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Carbon source regulates polysaccharide capsule biosynthesis in Streptococcus pneumoniae.

  • Troxler LJ Institute for Infectious Diseases, Faculty of Medicine, University of Bern, 3001 Bern, Switzerland.
  • Werren JP Institute for Infectious Diseases, Faculty of Medicine, University of Bern, 3001 Bern, Switzerland.
  • Schaffner TO Institute for Infectious Diseases, Faculty of Medicine, University of Bern, 3001 Bern, Switzerland.
  • Mostacci N Institute for Infectious Diseases, Faculty of Medicine, University of Bern, 3001 Bern, Switzerland.
  • Vermathen P Department of BioMedical Research and Radiology, University of Bern and Inselspital, 3012 Bern, Switzerland.
  • Vermathen M Department of Chemistry and Biochemistry, University of Bern, 3012 Bern, Switzerland.
  • Wüthrich D Interfaculty Bioinformatics Unit and Swiss Institute of Bioinformatics, University of Bern, 3012 Bern, Switzerland.
  • Simillion C Interfaculty Bioinformatics Unit and Swiss Institute of Bioinformatics, University of Bern, 3012 Bern, Switzerland.
  • Brugger SD Department of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, University of Zurich, 8091 Zurich, Switzerland.
  • Bruggmann R Interfaculty Bioinformatics Unit and Swiss Institute of Bioinformatics, University of Bern, 3012 Bern, Switzerland.
  • Hathaway LJ Institute for Infectious Diseases, Faculty of Medicine, University of Bern, 3001 Bern, Switzerland.
  • Furrer J Department of Chemistry and Biochemistry, University of Bern, 3012 Bern, Switzerland.
  • Hilty M Institute for Infectious Diseases, Faculty of Medicine, University of Bern, 3001 Bern, Switzerland markus.hilty@ifik.unibe.ch.
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  • 2019-10-10
Published in:
  • The Journal of biological chemistry. - 2019
Streptococcus
Streptococcus pneumoniae
bacterial metabolism
carbohydrate metabolism
exopolysaccharide capsule
fructose
glucose
nuclear magnetic resonance (NMR)
serotype
sucrose
virulence factor
Bacterial Capsules
Carbon
Fructose
Gene Expression Regulation, Bacterial
Glucose
Humans
Pneumococcal Infections
Polysaccharides, Bacterial
Streptococcus pneumoniae
Sucrose
English The exopolysaccharide capsule of Streptococcus pneumoniae is an important virulence factor, but the mechanisms that regulate capsule thickness are not fully understood. Here, we investigated the effects of various exogenously supplied carbohydrates on capsule production and gene expression in several pneumococcal serotypes. Microscopy analyses indicated a near absence of the capsular polysaccharide (CPS) when S. pneumoniae was grown on fructose. Moreover, serotype 7F pneumococci produced much less CPS than strains of other serotypes (6B, 6C, 9V, 15, and 23F) when grown on glucose or sucrose. RNA-sequencing revealed carbon source-dependent regulation of distinct genes of WT strains and capsule-switch mutants of serotypes 6B and 7F, but could not explain the mechanism of capsule thickness regulation. In contrast, 31P NMR of whole-cell extract from capsule-knockout strains (Δcps) clearly revealed the accumulation or absence of capsule precursor metabolites when cells were grown on glucose or fructose, respectively. This finding suggests that fructose uptake mainly results in intracellular fructose 1-phosphate, which is not converted to CPS precursors. In addition, serotype 7F strains accumulated more precursors than did 6B strains, indicating less efficient conversion of precursor metabolites into the CPS in 7F, in line with its thinner capsule. Finally, isotopologue sucrose labeling and NMR analyses revealed that the uptake of the labeled fructose subunit into the capsule is <10% that of glucose. Our findings on the effects of carbon sources on CPS production in different S. pneumoniae serotypes may contribute to a better understanding of pneumococcal diseases and could inform future therapeutic approaches.
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  • English
Open access status
hybrid
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https://sonar.ch/global/documents/185334
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