Extensive Cell Envelope Modulation Is Associated with Virulence in Brucella abortus
Brucella virulence is linked to components of the cell envelope and tightly connected to the function of the BvrR/BvrS sensory-regulatory system. To quantify the impact of BvrR/BvrS on cell envelope proteins, we performed a label-free mass spectrometry-based proteomic analysis of spontaneously relea...
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Published in | Journal of proteome research Vol. 6; no. 4; pp. 1519 - 1529 |
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Main Authors | , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
American Chemical Society
01.04.2007
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Abstract | Brucella virulence is linked to components of the cell envelope and tightly connected to the function of the BvrR/BvrS sensory-regulatory system. To quantify the impact of BvrR/BvrS on cell envelope proteins, we performed a label-free mass spectrometry-based proteomic analysis of spontaneously released outer membrane fragments from four strains of Brucella abortus (wild type virulent, avirulent bvrR - and bvrS - mutants as well as reconstituted virulent bvrR + (bvrR -/pbvrR + )). We identified 167 differentially expressed proteins, of which 25 were assigned to the outer membrane. Approximately half of the outer membrane proteins decreased in abundance, whereas half increased. Notably, expression of five Omp3 family proteins decreased whereas five lipoproteins increased in the mutant strains. In the periplasmic space, by contrast, approximately 80% of the 60 differentially expressed proteins were increased in at least one avirulent mutant. Periplasmic proteins are primarily involved in substrate uptake and transport, and a uniform increase in this class may indicate a nutritional stress response, possibly a consequence of defective outer membrane function. Virtually all proteins reverted to wild type levels in the reconstituted virulent bvrR + strain. We propose that the wide changes in cell envelope protein expression relate to the markedly avirulent phenotype of bvrR - and bvrS - mutants and that Brucella virulence depends on regulatory networks involving cell envelope and metabolism rather than on discrete virulence factors. This model may be relevant to other α-Proteobacteria harboring BvrR/BvrS orthologous systems known to be essential for parasitism or endosymbiosis. Keywords: Brucella abortus • virulence • outer membrane • periplasm • proteomics |
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AbstractList | Brucella virulence is linked to components of the cell envelope and tightly connected to the function of the BvrR/BvrS sensory-regulatory system. To quantify the impact of BvrR/BvrS on cell envelope proteins, we performed a label-free mass spectrometry-based proteomic analysis of spontaneously released outer membrane fragments from four strains of Brucella abortus (wild type virulent, avirulent bvrR - and bvrS - mutants as well as reconstituted virulent bvrR + (bvrR -/pbvrR + )). We identified 167 differentially expressed proteins, of which 25 were assigned to the outer membrane. Approximately half of the outer membrane proteins decreased in abundance, whereas half increased. Notably, expression of five Omp3 family proteins decreased whereas five lipoproteins increased in the mutant strains. In the periplasmic space, by contrast, approximately 80% of the 60 differentially expressed proteins were increased in at least one avirulent mutant. Periplasmic proteins are primarily involved in substrate uptake and transport, and a uniform increase in this class may indicate a nutritional stress response, possibly a consequence of defective outer membrane function. Virtually all proteins reverted to wild type levels in the reconstituted virulent bvrR + strain. We propose that the wide changes in cell envelope protein expression relate to the markedly avirulent phenotype of bvrR - and bvrS - mutants and that Brucella virulence depends on regulatory networks involving cell envelope and metabolism rather than on discrete virulence factors. This model may be relevant to other α-Proteobacteria harboring BvrR/BvrS orthologous systems known to be essential for parasitism or endosymbiosis. Keywords: Brucella abortus • virulence • outer membrane • periplasm • proteomics Brucella virulence is linked to components of the cell envelope and tightly connected to the function of the BvrR/BvrS sensory-regulatory system. To quantify the impact of BvrR/BvrS on cell envelope proteins, we performed a label-free mass spectrometry-based proteomic analysis of spontaneously released outer membrane fragments from four strains of Brucella abortus (wild type virulent, avirulent bvrR- and bvrS- mutants as well as reconstituted virulent bvrR+ (bvrR-/pbvrR+)). We identified 167 differentially expressed proteins, of which 25 were assigned to the outer membrane. Approximately half of the outer membrane proteins decreased in abundance, whereas half increased. Notably, expression of five Omp3 family proteins decreased whereas five lipoproteins increased in the mutant strains. In the periplasmic space, by contrast, approximately 80% of the 60 differentially expressed proteins were increased in at least one avirulent mutant. Periplasmic proteins are primarily involved in substrate uptake and transport, and a uniform increase in this class may indicate a nutritional stress response, possibly a consequence of defective outer membrane function. Virtually all proteins reverted to wild type levels in the reconstituted virulent bvrR+ strain. We propose that the wide changes in cell envelope protein expression relate to the markedly avirulent phenotype of bvrR- and bvrS- mutants and that Brucella virulence depends on regulatory networks involving cell envelope and metabolism rather than on discrete virulence factors. This model may be relevant to other alpha-Proteobacteria harboring BvrR/BvrS orthologous systems known to be essential for parasitism or endosymbiosis. |
Author | Paquet, Caroline Tian, Mei Butler, Heather Moriyón, Ignacio Chelsky, Daniel Hunter, Joanna Chaves-Olarte, Esteban Kearney, Paul Lamontagne, Julie Paramithiotis, Eustache Schirm, Michael Moreno, Edgardo Hamaidi, Lyes |
Author_xml | – sequence: 1 givenname: Julie surname: Lamontagne fullname: Lamontagne, Julie – sequence: 2 givenname: Heather surname: Butler fullname: Butler, Heather – sequence: 3 givenname: Esteban surname: Chaves-Olarte fullname: Chaves-Olarte, Esteban – sequence: 4 givenname: Joanna surname: Hunter fullname: Hunter, Joanna – sequence: 5 givenname: Michael surname: Schirm fullname: Schirm, Michael – sequence: 6 givenname: Caroline surname: Paquet fullname: Paquet, Caroline – sequence: 7 givenname: Mei surname: Tian fullname: Tian, Mei – sequence: 8 givenname: Paul surname: Kearney fullname: Kearney, Paul – sequence: 9 givenname: Lyes surname: Hamaidi fullname: Hamaidi, Lyes – sequence: 10 givenname: Daniel surname: Chelsky fullname: Chelsky, Daniel – sequence: 11 givenname: Ignacio surname: Moriyón fullname: Moriyón, Ignacio – sequence: 12 givenname: Edgardo surname: Moreno fullname: Moreno, Edgardo – sequence: 13 givenname: Eustache surname: Paramithiotis fullname: Paramithiotis, Eustache |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/17343405$$D View this record in MEDLINE/PubMed |
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Snippet | Brucella virulence is linked to components of the cell envelope and tightly connected to the function of the BvrR/BvrS sensory-regulatory system. To quantify... |
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SubjectTerms | Amino Acid Sequence Bacterial Outer Membrane Proteins - analysis Bacterial Outer Membrane Proteins - metabolism Brucella abortus - genetics Brucella abortus - metabolism Brucella abortus - pathogenicity Models, Biological Molecular Sequence Data Mutation Periplasmic Proteins - analysis Periplasmic Proteins - metabolism Porins - analysis Porins - metabolism Virulence |
Title | Extensive Cell Envelope Modulation Is Associated with Virulence in Brucella abortus |
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