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Colijn, C.

Publications and source records attributed to Colijn, C..

At least 19 recordsLinked to original sources

Species-specific transformer models of bacterial gene order and content for genomic surveillance tasks

Transformer models enable functionally meaningful representation of complex biological data, such as nucleotide or protein sequences. Existing foundation transformer models are trained on large multi-domain corpuses of unlabelled DNA or protein data, showing unmatched task generalisation. However, these foundation models are often outperformed on domain-specific tasks by models trained on taxonomically-constrained data, such as prokaryote gene annotation. By extension, species-specific transformer models hold promise for targeted analyses, given sufficient training data are available. Epidemiological analysis of bacterial pathogens exemplifies the use case of species-specific transformers, due to the wealth of genome data available, coupled with pathogen-specific analyses carried out during routine and outbreak surveillance. Here, we trained a transformer model, PanBART, on the gene content and gene order of two important and biologically distinct bacterial pathogens, Escherichia coli and Streptococcus pneumoniae, benchmarking against state-of-the-art non-transformer approaches for genomic epidemiology. We show PanBART learns representations of population structure in an unsupervised manner, and can be used to accurately assign genomes to biologically-meaningful sequence clusters. PanBART is also able to identify emergent lineages, differentiating them from pre-existing lineages, and can accurately predict genomes likely to uptake genes involved in antibiotic resistance before a transfer event has occurred. Finally, PanBART can be used to conduct co-selection analysis to identify pairs of genes likely to be evolving together. Our work demonstrates that species-specific transformer models can be employed in many critical public health scenarios. We lay the groundwork for wider application of such models in epidemiological analysis, and provide scenarios where such models excel.

bioinformatics↗

An Extended Clade Framework for Annotated Trees in the Context of Phylogeography and Transmission Tree Inference

Bayesian phylogenetic inference produces large samples from a posterior distribution over phylogenetic trees that represents uncertainty in both tree topology and associated variables. Such a collection of trees is hard to interpret and it is common practice to summarize such samples into a single representative tree. Methods for constructing representative trees have largely been restricted to plain tree topologies, encoding only relationships among taxa. Inference with more sophisticated models produce annotated tree objects. These have additional information representing nodes locations in the case of phylogeography, host information when inferring transmission trees, or sampled ancestor status when incorporating fossil information. Nevertheless, these annotated representations are reduced to a single representative tree, typically using methods developed for plain tree topologies and without accounting for the resulting methodological mismatch. Here, we introduce the concept of an extended clade and investigate an extension of the conditional clade distribution (CCD) model. Through motivating examples and case studies in discrete trait phylogeography and transmission tree reconstruction, we demonstrate limitations of standard summary tree approaches and show how these can be addressed using an extended CCD framework that explicitly incorporates the annotated tree structure.

bioinformatics↗

A reusable model of pangenome selection informs optimal surveillance strategies over vaccine introductions

BackgroundThe human pathogen Streptococcus pneumoniae is a major cause of disease, including pneumonia and meningitis. The introduction of Pneumococcal Conjugate Vaccines (PCVs) initially reduced the burden of disease through a reduction of colonisation by vaccine-targeted serotypes. However, since PCVs only target a proportion of pneumococcal serotypes, they shift intraspecific competition, eventually allowing non-targeted types to replace vaccine types. Understanding the host and pathogen factors causing replacement is important for future vaccine development. Mechanistic understanding of vaccine replacement dynamics is crucial for forecasting and optimisation of genomic surveillance strategies to evaluate realised vaccine effectiveness. MethodsWe developed a mathematical model of the genomic and demographic factors which explain vaccine replacement, used this model to replicate serotype-frequency changes, and investigated cost-effective genomic surveillance strategies. We extended a forward-time model based on the Wright-Fisher model, developing a user-friendly model framework that describes the post-vaccine dynamics of S. pneumoniae populations. Our model describes vaccine replacement as a function of vaccine impact, immigration of new strains, and negative frequency-dependent selection (NFDS) on the accessory genome content. ResultsWe used our model to study vaccine replacement in newly sequenced genomic surveillance data from Nepal, and existing data from the US, and the UK, with distinct surveillance strategies. We showed that the model with NFDS better replicates replacement dynamics than a null model without NFDS, and that NFDS likely only acts on part of the S. pneumoniae accessory genome. We found consistent estimates for vaccination effectiveness across the different study locations and country-specific genes under NFDS, highlighting the importance of conducting genomic surveillance in each country of interest. By simulating data from the model, we showed that an optimal surveillance strategy prioritises per-sampling sample size over sampling frequency for small sampling budgets. ConclusionsOur model can be used to predict vaccine replacement dynamics after PCV introduction, and can be easily reapplied to analyse new data from vaccine introductions or new regions. Our model is available in the R package STUBENTIGER (Studying Balancing Evolution (NFDS) To Investigate Genome Replacement) on GitHub https://github.com/bacpop/Stubentiger.

