Analysis of the outer membrane proteome and secretome of Bacteroides fragilis reveals a multiplicity of secretion mechanisms

Bacteroides fragilis is a widely distributed member of the human gut microbiome and an opportunistic pathogen. Cell surface molecules produced by this organism likely play important roles in colonization, communication with other microbes, and pathogenicity, but the protein composition of the outer...

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Published inPloS one Vol. 10; no. 2; p. e0117732
Main Authors Wilson, Marlena M, Anderson, D Eric, Bernstein, Harris D
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 06.02.2015
Public Library of Science (PLoS)
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Abstract Bacteroides fragilis is a widely distributed member of the human gut microbiome and an opportunistic pathogen. Cell surface molecules produced by this organism likely play important roles in colonization, communication with other microbes, and pathogenicity, but the protein composition of the outer membrane (OM) and the mechanisms used to transport polypeptides into the extracellular space are poorly characterized. Here we used LC-MS/MS to analyze the OM proteome and secretome of B. fragilis NCTC 9343 grown under laboratory conditions. Of the 229 OM proteins that we identified, 108 are predicted to be lipoproteins, and 61 are predicted to be TonB-dependent transporters. Based on their proximity to genes encoding TonB-dependent transporters, many of the lipoprotein genes likely encode proteins involved in nutrient or small molecule uptake. Interestingly, protease accessibility and biotinylation experiments indicated that an unusually large fraction of the lipoproteins are cell-surface exposed. We also identified three proteins that are members of a novel family of autotransporters, multiple potential type I protein secretion systems, and proteins that appear to be components of a type VI secretion apparatus. The secretome consisted of lipoproteins and other proteins that might be substrates of the putative type I or type VI secretion systems. Our proteomic studies show that B. fragilis differs considerably from well-studied Gram-negative bacteria such as Escherichia coli in both the spectrum of OM proteins that it produces and the range of secretion strategies that it utilizes.
AbstractList Bacteroides fragilis is a widely distributed member of the human gut microbiome and an opportunistic pathogen. Cell surface molecules produced by this organism likely play important roles in colonization, communication with other microbes, and pathogenicity, but the protein composition of the outer membrane (OM) and the mechanisms used to transport polypeptides into the extracellular space are poorly characterized. Here we used LC-MS/MS to analyze the OM proteome and secretome of B. fragilis NCTC 9343 grown under laboratory conditions. Of the 229 OM proteins that we identified, 108 are predicted to be lipoproteins, and 61 are predicted to be TonB-dependent transporters. Based on their proximity to genes encoding TonB-dependent transporters, many of the lipoprotein genes likely encode proteins involved in nutrient or small molecule uptake. Interestingly, protease accessibility and biotinylation experiments indicated that an unusually large fraction of the lipoproteins are cell-surface exposed. We also identified three proteins that are members of a novel family of autotransporters, multiple potential type I protein secretion systems, and proteins that appear to be components of a type VI secretion apparatus. The secretome consisted of lipoproteins and other proteins that might be substrates of the putative type I or type VI secretion systems. Our proteomic studies show that B. fragilis differs considerably from well-studied Gram-negative bacteria such as Escherichia coli in both the spectrum of OM proteins that it produces and the range of secretion strategies that it utilizes.
Bacteroides fragilis is a widely distributed member of the human gut microbiome and an opportunistic pathogen. Cell surface molecules produced by this organism likely play important roles in colonization, communication with other microbes, and pathogenicity, but the protein composition of the outer membrane (OM) and the mechanisms used to transport polypeptides into the extracellular space are poorly characterized. Here we used LC-MS/MS to analyze the OM proteome and secretome of B. fragilis NCTC 9343 grown under laboratory conditions. Of the 229 OM proteins that we identified, 108 are predicted to be lipoproteins, and 61 are predicted to be TonB-dependent transporters. Based on their proximity to genes encoding TonB-dependent transporters, many of the lipoprotein genes likely encode proteins involved in nutrient or small molecule uptake. Interestingly, protease accessibility and biotinylation experiments indicated that an unusually large fraction of the lipoproteins are cell-surface exposed. We also identified three proteins that are members of a novel family of autotransporters, multiple potential type I protein secretion systems, and proteins that appear to be components of a type VI secretion apparatus. The secretome consisted of lipoproteins and other proteins that might be substrates of the putative type I or type VI secretion systems. Our proteomic studies show that B. fragilis differs considerably from well-studied Gram-negative bacteria such as Escherichia coli in both the spectrum of OM proteins that it produces and the range of secretion strategies that it utilizes.
