GtcA is required for LTA glycosylation in Listeria monocytogenes serovar 1/2a and Bacillus subtilis
The cell wall polymers wall teichoic acid (WTA) and lipoteichoic acid (LTA) are often modified with glycosyl and D-alanine residues. Recent studies have shown that a three-component glycosylation system is used for the modification of LTA in several Gram-positive bacteria including Bacillus subtilis...
Main Authors: | , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2020-12-01
|
Series: | The Cell Surface |
Subjects: | |
Online Access: | http://www.sciencedirect.com/science/article/pii/S2468233020300050 |
_version_ | 1818591633163157504 |
---|---|
author | Jeanine Rismondo Talal F.M. Haddad Yang Shen Martin J. Loessner Angelika Gründling |
author_facet | Jeanine Rismondo Talal F.M. Haddad Yang Shen Martin J. Loessner Angelika Gründling |
author_sort | Jeanine Rismondo |
collection | DOAJ |
description | The cell wall polymers wall teichoic acid (WTA) and lipoteichoic acid (LTA) are often modified with glycosyl and D-alanine residues. Recent studies have shown that a three-component glycosylation system is used for the modification of LTA in several Gram-positive bacteria including Bacillus subtilis and Listeria monocytogenes. In the L. monocytogenes 1/2a strain 10403S, the cytoplasmic glycosyltransferase GtlA is thought to use UDP-galactose to produce the C55-P-galactose lipid intermediate, which is transported across the membrane by an unknown flippase. Next, the galactose residue is transferred onto the LTA backbone on the outside of the cell by the glycosyltransferase GtlB. Here we show that GtcA is necessary for the glycosylation of LTA in L. monocytogenes 10403S and B. subtilis 168 and we hypothesize that these proteins act as C55-P-sugar flippases. With this we revealed that GtcA is involved in the glycosylation of both teichoic acid polymers in L. monocytogenes 10403S, namely WTA with N-acetylglucosamine and LTA with galactose residues. These findings indicate that the L. monocytogenes GtcA protein can act on different C55-P-sugar intermediates. Further characterization of GtcA in L. monocytogenes led to the identification of residues essential for its overall function as well as residues, which predominately impact WTA or LTA glycosylation. |
first_indexed | 2024-12-16T10:15:32Z |
format | Article |
id | doaj.art-596c430f90e445a1be782c50458e2f8f |
institution | Directory Open Access Journal |
issn | 2468-2330 |
language | English |
last_indexed | 2024-12-16T10:15:32Z |
publishDate | 2020-12-01 |
publisher | Elsevier |
record_format | Article |
series | The Cell Surface |
spelling | doaj.art-596c430f90e445a1be782c50458e2f8f2022-12-21T22:35:28ZengElsevierThe Cell Surface2468-23302020-12-016100038GtcA is required for LTA glycosylation in Listeria monocytogenes serovar 1/2a and Bacillus subtilisJeanine Rismondo0Talal F.M. Haddad1Yang Shen2Martin J. Loessner3Angelika Gründling4Section of Molecular Microbiology and Medical Research Council Centre for Molecular Bacteriology and Infection, Imperial College London, London SW7 2AZ, United KingdomSection of Molecular Microbiology and Medical Research Council Centre for Molecular Bacteriology and Infection, Imperial College London, London SW7 2AZ, United KingdomInstitute of Food, Nutrition and Health, ETH Zurich, 8092 Zurich, SwitzerlandInstitute of Food, Nutrition and Health, ETH Zurich, 8092 Zurich, SwitzerlandSection of Molecular Microbiology and Medical Research Council Centre for Molecular Bacteriology and Infection, Imperial College London, London SW7 2AZ, United Kingdom; Corresponding author.The cell wall polymers wall teichoic acid (WTA) and lipoteichoic acid (LTA) are often modified with glycosyl and D-alanine residues. Recent studies have shown that a three-component glycosylation system is used for the modification of LTA in several Gram-positive bacteria including Bacillus subtilis and Listeria monocytogenes. In the L. monocytogenes 1/2a strain 10403S, the cytoplasmic glycosyltransferase GtlA is thought to use UDP-galactose to produce the C55-P-galactose lipid intermediate, which is transported across the membrane by an unknown flippase. Next, the galactose residue is transferred onto the LTA backbone on the outside of the cell by the glycosyltransferase GtlB. Here we show that GtcA is necessary for the glycosylation of LTA in L. monocytogenes 10403S and B. subtilis 168 and we hypothesize that these proteins act as C55-P-sugar flippases. With this we revealed that GtcA is involved in the glycosylation of both teichoic acid polymers in L. monocytogenes 10403S, namely WTA with N-acetylglucosamine and LTA with galactose residues. These findings indicate that the L. monocytogenes GtcA protein can act on different C55-P-sugar intermediates. Further characterization of GtcA in L. monocytogenes led to the identification of residues essential for its overall function as well as residues, which predominately impact WTA or LTA glycosylation.http://www.sciencedirect.com/science/article/pii/S2468233020300050Gram-positive bacteriaCell wallLipoteichoic acidWall teichoic acidGlycosylationBactoprenol |
spellingShingle | Jeanine Rismondo Talal F.M. Haddad Yang Shen Martin J. Loessner Angelika Gründling GtcA is required for LTA glycosylation in Listeria monocytogenes serovar 1/2a and Bacillus subtilis The Cell Surface Gram-positive bacteria Cell wall Lipoteichoic acid Wall teichoic acid Glycosylation Bactoprenol |
title | GtcA is required for LTA glycosylation in Listeria monocytogenes serovar 1/2a and Bacillus subtilis |
title_full | GtcA is required for LTA glycosylation in Listeria monocytogenes serovar 1/2a and Bacillus subtilis |
title_fullStr | GtcA is required for LTA glycosylation in Listeria monocytogenes serovar 1/2a and Bacillus subtilis |
title_full_unstemmed | GtcA is required for LTA glycosylation in Listeria monocytogenes serovar 1/2a and Bacillus subtilis |
title_short | GtcA is required for LTA glycosylation in Listeria monocytogenes serovar 1/2a and Bacillus subtilis |
title_sort | gtca is required for lta glycosylation in listeria monocytogenes serovar 1 2a and bacillus subtilis |
topic | Gram-positive bacteria Cell wall Lipoteichoic acid Wall teichoic acid Glycosylation Bactoprenol |
url | http://www.sciencedirect.com/science/article/pii/S2468233020300050 |
work_keys_str_mv | AT jeaninerismondo gtcaisrequiredforltaglycosylationinlisteriamonocytogenesserovar12aandbacillussubtilis AT talalfmhaddad gtcaisrequiredforltaglycosylationinlisteriamonocytogenesserovar12aandbacillussubtilis AT yangshen gtcaisrequiredforltaglycosylationinlisteriamonocytogenesserovar12aandbacillussubtilis AT martinjloessner gtcaisrequiredforltaglycosylationinlisteriamonocytogenesserovar12aandbacillussubtilis AT angelikagrundling gtcaisrequiredforltaglycosylationinlisteriamonocytogenesserovar12aandbacillussubtilis |