Accessibility to Peptidoglycan Is Important for the Recognition of Gram-Positive Bacteria in Drosophila

Summary: In Drosophila, it is thought that peptidoglycan recognition proteins (PGRPs) SA and LC structurally discriminate between bacterial peptidoglycans with lysine (Lys) or diaminopimelic (DAP) acid, respectively, thus inducing differential antimicrobial transcription response. Here, we find that...

Full description

Bibliographic Details
Main Authors: Filipa Vaz, Ilias Kounatidis, Gonçalo Covas, Richard M. Parton, Maria Harkiolaki, Ilan Davis, Sergio Raposo Filipe, Petros Ligoxygakis
Format: Article
Language:English
Published: Elsevier 2019-05-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124719305832
id doaj-3702d3a2c90b43d59f71ef43962a4719
record_format Article
spelling doaj-3702d3a2c90b43d59f71ef43962a47192020-11-25T00:20:23ZengElsevierCell Reports2211-12472019-05-0127824802492.e6Accessibility to Peptidoglycan Is Important for the Recognition of Gram-Positive Bacteria in DrosophilaFilipa Vaz0Ilias Kounatidis1Gonçalo Covas2Richard M. Parton3Maria Harkiolaki4Ilan Davis5Sergio Raposo Filipe6Petros Ligoxygakis7Department of Biochemistry, University of Oxford, South Parks Rd., OX1 3QU Oxford, UK; Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Avenida da República, 2780-157 Oeiras, PortugalDepartment of Biochemistry, University of Oxford, South Parks Rd., OX1 3QU Oxford, UK; Diamond Light Source, Ltd., Harwell Science and Innovation Campus, OX11 0DE Didcot, UKInstituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Avenida da República, 2780-157 Oeiras, Portugal; UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, 2829-516 Caparica, PortugalDepartment of Biochemistry, University of Oxford, South Parks Rd., OX1 3QU Oxford, UKDiamond Light Source, Ltd., Harwell Science and Innovation Campus, OX11 0DE Didcot, UKDepartment of Biochemistry, University of Oxford, South Parks Rd., OX1 3QU Oxford, UKInstituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Avenida da República, 2780-157 Oeiras, Portugal; UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, 2829-516 Caparica, Portugal; Corresponding authorDepartment of Biochemistry, University of Oxford, South Parks Rd., OX1 3QU Oxford, UK; Corresponding authorSummary: In Drosophila, it is thought that peptidoglycan recognition proteins (PGRPs) SA and LC structurally discriminate between bacterial peptidoglycans with lysine (Lys) or diaminopimelic (DAP) acid, respectively, thus inducing differential antimicrobial transcription response. Here, we find that accessibility to PG at the cell wall plays a central role in immunity to infection. When wall teichoic acids (WTAs) are genetically removed from S. aureus (Lys type) and Bacillus subtilis (DAP type), thus increasing accessibility, the binding of both PGRPs to either bacterium is increased. PGRP-SA and -LC double mutant flies are more susceptible to infection with both WTA-less bacteria. In addition, WTA-less bacteria grow better in PGRP-SA/-LC double mutant flies. Finally, infection with WTA-less bacteria abolishes any differential activation of downstream antimicrobial transcription. Our results indicate that accessibility to cell wall PG is a major factor in PGRP-mediated immunity and may be the cause for discrimination between classes of pathogens. : It is widely believed that preference in recognition of structural features of bacterial peptidoglycan (PG) drives specificity in the Drosophila antibacterial response. Vaz et al. challenge this dogma by showing that accessibility to PG plays a central role in bacterial sensing and that structural discrimination is much less stringent than previously thought. Keywords: Drosophila, PGRPs, innate immunity, S. aureus, B. subtilis, TagO, peptidoglycanhttp://www.sciencedirect.com/science/article/pii/S2211124719305832
collection DOAJ
