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 inPloS one Vol. 9; no. 9; p. e107015
Main Authors Allan, Raymond N, Skipp, Paul, Jefferies, Johanna, Clarke, Stuart C, Faust, Saul N, Hall-Stoodley, Luanne, Webb, Jeremy
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 04.09.2014
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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.
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
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ContentType Journal Article
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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– notice: 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.
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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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SSID ssj0053866
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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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pubmedcentral
proquest
gale
crossref
pubmed
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
StartPage e107015
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
URI https://www.ncbi.nlm.nih.gov/pubmed/25188255
https://www.proquest.com/docview/1560109246
https://pubmed.ncbi.nlm.nih.gov/PMC4154835
https://doaj.org/article/7ae11d4daa294253b6fbdedfa58e8b99
http://dx.doi.org/10.1371/journal.pone.0107015
Volume 9
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