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Pronounced metabolic changes in adaptation to biofilm growth by Streptococcus pneumoniae

Pronounced metabolic changes in adaptation to biofilm growth by Streptococcus pneumoniae
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 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.

Adaptation, Physiological, Bacterial Adhesion, Bacterial Proteins, Biofilms, Gene Expression Profiling, Gene Expression Regulation, Bacterial, Genotype, Metabolic Networks and Pathways, Molecular Sequence Annotation, Phenotype, Plankton, Proteomics, Streptococcus pneumoniae, Virulence, Journal Article, Research Support, Non-U.S. Gov't
1932-6203
1-13
Allan, Raymond N
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Skipp, Paul
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Jefferies, Johanna
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Clarke, Stuart C
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Faust, Saul N
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Hall-Stoodley, Luanne
94ebdc00-b549-4488-b15f-5310fb965f5b
Webb, Jeremy
1ecadf17-c81c-48ae-b761-b2c1d03a5e89
Allan, Raymond N
390a7d0a-38e1-410a-8dfe-c8ef8408f5e1
Skipp, Paul
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Jefferies, Johanna
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Clarke, Stuart C
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Faust, Saul N
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Hall-Stoodley, Luanne
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Webb, Jeremy
1ecadf17-c81c-48ae-b761-b2c1d03a5e89

Allan, Raymond N, Skipp, Paul, Jefferies, Johanna, Clarke, Stuart C, Faust, Saul N, Hall-Stoodley, Luanne and Webb, Jeremy (2014) Pronounced metabolic changes in adaptation to biofilm growth by Streptococcus pneumoniae. PLoS ONE, 9 (9), 1-13. (doi:10.1371/journal.pone.0107015).

Record type: Article

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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journal.pone.0107015 - Version of Record
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More information

Accepted/In Press date: 5 August 2014
e-pub ahead of print date: 4 September 2014
Published date: 4 September 2014
Keywords: Adaptation, Physiological, Bacterial Adhesion, Bacterial Proteins, Biofilms, Gene Expression Profiling, Gene Expression Regulation, Bacterial, Genotype, Metabolic Networks and Pathways, Molecular Sequence Annotation, Phenotype, Plankton, Proteomics, Streptococcus pneumoniae, Virulence, Journal Article, Research Support, Non-U.S. Gov't
Organisations: Clinical & Experimental Sciences

Identifiers

Local EPrints ID: 406421
URI: https://eprints.soton.ac.uk/id/eprint/406421
ISSN: 1932-6203
PURE UUID: 10c595eb-3d37-4950-96ce-a59cf7fbb828
ORCID for Paul Skipp: ORCID iD orcid.org/0000-0002-2995-2959
ORCID for Stuart C Clarke: ORCID iD orcid.org/0000-0002-7009-1548
ORCID for Saul N Faust: ORCID iD orcid.org/0000-0003-3410-7642

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Date deposited: 10 Mar 2017 10:46
Last modified: 12 Nov 2019 02:03

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