Characterizing the Escherichia coli O157:H7 proteome including protein associations with higher order assemblies.

<h4>Background</h4>The recent outbreak of severe infections with Shiga toxin (Stx) producing Escherichia coli (STEC) serotype O104:H4 highlights the need to understand horizontal gene transfer among E. coli strains, identify novel virulence factors and elucidate their pathogenesis. Quant...

Full description

Saved in:
Bibliographic Details
Main Authors: Rembert Pieper, Quanshun Zhang, David J Clark, Shih-Ting Huang, Moo-Jin Suh, John C Braisted, Samuel H Payne, Robert D Fleischmann, Scott N Peterson, Saul Tzipori
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0026554&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850137725592666112
author Rembert Pieper
Quanshun Zhang
David J Clark
Shih-Ting Huang
Moo-Jin Suh
John C Braisted
Samuel H Payne
Robert D Fleischmann
Scott N Peterson
Saul Tzipori
author_facet Rembert Pieper
Quanshun Zhang
David J Clark
Shih-Ting Huang
Moo-Jin Suh
John C Braisted
Samuel H Payne
Robert D Fleischmann
Scott N Peterson
Saul Tzipori
author_sort Rembert Pieper
collection DOAJ
description <h4>Background</h4>The recent outbreak of severe infections with Shiga toxin (Stx) producing Escherichia coli (STEC) serotype O104:H4 highlights the need to understand horizontal gene transfer among E. coli strains, identify novel virulence factors and elucidate their pathogenesis. Quantitative shotgun proteomics can contribute to such objectives, allowing insights into the part of the genome translated into proteins and the connectivity of biochemical pathways and higher order assemblies of proteins at the subcellular level.<h4>Methodology/principal findings</h4>We examined protein profiles in cell lysate fractions of STEC strain 86-24 (serotype O157:H7), following growth in cell culture or bacterial isolation from intestines of infected piglets, in the context of functionally and structurally characterized biochemical pathways of E. coli. Protein solubilization in the presence of Triton X-100, EDTA and high salt was followed by size exclusion chromatography into the approximate M(r) ranges greater than 280 kDa, 280-80 kDa and 80-10 kDa. Peptide mixtures resulting from these and the insoluble fraction were analyzed by quantitative 2D-LC-nESI-MS/MS. Of the 2521 proteins identified at a 1% false discovery rate, representing 47% of all predicted E. coli O157:H7 gene products, the majority of integral membrane proteins were enriched in the high M(r) fraction. Hundreds of proteins were enriched in a M(r) range higher than that predicted for a monomer supporting their participation in protein complexes. The insoluble STEC fraction revealed enrichment of aggregation-prone proteins, including many that are part of large structure/function entities such as the ribosome, cytoskeleton and O-antigen biosynthesis cluster.<h4>Significance</h4>Nearly all E. coli O157:H7 proteins encoded by prophage regions were expressed at low abundance levels or not detected. Comparative quantitative analyses of proteins from distinct cell lysate fractions allowed us to associate uncharacterized proteins with membrane attachment, potential participation in stable protein complexes, and susceptibility to aggregation as part of larger structural assemblies.
format Article
id doaj-art-7a2f7afcbd084e9187ead2156c882c67
institution OA Journals
issn 1932-6203
language English
publishDate 2011-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj-art-7a2f7afcbd084e9187ead2156c882c672025-08-20T02:30:46ZengPublic Library of Science (PLoS)PLoS ONE1932-62032011-01-01611e2655410.1371/journal.pone.0026554Characterizing the Escherichia coli O157:H7 proteome including protein associations with higher order assemblies.Rembert PieperQuanshun ZhangDavid J ClarkShih-Ting HuangMoo-Jin SuhJohn C BraistedSamuel H PayneRobert D FleischmannScott N PetersonSaul Tzipori<h4>Background</h4>The recent outbreak of severe infections with Shiga toxin (Stx) producing Escherichia coli (STEC) serotype O104:H4 highlights the need to understand horizontal gene transfer among E. coli strains, identify novel virulence factors and elucidate their pathogenesis. Quantitative shotgun proteomics can contribute to such objectives, allowing insights into the part of the genome translated into proteins and the connectivity of biochemical pathways and higher order assemblies of proteins at the subcellular level.