Discovery of a Diverse Set of Bacteria That Build Their Cell Walls without the Canonical Peptidoglycan Polymerase aPBP

ABSTRACT Peptidoglycan (PG) is a highly cross-linked peptide-glycan mesh that confers structural rigidity and shape to most bacterial cells. Polymerization of new PG is usually achieved by the concerted activity of two membrane-bound machineries, class-A penicillin binding proteins (aPBPs) and class...

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Autores principales:	Sharanjeet Atwal, Suthida Chuenklin, Edward M. Bonder, Juan Flores, Joseph J. Gillespie, Timothy P. Driscoll, Jeanne Salje
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	peptidoglycan penicillin binding proteins Rickettsiales obligate intracellular bacteria endosymbionts orthogonal chemical probes Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e3c8a708b4ba43578dbed7bc6369677f
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spelling	oai:doaj.org-article:e3c8a708b4ba43578dbed7bc6369677f2021-11-10T18:37:51ZDiscovery of a Diverse Set of Bacteria That Build Their Cell Walls without the Canonical Peptidoglycan Polymerase aPBP10.1128/mBio.01342-212150-7511https://doaj.org/article/e3c8a708b4ba43578dbed7bc6369677f2021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01342-21https://doaj.org/toc/2150-7511ABSTRACT Peptidoglycan (PG) is a highly cross-linked peptide-glycan mesh that confers structural rigidity and shape to most bacterial cells. Polymerization of new PG is usually achieved by the concerted activity of two membrane-bound machineries, class-A penicillin binding proteins (aPBPs) and class-B penicillin binding proteins (bPBPs) in complex with shape, elongation, division, and sporulation (SEDS) proteins. Here, we have identified four phylogenetically distinct groups of bacteria that lack any identifiable aPBPs. We performed experiments on a panel of species within one of these groups, the Rickettsiales, and found that bacteria lacking aPBPs build a PG-like cell wall with minimal abundance and rigidity relative to cell walls of aPBP-containing bacteria. This reduced cell wall may have evolved to minimize the activation of host responses to pathogens and endosymbionts while retaining the minimal PG-biosynthesis machinery required for cell elongation and division. We term these “peptidoglycan-intermediate” bacteria, a cohort of host-associated species that includes some human pathogens. IMPORTANCE Peptidoglycan (PG) is a large, cross-linked polymer that forms the cell wall of most bacterial species and confers shape, rigidity, and protection from osmotic shock. It is also a potent stimulator of the immune response in animals. PG is normally polymerized by two groups of enzymes, aPBPs and bPBPs working together with shape, elongation, division, and sporulation (SEDS) proteins. We have identified a diverse set of host-associated bacteria that have selectively lost aPBP genes while retaining bPBP/SEDS and show that some of these build a minimal PG-like structure. It is expected that these minimal cell walls built in the absence of aPBPs improve the evolutionary fitness of host-associated bacteria, potentially through evasion of PG-recognition by the host immune system.Sharanjeet AtwalSuthida ChuenklinEdward M. BonderJuan FloresJoseph J. GillespieTimothy P. DriscollJeanne SaljeAmerican Society for Microbiologyarticlepeptidoglycanpenicillin binding proteinsRickettsialesobligate intracellular bacteriaendosymbiontsorthogonal chemical probesMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	peptidoglycan penicillin binding proteins Rickettsiales obligate intracellular bacteria endosymbionts orthogonal chemical probes Microbiology QR1-502
spellingShingle	peptidoglycan penicillin binding proteins Rickettsiales obligate intracellular bacteria endosymbionts orthogonal chemical probes Microbiology QR1-502 Sharanjeet Atwal Suthida Chuenklin Edward M. Bonder Juan Flores Joseph J. Gillespie Timothy P. Driscoll Jeanne Salje Discovery of a Diverse Set of Bacteria That Build Their Cell Walls without the Canonical Peptidoglycan Polymerase aPBP
description	ABSTRACT Peptidoglycan (PG) is a highly cross-linked peptide-glycan mesh that confers structural rigidity and shape to most bacterial cells. Polymerization of new PG is usually achieved by the concerted activity of two membrane-bound machineries, class-A penicillin binding proteins (aPBPs) and class-B penicillin binding proteins (bPBPs) in complex with shape, elongation, division, and sporulation (SEDS) proteins. Here, we have identified four phylogenetically distinct groups of bacteria that lack any identifiable aPBPs. We performed experiments on a panel of species within one of these groups, the Rickettsiales, and found that bacteria lacking aPBPs build a PG-like cell wall with minimal abundance and rigidity relative to cell walls of aPBP-containing bacteria. This reduced cell wall may have evolved to minimize the activation of host responses to pathogens and endosymbionts while retaining the minimal PG-biosynthesis machinery required for cell elongation and division. We term these “peptidoglycan-intermediate” bacteria, a cohort of host-associated species that includes some human pathogens. IMPORTANCE Peptidoglycan (PG) is a large, cross-linked polymer that forms the cell wall of most bacterial species and confers shape, rigidity, and protection from osmotic shock. It is also a potent stimulator of the immune response in animals. PG is normally polymerized by two groups of enzymes, aPBPs and bPBPs working together with shape, elongation, division, and sporulation (SEDS) proteins. We have identified a diverse set of host-associated bacteria that have selectively lost aPBP genes while retaining bPBP/SEDS and show that some of these build a minimal PG-like structure. It is expected that these minimal cell walls built in the absence of aPBPs improve the evolutionary fitness of host-associated bacteria, potentially through evasion of PG-recognition by the host immune system.
format	article
author	Sharanjeet Atwal Suthida Chuenklin Edward M. Bonder Juan Flores Joseph J. Gillespie Timothy P. Driscoll Jeanne Salje
author_facet	Sharanjeet Atwal Suthida Chuenklin Edward M. Bonder Juan Flores Joseph J. Gillespie Timothy P. Driscoll Jeanne Salje
author_sort	Sharanjeet Atwal
title	Discovery of a Diverse Set of Bacteria That Build Their Cell Walls without the Canonical Peptidoglycan Polymerase aPBP
title_short	Discovery of a Diverse Set of Bacteria That Build Their Cell Walls without the Canonical Peptidoglycan Polymerase aPBP
title_full	Discovery of a Diverse Set of Bacteria That Build Their Cell Walls without the Canonical Peptidoglycan Polymerase aPBP
title_fullStr	Discovery of a Diverse Set of Bacteria That Build Their Cell Walls without the Canonical Peptidoglycan Polymerase aPBP
title_full_unstemmed	Discovery of a Diverse Set of Bacteria That Build Their Cell Walls without the Canonical Peptidoglycan Polymerase aPBP
title_sort	discovery of a diverse set of bacteria that build their cell walls without the canonical peptidoglycan polymerase apbp
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/e3c8a708b4ba43578dbed7bc6369677f
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Discovery of a Diverse Set of Bacteria That Build Their Cell Walls without the Canonical Peptidoglycan Polymerase aPBP

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