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

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...

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Veröffentlicht in:Antimicrobial agents and chemotherapy 2015-12, Vol.59 (12), p.7637-7649
Hauptverfasser: Colicchio, Roberta, Pagliuca, Chiara, Pastore, Gabiria, Cicatiello, Annunziata Gaetana, Pagliarulo, Caterina, Talà, Adelfia, Scaglione, Elena, Sammartino, Josè Camilla, Bucci, Cecilia, Alifano, Pietro, Salvatore, Paola
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container_issue 12
container_start_page 7637
container_title Antimicrobial agents and chemotherapy
container_volume 59
creator Colicchio, Roberta
Pagliuca, Chiara
Pastore, Gabiria
Cicatiello, Annunziata Gaetana
Pagliarulo, Caterina
Talà, Adelfia
Scaglione, Elena
Sammartino, Josè Camilla
Bucci, Cecilia
Alifano, Pietro
Salvatore, Paola
description 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.
doi_str_mv 10.1128/AAC.01746-15
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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. 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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. 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subjects 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
DNA-Directed RNA Polymerases - genetics
DNA-Directed RNA Polymerases - metabolism
Drug Resistance, Multiple, Bacterial
Drug Resistance, Multiple, Bacterial - genetics
Gene Expression Regulation, Bacterial
Genetic Fitness
High-Throughput Nucleotide Sequencing
Humans
Mechanisms of Resistance
Monocytes - drug effects
Monocytes - microbiology
Mutation
Neisseria meningitidis
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
Virulence Factors - genetics
Virulence Factors - metabolism
title Fitness Cost of Rifampin Resistance in Neisseria meningitidis: In Vitro Study of Mechanisms Associated with rpoB H553Y Mutation
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