language English
format Article
sources DOAJ
author Filipa Vaz
Ilias Kounatidis
Gonçalo Covas
Richard M. Parton
Maria Harkiolaki
Ilan Davis
Sergio Raposo Filipe
Petros Ligoxygakis
spellingShingle Filipa Vaz
Ilias Kounatidis
Gonçalo Covas
Richard M. Parton
Maria Harkiolaki
Ilan Davis
Sergio Raposo Filipe
Petros Ligoxygakis
Accessibility to Peptidoglycan Is Important for the Recognition of Gram-Positive Bacteria in Drosophila
Cell Reports
author_facet Filipa Vaz
Ilias Kounatidis
Gonçalo Covas
Richard M. Parton
Maria Harkiolaki
Ilan Davis
Sergio Raposo Filipe
Petros Ligoxygakis
author_sort Filipa Vaz
title Accessibility to Peptidoglycan Is Important for the Recognition of Gram-Positive Bacteria in Drosophila
title_short Accessibility to Peptidoglycan Is Important for the Recognition of Gram-Positive Bacteria in Drosophila
title_full Accessibility to Peptidoglycan Is Important for the Recognition of Gram-Positive Bacteria in Drosophila
title_fullStr Accessibility to Peptidoglycan Is Important for the Recognition of Gram-Positive Bacteria in Drosophila
title_full_unstemmed Accessibility to Peptidoglycan Is Important for the Recognition of Gram-Positive Bacteria in Drosophila
title_sort accessibility to peptidoglycan is important for the recognition of gram-positive bacteria in drosophila
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2019-05-01
description Summary: In Drosophila, it is thought that peptidoglycan recognition proteins (PGRPs) SA and LC structurally discriminate between bacterial peptidoglycans with lysine (Lys) or diaminopimelic (DAP) acid, respectively, thus inducing differential antimicrobial transcription response. Here, we find that accessibility to PG at the cell wall plays a central role in immunity to infection. When wall teichoic acids (WTAs) are genetically removed from S. aureus (Lys type) and Bacillus subtilis (DAP type), thus increasing accessibility, the binding of both PGRPs to either bacterium is increased. PGRP-SA and -LC double mutant flies are more susceptible to infection with both WTA-less bacteria. In addition, WTA-less bacteria grow better in PGRP-SA/-LC double mutant flies. Finally, infection with WTA-less bacteria abolishes any differential activation of downstream antimicrobial transcription. Our results indicate that accessibility to cell wall PG is a major factor in PGRP-mediated immunity and may be the cause for discrimination between classes of pathogens. : It is widely believed that preference in recognition of structural features of bacterial peptidoglycan (PG) drives specificity in the Drosophila antibacterial response. Vaz et al. challenge this dogma by showing that accessibility to PG plays a central role in bacterial sensing and that structural discrimination is much less stringent than previously thought. Keywords: Drosophila, PGRPs, innate immunity, S. aureus, B. subtilis, TagO, peptidoglycan
url http://www.sciencedirect.com/science/article/pii/S2211124719305832
work_keys_str_mv AT filipavaz accessibilitytopeptidoglycanisimportantfortherecognitionofgrampositivebacteriaindrosophila
AT iliaskounatidis accessibilitytopeptidoglycanisimportantfortherecognitionofgrampositivebacteriaindrosophila
AT goncalocovas accessibilitytopeptidoglycanisimportantfortherecognitionofgrampositivebacteriaindrosophila
AT richardmparton accessibilitytopeptidoglycanisimportantfortherecognitionofgrampositivebacteriaindrosophila
AT mariaharkiolaki accessibilitytopeptidoglycanisimportantfortherecognitionofgrampositivebacteriaindrosophila
AT ilandavis accessibilitytopeptidoglycanisimportantfortherecognitionofgrampositivebacteriaindrosophila
AT sergioraposofilipe accessibilitytopeptidoglycanisimportantfortherecognitionofgrampositivebacteriaindrosophila
AT petrosligoxygakis accessibilitytopeptidoglycanisimportantfortherecognitionofgrampositivebacteriaindrosophila
_version_ 1725368001443659776