Chlamydial MreB Directs Cell Division and Peptidoglycan Synthesis in <named-content content-type="genus-species">Escherichia coli</named-content> in the Absence of FtsZ Activity

ABSTRACT Cell division is the ultimate process for the propagation of bacteria, and FtsZ is an essential protein used by nearly all bacteria for this function. Chlamydiae belong to a small group of bacteria that lack the universal cell division protein FtsZ but still divide by binary fission. Chlamy...

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Autores principales: Dev K. Ranjit, George W. Liechti, Anthony T. Maurelli
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:8ab6b8e4b99d43a6bd19698dee9c19412021-11-15T15:56:58ZChlamydial MreB Directs Cell Division and Peptidoglycan Synthesis in <named-content content-type="genus-species">Escherichia coli</named-content> in the Absence of FtsZ Activity10.1128/mBio.03222-192150-7511https://doaj.org/article/8ab6b8e4b99d43a6bd19698dee9c19412020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.03222-19https://doaj.org/toc/2150-7511ABSTRACT Cell division is the ultimate process for the propagation of bacteria, and FtsZ is an essential protein used by nearly all bacteria for this function. Chlamydiae belong to a small group of bacteria that lack the universal cell division protein FtsZ but still divide by binary fission. Chlamydial MreB is a member of the shape-determining MreB/Mbl family of proteins responsible for rod shape morphology in Escherichia coli. Chlamydia also encodes a homolog of RodZ, an MreB assembly cytoskeletal protein that links MreB to cell wall synthesis proteins. We hypothesized that MreB directs cell division in Chlamydia and that chlamydial MreB could replace FtsZ function for cell division in E. coli. Overexpression of chlamydial mreB-rodZ in E. coli induced prominent morphological changes with production of large swollen or oval bacteria, eventually resulting in bacterial lysis. Low-level expression of chlamydial mreB-rodZ restored viability of a lethal ΔmreB mutation in E. coli, although the bacteria lost their typical rod shape and grew as rounded cells. When FtsZ activity was inhibited by overexpression of SulA in the ΔmreB mutant of E. coli complemented with chlamydial mreB-rodZ, spherical E. coli grew and divided. Localization studies using a fluorescent fusion chlamydial MreB protein indicated that chlamydial RodZ directs chlamydial MreB to the E. coli division septum. These results demonstrate that chlamydial MreB, in partnership with chlamydial RodZ, acts as a cell division protein. Our findings suggest that an mreB-rodZ-based mechanism allows Chlamydia to divide without the universal division protein FtsZ. IMPORTANCE The study of Chlamydia growth and cell division is complicated by its obligate intracellular nature and biphasic lifestyle. Chlamydia also lacks the universal division protein FtsZ. We employed the cell division system of Escherichia coli as a surrogate to identify chlamydial cell division proteins. We demonstrate that chlamydial MreB, together with chlamydial RodZ, forms a cell division and growth complex that can replace FtsZ activity and support cell division in E. coli. Chlamydial RodZ plays a major role in directing chlamydial MreB localization to the cell division site. It is likely that the evolution of chlamydial MreB and RodZ to form a functional cell division complex allowed Chlamydia to dispense with its FtsZ-based cell division machinery during genome reduction. Thus, MreB-RodZ represents a possible mechanism for cell division in other bacteria lacking FtsZ.Dev K. RanjitGeorge W. LiechtiAnthony T. MaurelliAmerican Society for MicrobiologyarticleChlamydiaMreBRodZFtsZcell divisionpeptidoglycanMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution DOAJ
collection DOAJ
language EN
topic Chlamydia
MreB
RodZ
FtsZ
cell division
peptidoglycan
Microbiology
QR1-502
spellingShingle Chlamydia
MreB
RodZ
FtsZ
cell division
peptidoglycan
Microbiology
QR1-502
Dev K. Ranjit
George W. Liechti
Anthony T. Maurelli