genomics↗

The global phylogeography of rapidly expanding multidrug resistant Ural lineage 4.2 Mycobacterium tuberculosis

Multidrug resistant tuberculosis (MDR-TB) is a leading global health challenge. Recent studies identified a reproductively fit Ural lineage 4.2 MDR M. tuberculosis (Mtb) variant circulating within the Republic of Moldova. We searched a large publicly available dataset of [~]200,000 Mtb whole genome sequences and identified a clade of 1604 drug-resistant Mtb sequences harboring conserved resistance-conferring mutations that are closely related to the MDR Mtb variant circulating in Moldova. We identified the Russian Federation as the most likely country of origin for this clade, and we inferred several independent migration events from Russia and Moldova to other former Soviet Republics and several European countries. Using local branching index, we found that this clade is expanding more rapidly than comparable clades of lineage 4.2. This evolutionarily successful strains presence beyond Moldova poses a threat to MDR-TB control, and enhanced surveillance is necessary to reduce the risk of MDR-TB epidemics in the region. FundingThe authors report funding from the National Institutes of Health (R01AI180209, P01AI159402)

microbiology↗

Sampling Aware Ancestral State Inference

In phylogeography, ancestral state inference methods are used to identify the geographic or host species origin of viral or bacterial lineages and reconstruct their transmission histories over time. However, differences in sampling among states can bias these inference methods. We introduce sampling-aware ancestral state inference (SAASI), a method that accounts for sampling differences. Here, we apply SAASI to the multi-host spread of the H5N1 virus in the United States in 2024 and find that the key transmission event from wild birds to cattle is estimated to occur later under lower sampling in wild birds (compared to other species) than when sampling is not accounted for. Using simulation, we find that SAASI infers past viral locations/host species considerably more accurately than standard methods when sampling bias exists, is computationally feasible for large datasets and scales to trees with 100,000 tips.

evolutionary biology↗

The distribution of clade size in a coalescent diversification model

Characterizing the patterns and determinants of biological diversity is a central aim of evolutionary biology. Doing so requires developing expectations for clade size, the relationship between the number of species in a clade and its age, for standard diversification models, such as the coalescent or birth-death process. These expectations are necessary for identifying diversity outliers, specious or depauperate clades in the macroevolutionary context or transmission clusters of particular or little public health concern in the epidemiological context, and for testing alternative diversification hypotheses. Here, we derive a closed-form expression for the distribution of clade sizes under the widely used Kingman coalescent diversification model and extend the results to allow the number of niches (the effective population size) to vary through time. This result complements analogous results for the birth-death model in that it provides expectations for the joint distribution of clade sizes for a case where diversification is strongly density-dependent.

genetics↗

Taking a BREATH (Bayesian Reconstruction and Evolutionary Analysis of Transmission Histories) to simultaneously infer phylogenetic and transmission trees for partially sampled outbreaks

We introduce and apply Bayesian Reconstruction and Evolutionary Analysis of Transmission Histories (BREATH), a method to simultaneously construct phylogenetic trees and transmission trees using sequence data for a host-to-host outbreak. BREATHs transmission process that accounts for a flexible natural history of infection (including a latent period if desired) and a separate process for sampling. It allows for unsampled individuals and within-host evolution. It also accounts for the fact that an outbreak may still be ongoing at the time of analysis, using right truncation adjustment. We perform a simulation study to verify our implementation and explore sensitivity to unknown or misspecified parameters. We then apply BREATH to a previously-described 13-year outbreak of tuberculosis. We find that using a transmission process to inform the phylogenetic reconstruction results in better resolution of the phylogeny (in topology, branch length and tree height) and a more precise estimate of the time of origin of the outbreak. Considerable uncertainty remains about transmission events in the outbreak, but our reconstructed transmission network resolves two major waves of transmission consistent with the previously-described epidemiology, estimates the numbers of unsampled individuals, and describes some high-probability transmission pairs. An open source implementation of BREATH is available from https://github.com/rbouckaert/BREATH as the BREATH package to BEAST 2.

evolutionary biology↗

e3SIM: epidemiological-ecological-evolutionary simulation framework for genomic epidemiology