<h4>Methodology/principal findings</h4>We examined protein profiles in cell lysate fractions of STEC strain 86-24 (serotype O157:H7), following growth in cell culture or bacterial isolation from intestines of infected piglets, in the context of functionally and structurally characterized biochemical pathways of E. coli. Protein solubilization in the presence of Triton X-100, EDTA and high salt was followed by size exclusion chromatography into the approximate M(r) ranges greater than 280 kDa, 280-80 kDa and 80-10 kDa. Peptide mixtures resulting from these and the insoluble fraction were analyzed by quantitative 2D-LC-nESI-MS/MS. Of the 2521 proteins identified at a 1% false discovery rate, representing 47% of all predicted E. coli O157:H7 gene products, the majority of integral membrane proteins were enriched in the high M(r) fraction. Hundreds of proteins were enriched in a M(r) range higher than that predicted for a monomer supporting their participation in protein complexes. The insoluble STEC fraction revealed enrichment of aggregation-prone proteins, including many that are part of large structure/function entities such as the ribosome, cytoskeleton and O-antigen biosynthesis cluster.<h4>Significance</h4>Nearly all E. coli O157:H7 proteins encoded by prophage regions were expressed at low abundance levels or not detected. Comparative quantitative analyses of proteins from distinct cell lysate fractions allowed us to associate uncharacterized proteins with membrane attachment, potential participation in stable protein complexes, and susceptibility to aggregation as part of larger structural assemblies.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0026554&type=printable
spellingShingle Rembert Pieper
Quanshun Zhang
David J Clark
Shih-Ting Huang
Moo-Jin Suh
John C Braisted
Samuel H Payne
Robert D Fleischmann
Scott N Peterson
Saul Tzipori
Characterizing the Escherichia coli O157:H7 proteome including protein associations with higher order assemblies.
PLoS ONE
title Characterizing the Escherichia coli O157:H7 proteome including protein associations with higher order assemblies.
title_full Characterizing the Escherichia coli O157:H7 proteome including protein associations with higher order assemblies.
title_fullStr Characterizing the Escherichia coli O157:H7 proteome including protein associations with higher order assemblies.
title_full_unstemmed Characterizing the Escherichia coli O157:H7 proteome including protein associations with higher order assemblies.
title_short Characterizing the Escherichia coli O157:H7 proteome including protein associations with higher order assemblies.
title_sort characterizing the escherichia coli o157 h7 proteome including protein associations with higher order assemblies
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0026554&type=printable
work_keys_str_mv AT rembertpieper characterizingtheescherichiacolio157h7proteomeincludingproteinassociationswithhigherorderassemblies
AT quanshunzhang characterizingtheescherichiacolio157h7proteomeincludingproteinassociationswithhigherorderassemblies
AT davidjclark characterizingtheescherichiacolio157h7proteomeincludingproteinassociationswithhigherorderassemblies
AT shihtinghuang characterizingtheescherichiacolio157h7proteomeincludingproteinassociationswithhigherorderassemblies
AT moojinsuh characterizingtheescherichiacolio157h7proteomeincludingproteinassociationswithhigherorderassemblies
AT johncbraisted characterizingtheescherichiacolio157h7proteomeincludingproteinassociationswithhigherorderassemblies
AT samuelhpayne characterizingtheescherichiacolio157h7proteomeincludingproteinassociationswithhigherorderassemblies
AT robertdfleischmann characterizingtheescherichiacolio157h7proteomeincludingproteinassociationswithhigherorderassemblies
AT scottnpeterson characterizingtheescherichiacolio157h7proteomeincludingproteinassociationswithhigherorderassemblies
AT saultzipori characterizingtheescherichiacolio157h7proteomeincludingproteinassociationswithhigherorderassemblies