Pronounced metabolic changes in adaptation to biofilm growth by Streptococcus pneumoniae
Streptococcus pneumoniae accounts for a significant global burden of morbidity and mortality and biofilm development is increasingly recognised as important for colonization and infection. Analysis of protein expression patterns during biofilm development may therefore provide valuable insights to t...
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Published in | PloS one Vol. 9; no. 9; p. e107015 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
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United States
Public Library of Science
04.09.2014
Public Library of Science (PLoS) |
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Abstract | Streptococcus pneumoniae accounts for a significant global burden of morbidity and mortality and biofilm development is increasingly recognised as important for colonization and infection. Analysis of protein expression patterns during biofilm development may therefore provide valuable insights to the understanding of pneumococcal persistence strategies and to improve vaccines. iTRAQ (isobaric tagging for relative and absolute quantification), a high-throughput gel-free proteomic approach which allows high resolution quantitative comparisons of protein profiles between multiple phenotypes, was used to interrogate planktonic and biofilm growth in a clinical serotype 14 strain. Comparative analyses of protein expression between log-phase planktonic and 1-day and 7-day biofilm cultures representing nascent and late phase biofilm growth were carried out. Overall, 244 proteins were identified, of which >80% were differentially expressed during biofilm development. Quantitatively and qualitatively, metabolic regulation appeared to play a central role in the adaptation from the planktonic to biofilm phenotype. Pneumococci adapted to biofilm growth by decreasing enzymes involved in the glycolytic pathway, as well as proteins involved in translation, transcription, and virulence. In contrast, proteins with a role in pyruvate, carbohydrate, and arginine metabolism were significantly increased during biofilm development. Downregulation of glycolytic and translational proteins suggests that pneumococcus adopts a covert phenotype whilst adapting to an adherent lifestyle, while utilization of alternative metabolic pathways highlights the resourcefulness of pneumococcus to facilitate survival in diverse environmental conditions. These metabolic proteins, conserved across both the planktonic and biofilm phenotypes, may also represent target candidates for future vaccine development and treatment strategies. Data are available via ProteomeXchange with identifier PXD001182. |
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AbstractList | Streptococcus pneumoniae accounts for a significant global burden of morbidity and mortality and biofilm development is increasingly recognised as important for colonization and infection. Analysis of protein expression patterns during biofilm development may therefore provide valuable insights to the understanding of pneumococcal persistence strategies and to improve vaccines. iTRAQ (isobaric tagging for relative and absolute quantification), a high-throughput gel-free proteomic approach which allows high resolution quantitative comparisons of protein profiles between multiple phenotypes, was used to interrogate planktonic and biofilm growth in a clinical serotype 14 strain. Comparative analyses of protein expression between log-phase planktonic and 1-day and 7-day biofilm cultures representing nascent and late phase biofilm growth were carried out. Overall, 244 proteins were identified, of which >80% were differentially expressed during biofilm development. Quantitatively and qualitatively, metabolic regulation appeared to play a central role in the adaptation from the planktonic to biofilm phenotype. Pneumococci adapted to biofilm growth by decreasing enzymes involved in the glycolytic pathway, as well as proteins involved in translation, transcription, and virulence. In contrast, proteins with a role in pyruvate, carbohydrate, and arginine metabolism were significantly increased during biofilm development. Downregulation of glycolytic and translational proteins suggests that pneumococcus adopts a covert phenotype whilst adapting to an adherent lifestyle, while utilization of alternative metabolic pathways highlights the resourcefulness of pneumococcus to facilitate survival in diverse environmental conditions. These metabolic proteins, conserved across both the planktonic and biofilm phenotypes, may also represent target candidates for future vaccine development and treatment strategies. Data are available via ProteomeXchange with identifier PXD001182. Streptococcus pneumoniae accounts for a significant global burden of morbidity and mortality and biofilm development is increasingly recognised as important for colonization and infection. Analysis of protein expression patterns during biofilm development may therefore provide valuable insights to the understanding of pneumococcal persistence strategies and to improve vaccines. iTRAQ (isobaric tagging for relative and absolute quantification), a high-throughput gel-free proteomic approach which allows high resolution quantitative comparisons of protein profiles between multiple phenotypes, was used to interrogate planktonic and biofilm growth in a clinical serotype 14 strain. Comparative analyses of protein expression between log-phase planktonic and 1-day and 7-day