Potentiation of Phase Variation in Multiple Outer-Membrane Proteins During Spread of the Hyperinvasive Neisseria meningitidis Serogroup W ST-11 Lineage

J Infect Dis. 2019 Aug 30;220(7):1109-1117. doi: 10.1093/infdis/jiz275.

Abstract

Background: Since 2009, increases in the incidence of invasive meningococcal disease have occurred in the United Kingdom due to a sublineage of the Neisseria meningitidis serogroup W ST-11 clonal complex (hereafter, the "original UK strain"). In 2013, a descendent substrain (hereafter, the "2013 strain") became the dominant disease-causing variant. Multiple outer-membrane proteins of meningococci are subject to phase-variable switches in expression due to hypermutable simple-sequence repeats. We investigated whether alterations in phase-variable genes may have influenced the relative prevalence of the original UK and 2013 substrains, using multiple disease and carriage isolates.

Methods: Repeat numbers were determined by either bioinformatics analysis of whole-genome sequencing data or polymerase chain reaction amplification and sizing of fragments from genomic DNA extracts. Immunoblotting and sequence-translation analysis was performed to identify expression states.

Results: Significant increases in repeat numbers were detected between the original UK and 2013 strains in genes encoding PorA, NadA, and 2 Opa variants. Invasive and carriage isolates exhibited similar repeat numbers, but the absence of pilC gene expression was frequently associated with disease.

Conclusions: Elevated repeat numbers in outer-membrane protein genes of the 2013 strain are indicative of higher phase-variation rates, suggesting that rapid expansion of this strain was due to a heightened ability to evade host immune responses during transmission and asymptomatic carriage.

Keywords: Neisseria meningitidis; NadA; Opa; phase variation; serogroup W; simple sequence repeat.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adhesins, Bacterial / genetics
  • Bacterial Outer Membrane Proteins / genetics*
  • DNA, Bacterial / analysis
  • Fimbriae Proteins / genetics
  • Gene Expression Regulation, Bacterial
  • Genetic Variation*
  • Meningococcal Infections / epidemiology
  • Meningococcal Infections / microbiology*
  • Microsatellite Repeats / genetics
  • Molecular Epidemiology
  • Neisseria meningitidis / genetics*
  • Porins / genetics
  • Sequence Analysis, DNA
  • Serogroup
  • United Kingdom
  • Whole Genome Sequencing

Substances

  • Adhesins, Bacterial
  • Bacterial Outer Membrane Proteins
  • DNA, Bacterial
  • NadA protein, Neisseria meningitidis
  • Porins
  • porin protein, Neisseria
  • Fimbriae Proteins
  • Opa protein, Neisseria