A SpoIID Homolog Cleaves Glycan Strands at the Chlamydial Division Septum

ABSTRACT Chlamydiales species are obligate intracellular bacteria lacking a classical peptidoglycan sacculus but relying on peptidoglycan synthesis for cytokinesis. While septal peptidoglycan biosynthesis seems to be regulated by MreB actin and its membrane anchor RodZ rather than FtsZ tubulin in Ch...

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Autores principales:	Nicolas Jacquier, Akhilesh K. Yadav, Trestan Pillonel, Patrick H. Viollier, Felipe Cava, Gilbert Greub
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Chlamydiales Waddlia chondrophila cell division peptidoglycan sporulation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c882de4ca87549c197f4259b777889d0
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spelling	oai:doaj.org-article:c882de4ca87549c197f4259b777889d02021-11-15T16:22:09ZA SpoIID Homolog Cleaves Glycan Strands at the Chlamydial Division Septum10.1128/mBio.01128-192150-7511https://doaj.org/article/c882de4ca87549c197f4259b777889d02019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01128-19https://doaj.org/toc/2150-7511ABSTRACT Chlamydiales species are obligate intracellular bacteria lacking a classical peptidoglycan sacculus but relying on peptidoglycan synthesis for cytokinesis. While septal peptidoglycan biosynthesis seems to be regulated by MreB actin and its membrane anchor RodZ rather than FtsZ tubulin in Chlamydiales, the mechanism of peptidoglycan remodeling is poorly understood. An amidase conserved in Chlamydiales is able to cleave peptide stems in peptidoglycan, but it is not clear how peptidoglycan glycan strands are cleaved since no classical lytic transglycosylase is encoded in chlamydial genomes. However, a protein containing a SpoIID domain, known to possess transglycosylase activity in Bacillus subtilis, is conserved in Chlamydiales. We show here that the SpoIID homologue of the Chlamydia-related pathogen Waddlia chondrophila is a septal peptidoglycan-binding protein. Moreover, we demonstrate that SpoIID acts as a lytic transglycosylase on peptidoglycan and as a muramidase on denuded glycan strands in vitro. As SpoIID-like proteins are widespread in nonsporulating bacteria, SpoIID might commonly be a septal peptidoglycan remodeling protein in bacteria, including obligate intracellular pathogens, and thus might represent a promising drug target. IMPORTANCE Chlamydiales species are obligate intracellular bacteria and important human pathogens that have a minimal division machinery lacking the proteins that are essential for bacterial division in other species, such as FtsZ. Chlamydial division requires synthesis of peptidoglycan, which forms a ring at the division septum and is rapidly turned over. However, little is known of peptidoglycan degradation, because many peptidoglycan-degrading enzymes are not encoded by chlamydial genomes. Here we show that an homologue of SpoIID, a peptidoglycan-degrading enzyme involved in sporulation of bacteria such as Bacillus subtilis, is expressed in Chlamydiales, localizes at the division septum, and degrades peptidoglycan in vitro, indicating that SpoIID is not only involved in sporulation but also likely implicated in division of some bacteria.Nicolas JacquierAkhilesh K. YadavTrestan PillonelPatrick H. ViollierFelipe CavaGilbert GreubAmerican Society for MicrobiologyarticleChlamydialesWaddlia chondrophilacell divisionpeptidoglycansporulationMicrobiologyQR1-502ENmBio, Vol 10, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Chlamydiales Waddlia chondrophila cell division peptidoglycan sporulation Microbiology QR1-502
spellingShingle	Chlamydiales Waddlia chondrophila cell division peptidoglycan sporulation Microbiology QR1-502 Nicolas Jacquier Akhilesh K. Yadav Trestan Pillonel Patrick H. Viollier Felipe Cava Gilbert Greub A SpoIID Homolog Cleaves Glycan Strands at the Chlamydial Division Septum
description	ABSTRACT Chlamydiales species are obligate intracellular bacteria lacking a classical peptidoglycan sacculus but relying on peptidoglycan synthesis for cytokinesis. While septal peptidoglycan biosynthesis seems to be regulated by MreB actin and its membrane anchor RodZ rather than FtsZ tubulin in Chlamydiales, the mechanism of peptidoglycan remodeling is poorly understood. An amidase conserved in Chlamydiales is able to cleave peptide stems in peptidoglycan, but it is not clear how peptidoglycan glycan strands are cleaved since no classical lytic transglycosylase is encoded in chlamydial genomes. However, a protein containing a SpoIID domain, known to possess transglycosylase activity in Bacillus subtilis, is conserved in Chlamydiales. We show here that the SpoIID homologue of the Chlamydia-related pathogen Waddlia chondrophila is a septal peptidoglycan-binding protein. Moreover, we demonstrate that SpoIID acts as a lytic transglycosylase on peptidoglycan and as a muramidase on denuded glycan strands in vitro. As SpoIID-like proteins are widespread in nonsporulating bacteria, SpoIID might commonly be a septal peptidoglycan remodeling protein in bacteria, including obligate intracellular pathogens, and thus might represent a promising drug target. IMPORTANCE Chlamydiales species are obligate intracellular bacteria and important human pathogens that have a minimal division machinery lacking the proteins that are essential for bacterial division in other species, such as FtsZ. Chlamydial division requires synthesis of peptidoglycan, which forms a ring at the division septum and is rapidly turned over. However, little is known of peptidoglycan degradation, because many peptidoglycan-degrading enzymes are not encoded by chlamydial genomes. Here we show that an homologue of SpoIID, a peptidoglycan-degrading enzyme involved in sporulation of bacteria such as Bacillus subtilis, is expressed in Chlamydiales, localizes at the division septum, and degrades peptidoglycan in vitro, indicating that SpoIID is not only involved in sporulation but also likely implicated in division of some bacteria.
format	article
author	Nicolas Jacquier Akhilesh K. Yadav Trestan Pillonel Patrick H. Viollier Felipe Cava Gilbert Greub
author_facet	Nicolas Jacquier Akhilesh K. Yadav Trestan Pillonel Patrick H. Viollier Felipe Cava Gilbert Greub
author_sort	Nicolas Jacquier
title	A SpoIID Homolog Cleaves Glycan Strands at the Chlamydial Division Septum
title_short	A SpoIID Homolog Cleaves Glycan Strands at the Chlamydial Division Septum
title_full	A SpoIID Homolog Cleaves Glycan Strands at the Chlamydial Division Septum
title_fullStr	A SpoIID Homolog Cleaves Glycan Strands at the Chlamydial Division Septum
title_full_unstemmed	A SpoIID Homolog Cleaves Glycan Strands at the Chlamydial Division Septum
title_sort	spoiid homolog cleaves glycan strands at the chlamydial division septum
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/c882de4ca87549c197f4259b777889d0
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A SpoIID Homolog Cleaves Glycan Strands at the Chlamydial Division Septum

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