Acquired amphotericin B resistance leads to fitness trade-offs that can be mitigated by compensatory evolution in Candida auris

Nat Microbiol. 2024 Dec;9(12):3304-3320. doi: 10.1038/s41564-024-01854-z. Epub 2024 Nov 20.

Abstract

Candida auris is a growing concern due to its resistance to antifungal drugs, particularly amphotericin B (AMB), detected in 30 to 60% of clinical isolates. However, the mechanisms of AMB resistance remain poorly understood. Here we investigated 441 in vitro- and in vivo-evolved C. auris lineages from 4 AMB-susceptible clinical strains of different clades. Genetic and sterol analyses revealed four major types of sterol alterations as a result of clinically rare variations in sterol biosynthesis genes ERG6, NCP1, ERG11, ERG3, HMG1, ERG10 and ERG12. In addition, aneuploidies in chromosomes 4 and 6 emerged during resistance evolution. Fitness trade-off phenotyping and mathematical modelling identified diverse strain- and mechanism-dependent fitness trade-offs. Variation in CDC25 rescued fitness trade-offs, thereby increasing the infection capacity. This possibly contributed to therapy-induced acquired AMB resistance in the clinic. Our findings highlight sterol-modulating mechanisms and fitness trade-off compensation as risks for AMB treatment failure in clinical settings.

MeSH terms

  • Amphotericin B* / pharmacology
  • Aneuploidy
  • Animals
  • Antifungal Agents* / pharmacology
  • Candida auris* / drug effects
  • Candida auris* / genetics
  • Candidiasis* / drug therapy
  • Candidiasis* / microbiology
  • Drug Resistance, Fungal* / genetics
  • Evolution, Molecular
  • Genetic Fitness
  • Humans
  • Microbial Sensitivity Tests*
  • Sterols / metabolism

Substances

  • Amphotericin B
  • Antifungal Agents
  • Sterols