Audience Academic
Author Anderson, D Eric
Wilson, Marlena M
Bernstein, Harris D
AuthorAffiliation 1 Genetics and Biochemistry Branch, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, United States of America
2 Advanced Mass Spectrometry Facility, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, United States of America
AuthorAffiliation_xml – name: 2 Advanced Mass Spectrometry Facility, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, United States of America
– name: 1 Genetics and Biochemistry Branch, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, United States of America
Author_xml – sequence: 1
  givenname: Marlena M
  surname: Wilson
  fullname: Wilson, Marlena M
  organization: Genetics and Biochemistry Branch, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, United States of America
– sequence: 2
  givenname: D Eric
  surname: Anderson
  fullname: Anderson, D Eric
  organization: Advanced Mass Spectrometry Facility, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, United States of America
– sequence: 3
  givenname: Harris D
  surname: Bernstein
  fullname: Bernstein, Harris D
  organization: Genetics and Biochemistry Branch, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, United States of America
BackLink https://www.ncbi.nlm.nih.gov/pubmed/25658944$$D View this record in MEDLINE/PubMed
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Competing Interests: The authors have declared that no competing interests exist.
Conceived and designed the experiments: MMW HDB. Performed the experiments: MMW DEA. Analyzed the data: MMW DEA HDB. Contributed reagents/materials/analysis tools: MMW DEA. Wrote the paper: MMW DEA HDB.
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PublicationDateYYYYMMDD 2015-02-06
PublicationDate_xml – month: 02
  year: 2015
  text: 2015-02-06
  day: 06
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: San Francisco
– name: San Francisco, CA USA
PublicationTitle PloS one
PublicationTitleAlternate PLoS One
PublicationYear 2015
Publisher Public Library of Science
Public Library of Science (PLoS)
Publisher_xml – sequence: 0
  name: Public Library of Science (PLoS)
– name: Public Library of Science
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Snippet Bacteroides fragilis is a widely distributed member of the human gut microbiome and an opportunistic pathogen. Cell surface molecules produced by this organism...
Bacteroides fragilis is a widely distributed member of the human gut microbiome and an opportunistic pathogen. Cell surface molecules produced by this organism...
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SubjectTerms Analysis
Bacterial Outer Membrane Proteins - biosynthesis
Bacterial Outer Membrane Proteins - genetics
Bacterial Secretion Systems - physiology
Bacteroides
Bacteroides fragilis
Bacteroides fragilis - genetics
Bacteroides fragilis - metabolism
Bacteroidetes
Biochemistry
Biotinylation
Blood lipids
Cell surface
Colonization
Diabetes
E coli
Escherichia coli
Genes
Genomes
Gram-negative bacteria
Humans
Intestinal microflora
Kidney diseases
Lipoproteins
Metabolism
Microbiomes
Molecular chains
Nutrient uptake
Opportunist infection
Pathogenicity
Pathogens
Polypeptides
Proteases
Protein composition
Proteins
Proteobacteria
Proteome - biosynthesis
Proteome - genetics
Proteomics
Secretion
Secretome
Substrates
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Title Analysis of the outer membrane proteome and secretome of Bacteroides fragilis reveals a multiplicity of secretion mechanisms
URI https://www.ncbi.nlm.nih.gov/pubmed/25658944
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http://dx.doi.org/10.1371/journal.pone.0117732
Volume 10
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