Metabolic specialization drives reduced pathogenicity in Pseudomonas aeruginosa isolates from cystic fibrosis patients

PLoS Biol. 2024 Aug 23;22(8):e3002781. doi: 10.1371/journal.pbio.3002781. eCollection 2024 Aug.

Abstract

Metabolism provides the foundation for all cellular functions. During persistent infections, in adapted pathogenic bacteria metabolism functions radically differently compared with more naïve strains. Whether this is simply a necessary accommodation to the persistence phenotype or if metabolism plays a direct role in achieving persistence in the host is still unclear. Here, we characterize a convergent shift in metabolic function(s) linked with the persistence phenotype during Pseudomonas aeruginosa colonization in the airways of people with cystic fibrosis. We show that clinically relevant mutations in the key metabolic enzyme, pyruvate dehydrogenase, lead to a host-specialized metabolism together with a lower virulence and immune response recruitment. These changes in infection phenotype are mediated by impaired type III secretion system activity and by secretion of the antioxidant metabolite, pyruvate, respectively. Our results show how metabolic adaptations directly impinge on persistence and pathogenicity in this organism.

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Cystic Fibrosis* / microbiology
  • Humans
  • Mutation*
  • Pseudomonas Infections* / microbiology
  • Pseudomonas aeruginosa* / genetics
  • Pseudomonas aeruginosa* / isolation & purification
  • Pseudomonas aeruginosa* / metabolism
  • Pseudomonas aeruginosa* / pathogenicity
  • Pyruvic Acid / metabolism
  • Type III Secretion Systems / genetics
  • Type III Secretion Systems / metabolism
  • Virulence

Substances

  • Type III Secretion Systems
  • Pyruvic Acid
  • Bacterial Proteins

Grants and funding

The work at the Novo Nordisk Foundation Center for Biosustainability is supported by the Novo Nordisk Foundation www.novonordiskfonden.dk (grant number NNF20CC0035580). This work was supported by the UK Cystic Fibrosis Trust www.cysticfibrosis.org.uk (grant number SRC017 - MW, SM, HKJ) and the Independent Research Fund Denmark/Natural Sciences www.dff.dk (grant number 9040-00106B - SM). HKL was supported by the Novo Nordisk Foundation www.novonordiskfonden.dk (Challenge grant NNF19OC0056411). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.