Infectious disease dynamics are driven by the complex interplay of epidemiological, ecological, and evolutionary processes. Accurately modeling these interactions is crucial for understanding pathogen spread and informing public health strategies. However, existing simulators often fail to capture the dynamic interplay between these processes, resulting in oversimplified models that do not fully reflect real-world complexities in which the pathogens genetic evolution dynamically influences disease transmission. We introduce the epidemiological-ecological-evolutionary simulator (e3SIM), an open-source framework that concurrently models the transmission dynamics and molecular evolution of pathogens within a host population while integrating environmental factors. Using an agent-based, discrete-generation, forward-in-time approach, e3SIM incorporates compartmental models, host-population contact networks, and quantitative-trait models for pathogens. This integration allows for realistic simulations of disease spread and pathogen evolution. Key features include a modular and scalable design, flexibility in modeling various epidemiological and population-genetic complexities, incorporation of time-varying environmental factors, and a user-friendly graphical interface. We demonstrate e3SIMs capabilities through simulations of realistic outbreak scenarios with SARS-CoV-2 and Mycobacterium tuberculosis, illustrating its flexibility for studying the genomic epidemiology of diverse pathogen types.

bioinformatics↗

A new method for detecting mixed Mycobacterium tuberculosis infection and reconstructing constituent strains provides insights into transmission

BackgroundMixed infection with multiple strains of the same pathogen in a single host can present clinical and analytical challenges. Whole genome sequence (WGS) data can identify signals of multiple strains in samples, though the precision of previous methods can be improved. Here, we present MixInfect2, a new tool to accurately detect mixed samples from Mycobacterium tuberculosis WGS data. We then evaluate three approaches for reconstructing the underlying mixed constituent strain sequences. This allows these samples to be included in downstream analysis to gain insights into the epidemiology and transmission of mixed infections. MethodsWe employed a Gaussian mixture model to cluster allele frequencies at mixed sites (hSNPs) in each sample to identify signals of multiple strains. Building upon our previous tool, MixInfect, we increased the accuracy of classifying in vitro mixed samples through multiple improvements to the bioinformatic pipeline. Major and minor proportion constituent strains were reconstructed using three approaches and assessed by comparing the estimated sequence to the known constituent strain sequence. Lastly, mixed infections in a real-world Mycobacterium tuberculosis population from Moldova were detected with MixInfect2 and clusters of recent transmission that included major and minor constituent strains were built. ResultsAll 36/36 in vitro mixed and 12/12 non-mixed samples were correctly classified with MixInfect2, and major strain proportions estimated with high accuracy, outperforming previous tools. Reconstructed major strain sequences closely matched the true constituent sequence by taking the allele at the highest frequency at hSNPs, while the best performing approach to reconstruct the minor proportion strain sequence was identifying the closest non-mixed isolate in the same population, though no approach was effective when the minor strain proportion was at 5%. Finally, fewer mixed infections were identified in Moldova than previous estimates (6.6% vs 17.4%) and we found multiple instances where the constituent strains of mixed samples were present in transmission clusters. ConclusionsMixInfect2 accurately detects samples with evidence of mixed infection from WGS data and provides an excellent estimate of the mixture proportions. While there are limitations in reconstructing the constituent strain sequences of mixed samples, we present recommendations for the best approach to include these isolates in further analyses.

genomics↗

Characterising indel diversity in a large Mycobacterium tuberculosis outbreak - implications for transmission reconstruction

Genomic sequencing of Mycobacterium tuberculosis (Mtb), the primary aetiological agent of tuberculosis (TB) in humans, has been used to understand transmission dynamics and reconstruct past outbreaks. Putative transmission events between hosts can be predicted by linking cases with low genomic variation between pathogen strains, though typically only variation in single nucleotide polymorphisms (SNPs) is used to calculate divergence. In highly clonal Mtb populations there can be many strains that appear identical by SNPs, reducing the utility of genomic data to disentangle potential transmission routes in these settings. Small insertions and deletions (indels) are found in high numbers across the Mtb genome and can be an important source of variation to increase the observed diversity in outbreaks. Here, we examine the value of including indels in the transmission reconstruction of a large Mtb outbreak in London, UK, characterised by low levels of SNP diversity between 1998 and 2013. Our results show that including indel polymorphism decreases the number of strains in the outbreak with at least one other identical sequence by 43% compared to using only SNP variation and reduces the size of largest clonal cluster by 53%. Considering both SNPs and indel polymorphisms alters the reconstructed transmission network and decreases likelihood of direct transmission between hosts with variation in indels. This work demonstrates the importance of incorporating indels into Mtb transmission reconstruction and we provide recommendations for further work to optimise the inclusion of indel diversity in such analyses.

