Pronounced metabolic changes in adaptation to biofilm growth by Streptococcus pneumoniae

PLoS One. 2014 Sep 4;9(9):e107015. doi: 10.1371/journal.pone.0107015. eCollection 2014.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological / genetics*
  • Bacterial Adhesion / genetics
  • Bacterial Proteins / genetics*
  • Bacterial Proteins / metabolism
  • Biofilms / growth & development*
  • Gene Expression Profiling
  • Gene Expression Regulation, Bacterial*
  • Genotype
  • Metabolic Networks and Pathways / genetics
  • Molecular Sequence Annotation
  • Phenotype
  • Plankton / genetics
  • Plankton / metabolism
  • Proteomics
  • Streptococcus pneumoniae / genetics*
  • Streptococcus pneumoniae / metabolism
  • Streptococcus pneumoniae / pathogenicity
  • Virulence

Substances

  • Bacterial Proteins

Grant support

This work was funded by The Bill and Melinda Gates Foundation grant GCE 1006884 (http://www.gatesfoundation.org). Funding was received by JW, SCC, SNF, LHS, and JJ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.