biofilm cultures representing nascent and late phase biofilm growth were carried out. Overall, 244 proteins were identified, of which >80% were differentially expressed during biofilm development. Quantitatively and qualitatively, metabolic regulation appeared to play a central role in the adaptation from the planktonic to biofilm phenotype. Pneumococci adapted to biofilm growth by decreasing enzymes involved in the glycolytic pathway, as well as proteins involved in translation, transcription, and virulence. In contrast, proteins with a role in pyruvate, carbohydrate, and arginine metabolism were significantly increased during biofilm development. Downregulation of glycolytic and translational proteins suggests that pneumococcus adopts a covert phenotype whilst adapting to an adherent lifestyle, while utilization of alternative metabolic pathways highlights the resourcefulness of pneumococcus to facilitate survival in diverse environmental conditions. These metabolic proteins, conserved across both the planktonic and biofilm phenotypes, may also represent target candidates for future vaccine development and treatment strategies. Data are available via ProteomeXchange with identifier PXD001182. |
Audience | Academic |
Author | Jefferies, Johanna Webb, Jeremy Clarke, Stuart C Faust, Saul N Skipp, Paul Allan, Raymond N Hall-Stoodley, Luanne |
AuthorAffiliation | 3 Centre for Biological Sciences, University of Southampton, Southampton, United Kingdom 1 Academic Unit of Clinical and Experimental Sciences, Faculty of Medicine and Institute for Life Sciences, University of Southampton, Southampton, United Kingdom 5 Public Health England, Southampton, United Kingdom 7 Microbial Infection and Immunity, Centre for Microbial Interface Biology, The Ohio State University, Columbus, Ohio, United States of America University of Oklahoma Health Sciences Center, United States of America 4 Centre for Proteomic Research, Institute for Life Sciences, University of Southampton, Southampton, United Kingdom 6 Southampton NIHR Respiratory Biomedical Research Unit, University Hospital Southampton NHS Foundation Trust, Southampton, United Kingdom 2 Southampton NIHR Wellcome Trust Clinical Research Facility, University Hospital Southampton NHS Foundation Trust, Southampton, United Kingdom |
AuthorAffiliation_xml | – name: 3 Centre for Biological Sciences, University of Southampton, Southampton, United Kingdom – name: University of Oklahoma Health Sciences Center, United States of America – name: 2 Southampton NIHR Wellcome Trust Clinical Research Facility, University Hospital Southampton NHS Foundation Trust, Southampton, United Kingdom – name: 1 Academic Unit of Clinical and Experimental Sciences, Faculty of Medicine and Institute for Life Sciences, University of Southampton, Southampton, United Kingdom – name: 7 Microbial Infection and Immunity, Centre for Microbial Interface Biology, The Ohio State University, Columbus, Ohio, United States of America – name: 5 Public Health England, Southampton, United Kingdom – name: 4 Centre for Proteomic Research, Institute for Life Sciences, University of Southampton, Southampton, United Kingdom – name: 6 Southampton NIHR Respiratory Biomedical Research Unit, University Hospital Southampton NHS Foundation Trust, Southampton, United Kingdom |
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Copyright | COPYRIGHT 2014 Public Library of Science 2014 Allan et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2014 Allan et al 2014 Allan et al |
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Notes | Competing Interests: The authors have declared that no competing interests exist. Conceived and designed the experiments: RNA PS JJ SCC SNF LHS JW. Performed the experiments: RNA. Analyzed the data: RNA LHS PS. Contributed reagents/materials/analysis tools: PS JJ SCC SNF LHS JW. Contributed to the writing of the manuscript: RNA PS JJ SCC SNF LHS JW. |
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Snippet | Streptococcus pneumoniae accounts for a significant global burden of morbidity and mortality and biofilm development is increasingly recognised as important... Streptococcus pneumoniae accounts for a significant global burden of morbidity and mortality and biofilm development is increasingly recognised as important... |
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SubjectTerms | Adaptation Adaptation, Physiological - genetics Arginine Bacterial Adhesion - genetics Bacterial Proteins - genetics Bacterial Proteins - metabolism Biofilms Biofilms - growth & development Biology and Life Sciences Biomedical research Carbohydrate metabolism Carbohydrates Colonization Comparative analysis Ear diseases Environmental conditions Gene Expression Profiling Gene Expression Regulation, Bacterial Genotype Glycolysis Growth Health aspects Hospitals Life sciences Medicine Metabolic Networks and Pathways - genetics Metabolic pathways Metabolism Molecular Sequence Annotation Morbidity Phenotype Plankton - genetics Plankton - metabolism Pneumonia Protein expression Proteins Proteomics Public health Pyruvic acid Research and Analysis Methods Streptococcus infections Streptococcus pneumoniae Streptococcus pneumoniae - genetics Streptococcus pneumoniae - metabolism Streptococcus pneumoniae - pathogenicity Tagging Transcription Vaccine development Vaccines Virulence |
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Title | Pronounced metabolic changes in adaptation to biofilm growth by Streptococcus pneumoniae |
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