Peptidoglycan Association of Murein Lipoprotein Is Required for KpsD-Dependent Group 2 Capsular Polysaccharide Expression and Serum Resistance in a Uropathogenic <italic toggle="yes">Escherichia coli</italic> Isolate

ABSTRACT Murein lipoprotein (Lpp) and peptidoglycan-associated lipoprotein (Pal) are major outer membrane lipoproteins in Escherichia coli. Their roles in cell-envelope integrity have been documented in E. coli laboratory strains, and while Lpp has been linked to serum resistance in vitro, the under...

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Autores principales: Jingyu Diao, Catrien Bouwman, Donghong Yan, Jing Kang, Anand K. Katakam, Peter Liu, Homer Pantua, Alexander R. Abbas, Nicholas N. Nickerson, Cary Austin, Mike Reichelt, Wendy Sandoval, Min Xu, Chris Whitfield, Sharookh B. Kapadia
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Publicado: American Society for Microbiology 2017
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spelling oai:doaj.org-article:749b1c49d18e422d93c20f1e9940a9d92021-11-15T15:51:30ZPeptidoglycan Association of Murein Lipoprotein Is Required for KpsD-Dependent Group 2 Capsular Polysaccharide Expression and Serum Resistance in a Uropathogenic <italic toggle="yes">Escherichia coli</italic> Isolate10.1128/mBio.00603-172150-7511https://doaj.org/article/749b1c49d18e422d93c20f1e9940a9d92017-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00603-17https://doaj.org/toc/2150-7511ABSTRACT Murein lipoprotein (Lpp) and peptidoglycan-associated lipoprotein (Pal) are major outer membrane lipoproteins in Escherichia coli. Their roles in cell-envelope integrity have been documented in E. coli laboratory strains, and while Lpp has been linked to serum resistance in vitro, the underlying mechanism has not been established. Here, lpp and pal mutants of uropathogenic E. coli strain CFT073 showed reduced survival in a mouse bacteremia model, but only the lpp mutant was sensitive to serum killing in vitro. The peptidoglycan-bound Lpp form was specifically required for preventing complement-mediated bacterial lysis in vitro and complement-mediated clearance in vivo. Compared to the wild-type strain, the lpp mutant had impaired K2 capsular polysaccharide production and was unable to respond to exposure to serum by elevating capsular polysaccharide amounts. These properties correlated with altered cellular distribution of KpsD, the predicted outer membrane translocon for “group 2” capsular polysaccharides. We identified a novel Lpp-dependent association between functional KpsD and peptidoglycan, highlighting important interplay between cell envelope components required for resistance to complement-mediated lysis in uropathogenic E. coli isolates. IMPORTANCE Uropathogenic E. coli (UPEC) isolates represent a significant cause of nosocomial urinary tract and bloodstream infections. Many UPEC isolates are resistant to serum killing. Here, we show that a major cell-envelope lipoprotein (murein lipoprotein) is required for serum resistance in vitro and for complement-mediated bacterial clearance in vivo. This is mediated, in part, through a novel mechanism by which murein lipoprotein affects the proper assembly of a key component of the machinery involved in production of “group 2” capsules. The absence of murein lipoprotein results in impaired production of the capsule layer, a known participant in complement resistance. These results demonstrate an important role for murein lipoprotein in complex interactions between different outer membrane biogenesis pathways and further highlight the importance of lipoprotein assembly and transport in bacterial pathogenesis.Jingyu DiaoCatrien BouwmanDonghong YanJing KangAnand K. KatakamPeter LiuHomer PantuaAlexander R. AbbasNicholas N. NickersonCary AustinMike ReicheltWendy SandovalMin XuChris WhitfieldSharookh B. KapadiaAmerican Society for MicrobiologyarticleEscherichia colicapsular polysaccharidecell envelopecomplement resistancemurein lipoproteinpolysaccharide exportMicrobiologyQR1-502ENmBio, Vol 8, Iss 3 (2017)
institution DOAJ
collection DOAJ
language EN
topic Escherichia coli
capsular polysaccharide
cell envelope
complement resistance
murein lipoprotein
polysaccharide export
Microbiology
QR1-502
spellingShingle Escherichia coli
capsular polysaccharide
cell envelope
complement resistance
murein lipoprotein
polysaccharide export
Microbiology
QR1-502
Jingyu Diao
Catrien Bouwman
Donghong Yan
Jing Kang
Anand K. Katakam
Peter Liu
Homer Pantua
Alexander R. Abbas
Nicholas N. Nickerson
