Quantitative Analyses Reveal Novel Roles for <italic toggle="yes">N-</italic>Glycosylation in a Major Enteric Bacterial Pathogen

ABSTRACT In eukaryotes, glycosylation plays a role in proteome stability, protein quality control, and modulating protein function; however, similar studies in bacteria are lacking. Here, we investigate the roles of general protein glycosylation systems in bacteria using the enteropathogen Campyloba...

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Autores principales:	Sherif Abouelhadid, Simon J. North, Paul Hitchen, Prerna Vohra, Cosmin Chintoan-Uta, Mark Stevens, Anne Dell, Jon Cuccui, Brendan W. Wren
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	glycosylation host-microbe interaction microbial physiology pathogenesis proteomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0d0372c0457a437f9746456acb366609
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spelling	oai:doaj.org-article:0d0372c0457a437f9746456acb3666092021-11-15T15:55:25ZQuantitative Analyses Reveal Novel Roles for <italic toggle="yes">N-</italic>Glycosylation in a Major Enteric Bacterial Pathogen10.1128/mBio.00297-192150-7511https://doaj.org/article/0d0372c0457a437f9746456acb3666092019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00297-19https://doaj.org/toc/2150-7511ABSTRACT In eukaryotes, glycosylation plays a role in proteome stability, protein quality control, and modulating protein function; however, similar studies in bacteria are lacking. Here, we investigate the roles of general protein glycosylation systems in bacteria using the enteropathogen Campylobacter jejuni as a well-defined example. By using a quantitative proteomic strategy, we were able to monitor changes in the C. jejuni proteome when glycosylation is disrupted. We demonstrate that in C. jejuni, N-glycosylation is essential to maintain proteome stability and protein quality control. These findings guided us to investigate the role of N-glycosylation in modulating bacterial cellular activities. In glycosylation-deficient C. jejuni, the multidrug efflux pump and electron transport pathways were significantly impaired. We demonstrate that in vivo, fully glycosylation-deficient C. jejuni bacteria were unable to colonize its natural avian host. These results provide the first evidence of a link between proteome stability and complex functions via a bacterial general glycosylation system. IMPORTANCE Advances in genomics and mass spectrometry have revealed several types of glycosylation systems in bacteria. However, why bacterial proteins are modified remains poorly defined. Here, we investigated the role of general N-linked glycosylation in a major food poisoning bacterium, Campylobacter jejuni. The aim of this study is to delineate the direct and indirect effects caused by disrupting this posttranslational modification. To achieve this, we employed a quantitative proteomic strategy to monitor alterations in the C. jejuni proteome. Our quantitative proteomic results linked general protein N-glycosylation to maintaining proteome stability. Functional analyses revealed novel roles for bacterial N-glycosylation in modulating multidrug efflux pump, enhancing nitrate reduction activity, and promoting host-microbe interaction. This work provides insights on the importance of general glycosylation in proteins in maintaining bacterial physiology, thus expanding our knowledge of the emergence of posttranslational modification in bacteria.Sherif AbouelhadidSimon J. NorthPaul HitchenPrerna VohraCosmin Chintoan-UtaMark StevensAnne DellJon CuccuiBrendan W. WrenAmerican Society for Microbiologyarticleglycosylationhost-microbe interactionmicrobial physiologypathogenesisproteomicsMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	glycosylation host-microbe interaction microbial physiology pathogenesis proteomics Microbiology QR1-502
spellingShingle	glycosylation host-microbe interaction microbial physiology pathogenesis proteomics Microbiology QR1-502 Sherif Abouelhadid Simon J. North Paul Hitchen Prerna Vohra Cosmin Chintoan-Uta Mark Stevens Anne Dell Jon Cuccui Brendan W. Wren Quantitative Analyses Reveal Novel Roles for <italic toggle="yes">N-</italic>Glycosylation in a Major Enteric Bacterial Pathogen
description	ABSTRACT In eukaryotes, glycosylation plays a role in proteome stability, protein quality control, and modulating protein function; however, similar studies in bacteria are lacking. Here, we investigate the roles of general protein glycosylation systems in bacteria using the enteropathogen Campylobacter jejuni as a well-defined example. By using a quantitative proteomic strategy, we were able to monitor changes in the C. jejuni proteome when glycosylation is disrupted. We demonstrate that in C. jejuni, N-glycosylation is essential to maintain proteome stability and protein quality control. These findings guided us to investigate the role of N-glycosylation in modulating bacterial cellular activities. In glycosylation-deficient C. jejuni, the multidrug efflux pump and electron transport pathways were significantly impaired. We demonstrate that in vivo, fully glycosylation-deficient C. jejuni bacteria were unable to colonize its natural avian host. These results provide the first evidence of a link between proteome stability and complex functions via a bacterial general glycosylation system. IMPORTANCE Advances in genomics and mass spectrometry have revealed several types of glycosylation systems in bacteria. However, why bacterial proteins are modified remains poorly defined. Here, we investigated the role of general N-linked glycosylation in a major food poisoning bacterium, Campylobacter jejuni. The aim of this study is to delineate the direct and indirect effects caused by disrupting this posttranslational modification. To achieve this, we employed a quantitative proteomic strategy to monitor alterations in the C. jejuni proteome. Our quantitative proteomic results linked general protein N-glycosylation to maintaining proteome stability. Functional analyses revealed novel roles for bacterial N-glycosylation in modulating multidrug efflux pump, enhancing nitrate reduction activity, and promoting host-microbe interaction. This work provides insights on the importance of general glycosylation in proteins in maintaining bacterial physiology, thus expanding our knowledge of the emergence of posttranslational modification in bacteria.
format	article
author	Sherif Abouelhadid Simon J. North Paul Hitchen Prerna Vohra Cosmin Chintoan-Uta Mark Stevens Anne Dell Jon Cuccui Brendan W. Wren
author_facet	Sherif Abouelhadid Simon J. North Paul Hitchen Prerna Vohra Cosmin Chintoan-Uta Mark Stevens Anne Dell Jon Cuccui Brendan W. Wren
author_sort	Sherif Abouelhadid
title	Quantitative Analyses Reveal Novel Roles for <italic toggle="yes">N-</italic>Glycosylation in a Major Enteric Bacterial Pathogen
title_short	Quantitative Analyses Reveal Novel Roles for <italic toggle="yes">N-</italic>Glycosylation in a Major Enteric Bacterial Pathogen
title_full	Quantitative Analyses Reveal Novel Roles for <italic toggle="yes">N-</italic>Glycosylation in a Major Enteric Bacterial Pathogen
title_fullStr	Quantitative Analyses Reveal Novel Roles for <italic toggle="yes">N-</italic>Glycosylation in a Major Enteric Bacterial Pathogen
title_full_unstemmed	Quantitative Analyses Reveal Novel Roles for <italic toggle="yes">N-</italic>Glycosylation in a Major Enteric Bacterial Pathogen
title_sort	quantitative analyses reveal novel roles for <italic toggle="yes">n-</italic>glycosylation in a major enteric bacterial pathogen
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/0d0372c0457a437f9746456acb366609
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Quantitative Analyses Reveal Novel Roles for <italic toggle="yes">N-</italic>Glycosylation in a Major Enteric Bacterial Pathogen

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