genomics↗

Estimating Genetic Similarity Matrices using Phylogenies

Genetic similarity is a measure of the genetic relatedness among individuals. The standard method for computing these matrices involves the inner product of observed genetic variants. Such an approach is inaccurate or impossible if genotypes are not available, or not densely sampled, or of poor quality (for example, genetic analysis of extinct species). We provide a new method for computing genetic similarities among individuals using phylogenetic trees. Our method can supplement (or stand in for) computations based on genotypes. We provide simulations suggesting that the genetic similarity matrices computed from trees are consistent with those computed from genotypes. With our methods, quantitative analysis on genetic traits and analysis of heritability and co-heritability can be conducted directly using genetic similarity matrices and so in the absence of genotype data, or under uncertainty in the phylogenetic tree. We use simulation studies to demonstrate the advantages of our method, and we provide applications to data.

genetics↗

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

Streptococcus pneumoniae can be split into multiple strains, each with a characteristic combination of core and accessory genome variation, able to co-circulate and compete within the same hosts. Previous analyses of epidemiological datasets suggested the short-term vaccine-associated dynamics of S. pneumoniae strains may be mediated through multi-locus negative frequency-dependent selection (NFDS), acting to maintain accessory loci at equilibrium frequencies. To test whether this model could explain how such multi-strain populations were generated, it was modified to incorporate recombination. The outputs of simulations featuring symmetrical recombination were compared with genomic data on locus frequencies and distributions between genotypes, pairwise genetic distances and tree shape. These demonstrated NFDS prevented the loss of variation through neutral drift, but generated unstructured populations of diverse isolates. Making recombination asymmetrical, favouring deletion of accessory loci over insertion, alongside multi-locus NFDS significantly improved the fit to genomic data. In a population at equilibrium, structuring into multiple strains was stable due to outbreeding depression, resulting from recombinants with reduced accessory genomes having lower fitness than their parental genotypes. As many bacteria inhibit the integration of insertions into their chromosomes, this combination of asymmetrical recombination and multi-locus NFDS may underlie the co-existence of strains within a single ecological niche.

evolutionary biology↗

Polynomial Phylogenetic Analysis of Tree Shapes

AO_SCPLOWBSTRACTC_SCPLOWPhylogenetic trees are a central tool in evolutionary biology. They demonstrate evolutionary patterns among species, genes, and with modern sequencing technologies, patterns of ancestry among sets of individuals. Phylogenetic trees usually consist of tree shapes, branch lengths and partial labels. Comparing tree shapes is a challenging aspect of comparing phylogenetic trees as there are few tools to describe tree shapes in a quantitative, accurate, comprehensive and easy-to-interpret way. Current methods to compare tree shapes are often based on scalar indices reflecting tree imbalance, and on frequencies of small subtrees. In this paper, we present tree comparisons and applications based on a polynomial that fully characterizes trees. Polynomials are important tools to describe discrete structures and have been used to study various objects including graphs and knots. There are also polynomials that describe rooted trees. We use tree-defining polynomials to compare tree shapes randomly generated by simulations and tree shapes reconstructed from data. Moreover, we show that the comparisons can be used to estimate parameters and to select the best-fit model that generates specific tree shapes.

systems biology↗

Transmission analysis of a large TB outbreak in London: mathematical modelling study using genomic data

Outbreaks of tuberculosis- such as the large isoniazid-resistant outbreak centered on London, United Kingdom, which originated in 1995- provide excellent opportunities to model transmission of this devastating disease. Transmission chains for tuberculosis are notoriously difficult to ascertain, but mathematical modelling approaches, combined with whole-genome sequencing (WGS) data, have strong potential to contribute to transmission analyses. Using such data, we aimed to reconstruct transmission histories for the outbreak using a Bayesian approach, and to use machine learning techniques with patient-level data to identify the key covariates associated with transmission. By using our transmission reconstruction method that accounts for phylogenetic uncertainty, we are able to identify 24 transmission events with reasonable confidence, 11 of which have zero single nucleotide polymorphism (SNP) distance, and as maximum distance of 3. Patient age, alcohol abuse and history of homelessness were found to be the most important predictors of being credible tuberculosis transmitters.

genomics↗

Genomic variant identification methods alter Mycobacterium tuberculosis transmission inference

