol, Elizaveta
Skotnicka, Dorota
Heimerl, Thomas
Gray, Joe
Kaever, Volkhard
Søgaard-Andersen, Lotte
Vollmer, Waldemar
Becker, Anke
author_facet Schäper, Simon
Yau, Hamish C. L.
Krol, Elizaveta
Skotnicka, Dorota
Heimerl, Thomas
Gray, Joe
Kaever, Volkhard
Søgaard-Andersen, Lotte
Vollmer, Waldemar
Becker, Anke
author_sort Schäper, Simon
collection PubMed
description Members of the Rhizobiales (class of α-proteobacteria) display zonal peptidoglycan cell wall growth at one cell pole, contrasting with the dispersed mode of cell wall growth along the sidewalls of many other rod-shaped bacteria. Here we show that the seven-transmembrane receptor (7TMR) protein RgsP (SMc00074), together with the putative membrane-anchored peptidoglycan metallopeptidase RgsM (SMc02432), have key roles in unipolar peptidoglycan formation during growth and at mid-cell during cell division in Sinorhizobium meliloti. RgsP is composed of a periplasmic globular 7TMR-DISMED2 domain, a membrane-spanning region, and cytoplasmic PAS, GGDEF and EAL domains. The EAL domain confers phosphodiesterase activity towards the second messenger cyclic di-GMP, a key regulatory player in the transition between bacterial lifestyles. RgsP and RgsM localize to sites of zonal cell wall synthesis at the new cell pole and cell divison site, suggesting a role in cell wall biogenesis. The two proteins are essential for cell wall biogenesis and cell growth. Cells depleted of RgsP or RgsM had an altered muropeptide composition and RgsM binds to peptidoglycan. RgsP and RgsM orthologs are functional when interchanged between α-rhizobial species pointing to a conserved mechanism for cell wall biogenesis/remodeling within the Rhizobiales. Overall, our findings suggest that RgsP and RgsM contribute to the regulation of unipolar cell wall biogenesis in α-rhizobia.
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spelling pubmed-61072842018-08-30 Seven-transmembrane receptor protein RgsP and cell wall-binding protein RgsM promote unipolar growth in Rhizobiales Schäper, Simon Yau, Hamish C. L. Krol, Elizaveta Skotnicka, Dorota Heimerl, Thomas Gray, Joe Kaever, Volkhard Søgaard-Andersen, Lotte Vollmer, Waldemar Becker, Anke PLoS Genet Research Article Members of the Rhizobiales (class of α-proteobacteria) display zonal peptidoglycan cell wall growth at one cell pole, contrasting with the dispersed mode of cell wall growth along the sidewalls of many other rod-shaped bacteria. Here we show that the seven-transmembrane receptor (7TMR) protein RgsP (SMc00074), together with the putative membrane-anchored peptidoglycan metallopeptidase RgsM (SMc02432), have key roles in unipolar peptidoglycan formation during growth and at mid-cell during cell division in Sinorhizobium meliloti. RgsP is composed of a periplasmic globular 7TMR-DISMED2 domain, a membrane-spanning region, and cytoplasmic PAS, GGDEF and EAL domains. The EAL domain confers phosphodiesterase activity towards the second messenger cyclic di-GMP, a key regulatory player in the transition between bacterial lifestyles. RgsP and RgsM localize to sites of zonal cell wall synthesis at the new cell pole and cell divison site, suggesting a role in cell wall biogenesis. The two proteins are essential for cell wall biogenesis and cell growth. Cells depleted of RgsP or RgsM had an altered muropeptide composition and RgsM binds to peptidoglycan. RgsP and RgsM orthologs are functional when interchanged between α-rhizobial species pointing to a conserved mechanism for cell wall biogenesis/remodeling within the Rhizobiales. Overall, our findings suggest that RgsP and RgsM contribute to the regulation of unipolar cell wall biogenesis in α-rhizobia. Public Library of Science 2018-08-13 /pmc/articles/PMC6107284/ /pubmed/30102748 http://dx.doi.org/10.1371/journal.pgen.1007594 Text en © 2018 Schäper et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Schäper, Simon
Yau, Hamish C. L.
Krol, Elizaveta
Skotnicka, Dorota
Heimerl, Thomas
Gray, Joe
Kaever, Volkhard
Søgaard-Andersen, Lotte
Vollmer, Waldemar
Becker, Anke
Seven-transmembrane receptor protein RgsP and cell wall-binding protein RgsM promote unipolar growth in Rhizobiales
title Seven-transmembrane receptor protein RgsP and cell wall-binding protein RgsM promote unipolar growth in Rhizobiales
title_full Seven-transmembrane receptor protein RgsP and cell wall-binding protein RgsM promote unipolar growth in Rhizobiales
title_fullStr Seven-transmembrane receptor protein RgsP and cell wall-binding protein RgsM promote unipolar growth in Rhizobiales
title_full_unstemmed Seven-transmembrane receptor protein RgsP and cell wall-binding protein RgsM promote unipolar growth in Rhizobiales
title_short Seven-transmembrane receptor protein RgsP and cell wall-binding protein RgsM promote unipolar growth in Rhizobiales
title_sort seven-transmembrane receptor protein rgsp and cell wall-binding protein rgsm promote unipolar growth in rhizobiales
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6107284/
https://www.ncbi.nlm.nih.gov/pubmed/30102748
http://dx.doi.org/10.1371/journal.pgen.1007594
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