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. 2008 Sep 30;105(39):15082-7.
doi: 10.1073/pnas.0712019105. Epub 2008 Sep 24.

Role of selection in the emergence of lineages and the evolution of virulence in Neisseria meningitidis

Caroline O Buckee  1 , Keith A Jolley, Mario Recker, Bridget Penman, Paula Kriz, Sunetra Gupta, Martin C J Maiden
Affiliations

Role of selection in the emergence of lineages and the evolution of virulence in Neisseria meningitidis

Caroline O Buckee et al. Proc Natl Acad Sci U S A. .

Abstract

Neisseria meningitis is a human commensal bacterium that occasionally causes life-threatening disease. As with a number of other bacterial pathogens, meningococcal populations comprise distinct lineages, which persist over many decades and during global spread in the face of high rates of recombination. In addition, the propensity to cause invasive disease is associated with particular "hyperinvasive" lineages that coexist with less invasive lineages despite the fact that disease does not contribute to host-to-host transmission. Here, by combining a modeling approach with molecular epidemiological data from 1,108 meningococci isolated in the Czech Republic over 27 years, we show that interstrain competition, mediated by immune selection, can explain both the persistence of multiple discrete meningococcal lineages and the association of a subset of these with invasive disease. The model indicates that the combinations of allelic variants of housekeeping genes that define these lineages are associated with very small differences in transmission efficiency among hosts. These findings have general implications for the emergence of lineage structure and virulence in recombining bacterial populations.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
The observed lifespan, in years, of alleles at each of the seven housekeeping loci (A) and the unique allelic combinations of these loci (B) within the Czech dataset.
Fig. 2.
Fig. 2.
Emergence of lineages. (A) The effects of competition (γ) on the coexistence of allelic combinations or strains, characterized by very small differences in transmission efficiency, within a hypothetical six-locus, two-allele system. The blue bars indicate the range of γ over which each strain can survive, overlaid on these in red is the (smaller) range of γ over which the strain can afford to carry excess virulence. Two features are to be noted: The number of cocirculating strains decreases as competition (γ) for available hosts increases, and fewer of the these strains are able to carry the burden of excess virulence. Parameters used: βi = 1.76 + 0.1·i for strains 1–32, and the converse for strains 33–64; μ = 0.02/yr, σ = 10/yr, αavirulent = 0, αvirulent = 2/yr. (B) The frequency distributions of strain types (now representing lineages caused by the purging of most allele combinations) among disease (brown) and carriage (blue) isolates for an intermediate value of γ (= 0.45). (C) Shown is the contrast between the distribution of clonal complexes among disease (brown) and carriage (blue) isolates obtained in 1993 within the Czech dataset.
Fig. 3.
Fig. 3.
Associations between ST1 (blue) and ST2 (green) with antigenic types ax, bx, ay, and by (representing the various epitope combinations possible within a two-locus, two-allele model) under strong immune selection. The different dynamic outcomes are each ST is uniquely associated with a dominant antigenic type (A), periodic replacement of antigenic type linked to a particular ST (B), and competitive exclusion of one ST (C). In this example, R0 of ST1 = 5, R0 of ST2 = 5.1 (A), 4.3 (B), and 4.05 (C). Other parameters used were: σ = 20.27 yr−1, ς = 2.03 yr−1, γ = 0.97. Population size = 1,000.
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