Pathogen genomic data are increasingly used to characterize global and local transmission patterns of important human pathogens and to inform public health interventions. Yet there is no current consensus on how to measure genomic variation. We investigated the effects of variant identification approaches on transmission inferences for M. tuberculosis by comparing variants identified by five different groups in the same sequence data from a clonal outbreak. We then measured the performance of commonly used variant calling approaches in recovering variation in a simulated tuberculosis outbreak and tested the effect of applying increasingly stringent filters on transmission inferences and phylogenies. We found that variant calling approaches used by different groups do not recover consistent sets of variants, often leading to conflicting transmission inferences. Further, performance in recovering true outbreak variation varied widely across approaches. Finally, stringent filters rapidly eroded the accuracy of transmission inferences and quality of phylogenies reconstructed from outbreak variation. We conclude that measurements of genetic distance and phylogenetic structure are dependent on variant calling approach. Variant calling algorithms trained upon true sequence data outperform other approaches and enable inclusion of repetitive regions typically excluded from genomic epidemiology studies, maximizing the information gleaned from outbreak genomes.

genomics↗

Designing ecologically-optimised vaccines using population genomics

Streptococcus pneumoniae (the pneumococcus) is a common nasopharyngeal commensal capable of infecting normally sterile anatomical sites, resulting in invasive pneumococcal disease (IPD). Effective vaccines preventing IPD exist, but each of the antigens they contain typically induces protective immunity against only one of the approximately 100 pneumococcal serotypes, which are differentiated by immunogenically-distinct polysaccharide capsules. Serotypes vary in their propensity to cause IPD, quantified as their invasiveness. Vaccines are designed to include serotypes commonly isolated from IPD, but the immunity they induce is sufficiently strong to also eliminate vaccine serotypes from carriage. This enables their replacement by non-vaccine serotypes in the nasopharynx. The emergence of invasive non-vaccine serotypes has undermined some vaccination programmes benefits. Recent advances in genomics and modeling have enabled forecasting of which non-vaccine serotypes will be successful post-vaccination. Here, we demonstrate that vaccines optimised using this framework can minimise IPD and antibiotic-resistant disease more effectively than existing formulations in the model, through mitigating the consequences of serotype replacement. The simulations also demonstrate that tailoring vaccines to the pre-vaccine bacterial population is likely to have a substantial impact on reducing IPD, highlighting the importance of epidemiological data, genomics and ecological models as tools for vaccine design and evaluation.

evolutionary biology↗

Predicting the short-term success of human influenza A variants with machine learning

Seasonal influenza viruses are constantly changing, and produce a different set of circulating strains each season. Small genetic changes can accumulate over time and result in antigenically different viruses; this may prevent the bodys immune system from recognizing those viruses. Due to rapid mutations, in particular in the hemagglutinin gene, seasonal influenza vaccines must be updated frequently. This requires choosing strains to include in the updates to maximize the vaccines benefits, according to estimates of which strains will be circulating in upcoming seasons. This is a challenging prediction task. In this paper we use longitudinally sampled phylogenetic trees based on hemagglutinin sequences from human influenza viruses, together with counts of epitope site polymorphisms in hemagglutinin, to predict which influenza virus strains are likely to be successful. We extract small groups of taxa (subtrees) and use a suite of features of these subtrees as key inputs to the machine learning tools. Using a range of training and testing strategies, including training on H3N2 and testing on H1N1, we find that successful prediction of future expansion of small subtrees is possible from these data, with accuracies of 0.71-0.85 and a classifier area under the curve (AUC) 0.75-0.9.

evolutionary biology↗

Network science inspires novel tree shape statistics

1The shape of phylogenetic trees can be used to gain evolutionary insights. A trees shape specifies the connectivity of a tree, while its branch lengths reflect either the time or genetic distance between branching events; well-known measures of tree shape include the Colless and Sackin imbalance, which describe the asymmetry of a tree. In other contexts, network science has become an important paradigm for describing structural features of networks and using them to understand complex systems, ranging from protein interactions to social systems. Network science is thus a potential source of many novel ways to characterize tree shape, as trees are also networks. Here, we tailor tools from network science, including diameter, average path length, and betweenness, closeness, and eigenvector centrality, to summarize phylogenetic tree shapes. We thereby propose tree shape summaries that are complementary to both asymmetry and the frequencies of small configurations. These new statistics can be computed in linear time and scale well to describe the shapes of large trees. We apply these statistics, alongside some conventional tree statistics, to phylogenetic trees from three very different viruses (HIV, dengue fever and measles), from the same virus in different epidemiological scenarios (influenza A and HIV) and from simulation models known to produce trees with different shapes. Using mutual information and supervised learning algorithms, we find that the statistics adapted from network science perform as well as or better than conventional statistics. We describe their distributions and prove some basic results about their extreme values in a tree. We conclude that network science-based tree shape summaries are a promising addition to the toolkit of tree shape features. All our shape summaries, as well as functions to select the most discriminating ones for two sets of trees, are freely available as an R package at http://github.com/Leonardini/treeCentrality.

bioinformatics↗