Negative frequency-dependent selection and asymmetrical transformation stabilise multi-strain bacterial population structures

Harrow, Gabrielle L.; Lees, John A.; Hanage, William P.; Lipsitch, Marc; Corander, Jukka; Colijn, Caroline; Croucher, Nicholas J.

doi:10.1038/s41396-020-00867-w

Cited by 22 publications

(20 citation statements)

References 96 publications

(175 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This conclusion is consistent with the results of some individual studies [35,52,53], although not all [29]. Such a result raises the spectre of separately estimating invasiveness for multiple serotypes within the hundreds of known S. pneumoniae strains, many of which are rare in individual populations [35, 86]. However, that such models fit better than those using only strain or serotype as a predictor only implies that neither factor alone determines an isolate’s invasiveness.…”

Section: Discussionsupporting

confidence: 89%

Analysing pneumococcal invasiveness using Bayesian models of pathogen progression rates

Løchen

Truscott

Croucher

2021

Preprint

Self Cite

View full text Add to dashboard Cite

The disease burden attributable to opportunistic pathogens depends on their prevalence in asymptomatic colonisation and the rate at which they progress to cause symptomatic disease. Increases in infections caused by commensals can result from the emergence of “hyperinvasive” strains. Such pathogens can be identified through quantifying progression rates using matched samples of typed microbes from disease cases and healthy carriers. This study describes Bayesian models for analysing such datasets, implemented in an RStan package (https://github.com/nickjcroucher/progressionEstimation). The models converged on stable fits that accurately reproduced observations from meta-analyses of Streptococcus pneumoniae datasets. The estimates of invasiveness, the progression rate from carriage to invasive disease, in cases per carrier per year correlated strongly with the dimensionless values from meta-analysis of odds ratios when sample sizes were large. At smaller sample sizes, the Bayesian models produced more informative estimates. This identified historically rare but high-risk S. pneumoniae serotypes that could be problematic following vaccine-associated disruption of the bacterial population. The package allows for hypothesis testing through model comparisons with Bayes factors. Application to datasets in which strain and serotype information were available for S. pneumoniae found significant evidence for within-strain and within-serotype variation in invasiveness. The heterogeneous geographical distribution of these genotypes is therefore likely to contribute to differences in the impact of vaccination in between locations. Hence genomic surveillance of opportunistic pathogens is crucial for quantifying the effectiveness of public health interventions, and enabling ongoing meta-analyses that can identify new, highly invasive variants.

show abstract

Section: Discussionsupporting

confidence: 89%

Analysing pneumococcal invasiveness using Bayesian models of pathogen progression rates

Løchen

Truscott

Croucher

2021

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…The atypical properties of these large and SNP-dense events underscores the strength of selection for adaptive evolution resulting from clinical interventions relative to naturally-occurring pressures. This suggests there is a continual flow of sequence between related species sharing a niche, which is normally inhibited by outbreeding depression [92], but may enable rapid adaptation following public health interventions against pathogens. Such transfers are sufficiently frequent for resistant genotypes to emerge and spread locally, but particularly successful genotypes, such as PMEN3, can rapidly spread between continents.…”

Section: Discussionmentioning

confidence: 99%

The role of interspecies recombination in the evolution of antibiotic-resistant pneumococci

D'Aeth

Mpg.

McGee

et al. 2021

eLife

Self Cite

View full text Add to dashboard Cite

Multidrug-resistant Streptococcus pneumoniae emerge through the modification of core genome loci through short interspecies homologous recombinations and acquisition of gene cassettes. Both occurred in the otherwise contrasting histories of the antibiotic-resistant S. pneumoniae lineages PMEN3 and PMEN9. A single PMEN3 clade spread globally, evading vaccine-induced immunity through frequent serotype switching, whereas locally-circulating PMEN9 clades independently gained resistance. Both lineages repeatedly integrated Tn916 and Tn1207.1, conferring tetracycline and macrolide resistance respectively, through homologous recombination importing sequences originating in other species. A species-wide dataset found over 100 instances of such interspecific acquisitions of resistance cassettes and flanking homologous arms. Phylodynamic analysis of the most commonly-sampled Tn1207.1 insertion in PMEN9, originating from a commensal and disrupting a competence gene, suggested its expansion across Germany was driven by a high ratio of macrolide-to-β-lactam consumption. Hence selection from antibiotic consumption was sufficient for these atypically large recombinations to overcome species boundaries across the pneumococcal chromosome.

show abstract

“…This consistent species/strain heterogeneity observed in different geographical areas for certain opportunistic pathogens might reflect ephemeral genotypes or the sampling of different local transmission events or microepidemics, although migration and further population diversification, repeated disseminations and local species-wide extinctions also appear to be plausible explanations. The specific gene content of some of these multistrain pathogens is limited, revealing poor adaptation to particular niches but with the ability to repeatedly explore through transiently acquired mobile loci or mobile genetic elements (Harrow et al, 2021).…”

Section: The Keys For Opening New Niches: Mutation Recombination and Horizontal Gene Transfermentioning

confidence: 99%

The Origin of Niches and Species in the Bacterial World

et al. 2021

View full text Add to dashboard Cite

Niches are spaces for the biological units of selection, from cells to complex communities. In a broad sense, “species” are biological units of individuation. Niches do not exist without individual organisms, and every organism has a niche. We use “niche” in the Hutchinsonian sense as an abstraction of a multidimensional environmental space characterized by a variety of conditions, both biotic and abiotic, whose quantitative ranges determine the positive or negative growth rates of the microbial individual, typically a species, but also parts of the communities of species contained in this space. Microbial organisms (“species”) constantly diversify, and such diversification (radiation) depends on the possibility of opening up unexploited or insufficiently exploited niches. Niche exploitation frequently implies “niche construction,” as the colonized niche evolves with time, giving rise to new potential subniches, thereby influencing the selection of a series of new variants in the progeny. The evolution of niches and organisms is the result of reciprocal interacting processes that form a single unified process. Centrifugal microbial diversification expands the limits of the species’ niches while a centripetal or cohesive process occurs simultaneously, mediated by horizontal gene transfers and recombinatorial events, condensing all of the information recovered during the diversifying specialization into “novel organisms” (possible future species), thereby creating a more complex niche, where the selfishness of the new organism(s) establishes a “homeostatic power” limiting the niche’s variation. Once the niche’s full carrying capacity has been reached, reproductive isolation occurs, as no foreign organisms can outcompete the established population/community, thereby facilitating speciation. In the case of individualization-speciation of the microbiota, its contribution to the animal’ gut structure is a type of “niche construction,” the result of crosstalk between the niche (host) and microorganism(s). Lastly, there is a parallelism between the hierarchy of niches and that of microbial individuals. The increasing anthropogenic effects on the biosphere (such as globalization) might reduce the diversity of niches and bacterial individuals, with the potential emergence of highly transmissible multispecialists (which are eventually deleterious) resulting from the homogenization of the microbiosphere, a possibility that should be explored and prevented.

show abstract

Negative frequency-dependent selection and asymmetrical transformation stabilise multi-strain bacterial population structures

Cited by 22 publications

References 96 publications

Analysing pneumococcal invasiveness using Bayesian models of pathogen progression rates

Analysing pneumococcal invasiveness using Bayesian models of pathogen progression rates

The role of interspecies recombination in the evolution of antibiotic-resistant pneumococci

The Origin of Niches and Species in the Bacterial World

Contact Info

Product

Resources

About