Chlamydial MreB Directs Cell Division and Peptidoglycan Synthesis in <named-content content-type="genus-species">Escherichia coli</named-content> in the Absence of FtsZ Activity
description ABSTRACT Cell division is the ultimate process for the propagation of bacteria, and FtsZ is an essential protein used by nearly all bacteria for this function. Chlamydiae belong to a small group of bacteria that lack the universal cell division protein FtsZ but still divide by binary fission. Chlamydial MreB is a member of the shape-determining MreB/Mbl family of proteins responsible for rod shape morphology in Escherichia coli. Chlamydia also encodes a homolog of RodZ, an MreB assembly cytoskeletal protein that links MreB to cell wall synthesis proteins. We hypothesized that MreB directs cell division in Chlamydia and that chlamydial MreB could replace FtsZ function for cell division in E. coli. Overexpression of chlamydial mreB-rodZ in E. coli induced prominent morphological changes with production of large swollen or oval bacteria, eventually resulting in bacterial lysis. Low-level expression of chlamydial mreB-rodZ restored viability of a lethal ΔmreB mutation in E. coli, although the bacteria lost their typical rod shape and grew as rounded cells. When FtsZ activity was inhibited by overexpression of SulA in the ΔmreB mutant of E. coli complemented with chlamydial mreB-rodZ, spherical E. coli grew and divided. Localization studies using a fluorescent fusion chlamydial MreB protein indicated that chlamydial RodZ directs chlamydial MreB to the E. coli division septum. These results demonstrate that chlamydial MreB, in partnership with chlamydial RodZ, acts as a cell division protein. Our findings suggest that an mreB-rodZ-based mechanism allows Chlamydia to divide without the universal division protein FtsZ. IMPORTANCE The study of Chlamydia growth and cell division is complicated by its obligate intracellular nature and biphasic lifestyle. Chlamydia also lacks the universal division protein FtsZ. We employed the cell division system of Escherichia coli as a surrogate to identify chlamydial cell division proteins. We demonstrate that chlamydial MreB, together with chlamydial RodZ, forms a cell division and growth complex that can replace FtsZ activity and support cell division in E. coli. Chlamydial RodZ plays a major role in directing chlamydial MreB localization to the cell division site. It is likely that the evolution of chlamydial MreB and RodZ to form a functional cell division complex allowed Chlamydia to dispense with its FtsZ-based cell division machinery during genome reduction. Thus, MreB-RodZ represents a possible mechanism for cell division in other bacteria lacking FtsZ.
format article
author Dev K. Ranjit
George W. Liechti
Anthony T. Maurelli
author_facet Dev K. Ranjit
George W. Liechti
Anthony T. Maurelli
author_sort Dev K. Ranjit
title Chlamydial MreB Directs Cell Division and Peptidoglycan Synthesis in <named-content content-type="genus-species">Escherichia coli</named-content> in the Absence of FtsZ Activity
title_short Chlamydial MreB Directs Cell Division and Peptidoglycan Synthesis in <named-content content-type="genus-species">Escherichia coli</named-content> in the Absence of FtsZ Activity
title_full Chlamydial MreB Directs Cell Division and Peptidoglycan Synthesis in <named-content content-type="genus-species">Escherichia coli</named-content> in the Absence of FtsZ Activity
title_fullStr Chlamydial MreB Directs Cell Division and Peptidoglycan Synthesis in <named-content content-type="genus-species">Escherichia coli</named-content> in the Absence of FtsZ Activity
title_full_unstemmed Chlamydial MreB Directs Cell Division and Peptidoglycan Synthesis in <named-content content-type="genus-species">Escherichia coli</named-content> in the Absence of FtsZ Activity
title_sort chlamydial mreb directs cell division and peptidoglycan synthesis in <named-content content-type="genus-species">escherichia coli</named-content> in the absence of ftsz activity
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/8ab6b8e4b99d43a6bd19698dee9c1941
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