Imbalance of peptidoglycan biosynthesis alters the cell surface charge of Listeria monocytogenes

The bacterial cell wall is composed of a thick layer of peptidoglycan and cell wall polymers, which are either embedded in the membrane or linked to the peptidoglycan backbone and referred to as lipoteichoic acid (LTA) and wall teichoic acid (WTA), respectively. Modifications of the peptidoglycan or...

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Main Authors: Lisa Maria Schulz, Patricia Rothe, Sven Halbedel, Angelika Gründling, Jeanine Rismondo
Format: Article
Language:English
Published: Elsevier 2022-12-01
Series:The Cell Surface
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2468233022000147
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author Lisa Maria Schulz
Patricia Rothe
Sven Halbedel
Angelika Gründling
Jeanine Rismondo
author_facet Lisa Maria Schulz
Patricia Rothe
Sven Halbedel
Angelika Gründling
Jeanine Rismondo
author_sort Lisa Maria Schulz
collection DOAJ
description The bacterial cell wall is composed of a thick layer of peptidoglycan and cell wall polymers, which are either embedded in the membrane or linked to the peptidoglycan backbone and referred to as lipoteichoic acid (LTA) and wall teichoic acid (WTA), respectively. Modifications of the peptidoglycan or WTA backbone can alter the susceptibility of the bacterial cell towards cationic antimicrobials and lysozyme. The human pathogen Listeria monocytogenes is intrinsically resistant towards lysozyme, mainly due to deacetylation and O-acetylation of the peptidoglycan backbone via PgdA and OatA. Recent studies identified additional factors, which contribute to the lysozyme resistance of this pathogen. One of these is the predicted ABC transporter, EslABC. An eslB mutant is hyper-sensitive towards lysozyme, likely due to the production of thinner and less O-acetylated peptidoglycan. Using a suppressor screen, we show here that suppression of eslB phenotypes could be achieved by enhancing peptidoglycan biosynthesis, reducing peptidoglycan hydrolysis or alterations in WTA biosynthesis and modification. The lack of EslB also leads to a higher negative surface charge, which likely stimulates the activity of peptidoglycan hydrolases and lysozyme. Based on our results, we hypothesize that the portion of cell surface exposed WTA is increased in the eslB mutant due to the thinner peptidoglycan layer and that latter one could be caused by an impairment in UDP-N-acetylglucosamine (UDP-GlcNAc) production or distribution.
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spelling doaj.art-8ef8569a121446128df76266a63d15f72022-12-22T04:40:36ZengElsevierThe Cell Surface2468-23302022-12-018100085Imbalance of peptidoglycan biosynthesis alters the cell surface charge of Listeria monocytogenesLisa Maria Schulz0Patricia Rothe1Sven Halbedel2Angelika Gründling3Jeanine Rismondo4Department of General Microbiology, Institute of Microbiology and Genetics, GZMB, Georg-August University Göttingen, Grisebachstr. 8, 37077 Göttingen, GermanyFG11, Division of Enteropathogenic Bacteria and Legionella, Robert Koch Institute, Burgstraße 37, 38855 Wernigerode, GermanyFG11, Division of Enteropathogenic Bacteria and Legionella, Robert Koch Institute, Burgstraße 37, 38855 Wernigerode, Germany; Institute for Medical Microbiology and Hospital Hygiene, Otto von Guericke University Magdeburg, Leipziger Straße 44, 39120 Magdeburg, GermanySection of Molecular Microbiology and Medical Research Council Centre for Molecular Bacteriology and Infection, Imperial College London, London SW7 2AZ, United KingdomDepartment of General Microbiology, Institute of Microbiology and Genetics, GZMB, Georg-August University Göttingen, Grisebachstr. 8, 37077 Göttingen, Germany; Section of Molecular Microbiology and Medical Research Council Centre for Molecular Bacteriology and Infection, Imperial College London, London SW7 2AZ, United Kingdom; Corresponding author at: Department of General Microbiology, Institute of Microbiology and Genetics, GZMB, Georg-August University Göttingen, Grisebachstr. 8, 37077 Göttingen, Germany.The bacterial cell wall is composed of a thick layer of peptidoglycan and cell wall polymers, which are either embedded in the membrane or linked to the peptidoglycan backbone and referred to as lipoteichoic acid (LTA) and wall teichoic acid (WTA), respectively. Modifications of the peptidoglycan or WTA backbone can alter the susceptibility of the bacterial cell towards cationic antimicrobials and lysozyme. The human pathogen Listeria monocytogenes is intrinsically resistant towards lysozyme, mainly due to deacetylation and O-acetylation of the peptidoglycan backbone via PgdA and OatA. Recent studies identified additional factors, which contribute to the lysozyme resistance of this pathogen. One of these is the predicted ABC transporter, EslABC. An eslB mutant is hyper-sensitive towards lysozyme, likely due to the production of thinner and less O-acetylated peptidoglycan. Using a suppressor screen, we show here that suppression of eslB phenotypes could be achieved by enhancing peptidoglycan biosynthesis, reducing peptidoglycan hydrolysis or alterations in WTA biosynthesis and modification. The lack of EslB also leads to a higher negative surface charge, which likely stimulates the activity of peptidoglycan hydrolases and lysozyme. Based on our results, we hypothesize that the portion of cell surface exposed WTA is increased in the eslB mutant due to the thinner peptidoglycan layer and that latter one could be caused by an impairment in UDP-N-acetylglucosamine (UDP-GlcNAc) production or distribution.http://www.sciencedirect.com/science/article/pii/S2468233022000147Listeria monocytogenesPeptidoglycan biosynthesisLysozymeWall teichoic acid
spellingShingle Lisa Maria Schulz
Patricia Rothe
Sven Halbedel
Angelika Gründling
Jeanine Rismondo
Imbalance of peptidoglycan biosynthesis alters the cell surface charge of Listeria monocytogenes
The Cell Surface
Listeria monocytogenes
Peptidoglycan biosynthesis
Lysozyme
Wall teichoic acid
title Imbalance of peptidoglycan biosynthesis alters the cell surface charge of Listeria monocytogenes
title_full Imbalance of peptidoglycan biosynthesis alters the cell surface charge of Listeria monocytogenes
title_fullStr Imbalance of peptidoglycan biosynthesis alters the cell surface charge of Listeria monocytogenes
title_full_unstemmed Imbalance of peptidoglycan biosynthesis alters the cell surface charge of Listeria monocytogenes
title_short Imbalance of peptidoglycan biosynthesis alters the cell surface charge of Listeria monocytogenes
title_sort imbalance of peptidoglycan biosynthesis alters the cell surface charge of listeria monocytogenes
topic Listeria monocytogenes
Peptidoglycan biosynthesis
Lysozyme
Wall teichoic acid
url http://www.sciencedirect.com/science/article/pii/S2468233022000147
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AT svenhalbedel imbalanceofpeptidoglycanbiosynthesisaltersthecellsurfacechargeoflisteriamonocytogenes
AT angelikagrundling imbalanceofpeptidoglycanbiosynthesisaltersthecellsurfacechargeoflisteriamonocytogenes
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