Fitness Cost of Rifampin Resistance in Neisseria meningitidis: In Vitro Study of Mechanisms Associated with rpoB H553Y Mutation

Antimicrob Agents Chemother. 2015 Dec;59(12):7637-49. doi: 10.1128/AAC.01746-15. Epub 2015 Sep 28.

Abstract

Rifampin chemoprophylaxis against Neisseria meningitidis infections led to the onset of rifampin resistance in clinical isolates harboring point mutations in the rpoB gene, coding for the RNA polymerase β chain. These resistant strains are rare in medical practice, suggesting their decreased fitness in the human host. In this study, we isolated rifampin-resistant rpoB mutants from hypervirulent serogroup C strain 93/4286 and analyzed their different properties, including the ability to grow/survive in different culture media and in differentiated THP-1 human monocytes and to compete with the wild-type strain in vitro. Our results demonstrate that different rpoB mutations (H553Y, H553R, and S549F) may have different effects, ranging from low- to high-cost effects, on bacterial fitness in vitro. Moreover, we found that the S549F mutation confers temperature sensitivity, possibly explaining why it is observed very rarely in clinical isolates. Comparative high-throughput RNA sequencing analysis of bacteria grown in chemically defined medium demonstrated that the low-cost H553Y substitution resulted in global transcriptional changes that functionally mimic the stringent response. Interestingly, many virulence-associated genes, including those coding for meningococcal type IV pili, porin A, adhesins/invasins, IgA protease, two-partner secretion system HrpA/HrpB, enzymes involved in resistance to oxidative injury, lipooligosaccharide sialylation, and capsular polysaccharide biosynthesis, were downregulated in the H553Y mutant compared to their level of expression in the wild-type strain. These data might account for the reduced capacity of this mutant to grow/survive in differentiated THP-1 cells and explain the rarity of H553Y mutants among clinical isolates.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adhesins, Bacterial / genetics
  • Adhesins, Bacterial / metabolism
  • Amino Acid Substitution
  • Anti-Bacterial Agents / pharmacology
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Cell Line
  • Culture Media
  • DNA-Directed RNA Polymerases / genetics*
  • DNA-Directed RNA Polymerases / metabolism
  • Drug Resistance, Multiple, Bacterial / genetics*
  • Gene Expression Regulation, Bacterial*
  • Genetic Fitness*
  • High-Throughput Nucleotide Sequencing
  • Humans
  • Monocytes / drug effects
  • Monocytes / microbiology
  • Mutation
  • Neisseria meningitidis / drug effects
  • Neisseria meningitidis / genetics*
  • Neisseria meningitidis / metabolism
  • Porins / genetics
  • Porins / metabolism
  • Rifampin / pharmacology
  • Serine Endopeptidases / genetics
  • Serine Endopeptidases / metabolism
  • Transcription, Genetic
  • Virulence Factors / genetics*
  • Virulence Factors / metabolism

Substances

  • Adhesins, Bacterial
  • Anti-Bacterial Agents
  • Bacterial Proteins
  • Culture Media
  • HrpA protein, Neisseria meningitidis
  • Porins
  • Virulence Factors
  • porin protein, Neisseria
  • DNA-Directed RNA Polymerases
  • Serine Endopeptidases
  • IgA-specific serine endopeptidase
  • Rifampin