Cary Austin
Mike Reichelt
Wendy Sandoval
Min Xu
Chris Whitfield
Sharookh B. Kapadia
Peptidoglycan Association of Murein Lipoprotein Is Required for KpsD-Dependent Group 2 Capsular Polysaccharide Expression and Serum Resistance in a Uropathogenic <italic toggle="yes">Escherichia coli</italic> Isolate
description ABSTRACT Murein lipoprotein (Lpp) and peptidoglycan-associated lipoprotein (Pal) are major outer membrane lipoproteins in Escherichia coli. Their roles in cell-envelope integrity have been documented in E. coli laboratory strains, and while Lpp has been linked to serum resistance in vitro, the underlying mechanism has not been established. Here, lpp and pal mutants of uropathogenic E. coli strain CFT073 showed reduced survival in a mouse bacteremia model, but only the lpp mutant was sensitive to serum killing in vitro. The peptidoglycan-bound Lpp form was specifically required for preventing complement-mediated bacterial lysis in vitro and complement-mediated clearance in vivo. Compared to the wild-type strain, the lpp mutant had impaired K2 capsular polysaccharide production and was unable to respond to exposure to serum by elevating capsular polysaccharide amounts. These properties correlated with altered cellular distribution of KpsD, the predicted outer membrane translocon for “group 2” capsular polysaccharides. We identified a novel Lpp-dependent association between functional KpsD and peptidoglycan, highlighting important interplay between cell envelope components required for resistance to complement-mediated lysis in uropathogenic E. coli isolates. IMPORTANCE Uropathogenic E. coli (UPEC) isolates represent a significant cause of nosocomial urinary tract and bloodstream infections. Many UPEC isolates are resistant to serum killing. Here, we show that a major cell-envelope lipoprotein (murein lipoprotein) is required for serum resistance in vitro and for complement-mediated bacterial clearance in vivo. This is mediated, in part, through a novel mechanism by which murein lipoprotein affects the proper assembly of a key component of the machinery involved in production of “group 2” capsules. The absence of murein lipoprotein results in impaired production of the capsule layer, a known participant in complement resistance. These results demonstrate an important role for murein lipoprotein in complex interactions between different outer membrane biogenesis pathways and further highlight the importance of lipoprotein assembly and transport in bacterial pathogenesis.
format article
author Jingyu Diao
Catrien Bouwman
Donghong Yan
Jing Kang
Anand K. Katakam
Peter Liu
Homer Pantua
Alexander R. Abbas
Nicholas N. Nickerson
Cary Austin
Mike Reichelt
Wendy Sandoval
Min Xu
Chris Whitfield
Sharookh B. Kapadia
author_facet Jingyu Diao
Catrien Bouwman
Donghong Yan
Jing Kang
Anand K. Katakam
Peter Liu
Homer Pantua
Alexander R. Abbas
Nicholas N. Nickerson
Cary Austin
Mike Reichelt
Wendy Sandoval
Min Xu
Chris Whitfield
Sharookh B. Kapadia
author_sort Jingyu Diao
title Peptidoglycan Association of Murein Lipoprotein Is Required for KpsD-Dependent Group 2 Capsular Polysaccharide Expression and Serum Resistance in a Uropathogenic <italic toggle="yes">Escherichia coli</italic> Isolate
title_short Peptidoglycan Association of Murein Lipoprotein Is Required for KpsD-Dependent Group 2 Capsular Polysaccharide Expression and Serum Resistance in a Uropathogenic <italic toggle="yes">Escherichia coli</italic> Isolate
title_full Peptidoglycan Association of Murein Lipoprotein Is Required for KpsD-Dependent Group 2 Capsular Polysaccharide Expression and Serum Resistance in a Uropathogenic <italic toggle="yes">Escherichia coli</italic> Isolate
title_fullStr Peptidoglycan Association of Murein Lipoprotein Is Required for KpsD-Dependent Group 2 Capsular Polysaccharide Expression and Serum Resistance in a Uropathogenic <italic toggle="yes">Escherichia coli</italic> Isolate
title_full_unstemmed Peptidoglycan Association of Murein Lipoprotein Is Required for KpsD-Dependent Group 2 Capsular Polysaccharide Expression and Serum Resistance in a Uropathogenic <italic toggle="yes">Escherichia coli</italic> Isolate
title_sort peptidoglycan association of murein lipoprotein is required for kpsd-dependent group 2 capsular polysaccharide expression and serum resistance in a uropathogenic <italic toggle="yes">escherichia coli</italic> isolate
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/749b1c49d18e422d93c20f1e9940a9d9
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