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Localized cardiolipin synthesis is required for the assembly of MreB during the polarized cell division of Chlamydia trachomatis

Pathogenic Chlamydia species are coccoid bacteria that use the rod-shape determining protein MreB to direct septal peptidoglycan synthesis during their polarized cell division process. How the site of polarized budding is determined in this bacterium, where contextual features like membrane curvatur...

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Autores principales: Ouellette, Scot P., Fisher-Marvin, Laura A., Harpring, McKenna, Lee, Junghoon, Rucks, Elizabeth A., Cox, John V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9499288/
https://www.ncbi.nlm.nih.gov/pubmed/36095021
http://dx.doi.org/10.1371/journal.ppat.1010836
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author Ouellette, Scot P.
Fisher-Marvin, Laura A.
Harpring, McKenna
Lee, Junghoon
Rucks, Elizabeth A.
Cox, John V.
author_facet Ouellette, Scot P.
Fisher-Marvin, Laura A.
Harpring, McKenna
Lee, Junghoon
Rucks, Elizabeth A.
Cox, John V.
author_sort Ouellette, Scot P.
collection PubMed
description Pathogenic Chlamydia species are coccoid bacteria that use the rod-shape determining protein MreB to direct septal peptidoglycan synthesis during their polarized cell division process. How the site of polarized budding is determined in this bacterium, where contextual features like membrane curvature are seemingly identical, is unclear. We hypothesized that the accumulation of the phospholipid, cardiolipin (CL), in specific regions of the cell membrane induces localized membrane changes that trigger the recruitment of MreB to the site where the bud will arise. To test this, we ectopically expressed cardiolipin synthase (Cls) and observed a polar distribution for this enzyme in Chlamydia trachomatis. In early division intermediates, Cls was restricted to the bud site where MreB is localized and peptidoglycan synthesis is initiated. The localization profile of 6xHis tagged Cls (Cls_6xH) throughout division mimicked the distribution of lipids that stain with NAO, a dye that labels CL. Treatment of Chlamydia with 3’,6-dinonylneamine (diNN), an antibiotic targeting CL-containing membrane domains, resulted in redistribution of Cls_6xH and NAO-staining phospholipids. In addition, 6xHis tagged MreB localization was altered by diNN treatment, suggesting an upstream regulatory role for CL-containing membranes in directing the assembly of MreB. This hypothesis is consistent with the observation that the clustered localization of Cls_6xH is not dependent upon MreB function or peptidoglycan synthesis. Furthermore, expression of a CL-binding protein at the inner membrane of C. trachomatis dramatically inhibited bacterial growth supporting the importance of CL in the division process. Our findings implicate a critical role for localized CL synthesis in driving MreB assembly at the bud site during the polarized cell division of Chlamydia.
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spelling pubmed-94992882022-09-23 Localized cardiolipin synthesis is required for the assembly of MreB during the polarized cell division of Chlamydia trachomatis Ouellette, Scot P. Fisher-Marvin, Laura A. Harpring, McKenna Lee, Junghoon Rucks, Elizabeth A. Cox, John V. PLoS Pathog Research Article Pathogenic Chlamydia species are coccoid bacteria that use the rod-shape determining protein MreB to direct septal peptidoglycan synthesis during their polarized cell division process. How the site of polarized budding is determined in this bacterium, where contextual features like membrane curvature are seemingly identical, is unclear. We hypothesized that the accumulation of the phospholipid, cardiolipin (CL), in specific regions of the cell membrane induces localized membrane changes that trigger the recruitment of MreB to the site where the bud will arise. To test this, we ectopically expressed cardiolipin synthase (Cls) and observed a polar distribution for this enzyme in Chlamydia trachomatis. In early division intermediates, Cls was restricted to the bud site where MreB is localized and peptidoglycan synthesis is initiated. The localization profile of 6xHis tagged Cls (Cls_6xH) throughout division mimicked the distribution of lipids that stain with NAO, a dye that labels CL. Treatment of Chlamydia with 3’,6-dinonylneamine (diNN), an antibiotic targeting CL-containing membrane domains, resulted in redistribution of Cls_6xH and NAO-staining phospholipids. In addition, 6xHis tagged MreB localization was altered by diNN treatment, suggesting an upstream regulatory role for CL-containing membranes in directing the assembly of MreB. This hypothesis is consistent with the observation that the clustered localization of Cls_6xH is not dependent upon MreB function or peptidoglycan synthesis. Furthermore, expression of a CL-binding protein at the inner membrane of C. trachomatis dramatically inhibited bacterial growth supporting the importance of CL in the division process. Our findings implicate a critical role for localized CL synthesis in driving MreB assembly at the bud site during the polarized cell division of Chlamydia. Public Library of Science 2022-09-12 /pmc/articles/PMC9499288/ /pubmed/36095021 http://dx.doi.org/10.1371/journal.ppat.1010836 Text en © 2022 Ouellette et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://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
Ouellette, Scot P.
Fisher-Marvin, Laura A.
Harpring, McKenna
Lee, Junghoon
Rucks, Elizabeth A.
Cox, John V.
Localized cardiolipin synthesis is required for the assembly of MreB during the polarized cell division of Chlamydia trachomatis
title Localized cardiolipin synthesis is required for the assembly of MreB during the polarized cell division of Chlamydia trachomatis
title_full Localized cardiolipin synthesis is required for the assembly of MreB during the polarized cell division of Chlamydia trachomatis
title_fullStr Localized cardiolipin synthesis is required for the assembly of MreB during the polarized cell division of Chlamydia trachomatis
title_full_unstemmed Localized cardiolipin synthesis is required for the assembly of MreB during the polarized cell division of Chlamydia trachomatis
title_short Localized cardiolipin synthesis is required for the assembly of MreB during the polarized cell division of Chlamydia trachomatis
title_sort localized cardiolipin synthesis is required for the assembly of mreb during the polarized cell division of chlamydia trachomatis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9499288/
https://www.ncbi.nlm.nih.gov/pubmed/36095021
http://dx.doi.org/10.1371/journal.ppat.1010836
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