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"Luis Pedro Coelho"
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Disentangling the impact of environmental and phylogenetic constraints on prokaryotic within-species diversity
Microbial organisms inhabit virtually all environments and encompass a vast biological diversity. The pangenome concept aims to facilitate an understanding of diversity within defined phylogenetic groups. Hence, pangenomes are increasingly used to characterize the strain diversity of prokaryotic species. To understand the interdependence of pangenome features (such as the number of core and accessory genes) and to study the impact of environmental and phylogenetic constraints on the evolution of conspecific strains, we computed pangenomes for 155 phylogenetically diverse species (from ten phyla) using 7,000 high-quality genomes to each of which the respective habitats were assigned. Species habitat ubiquity was associated with several pangenome features. In particular, core-genome size was more important for ubiquity than accessory genome size. In general, environmental preferences had a stronger impact on pangenome evolution than phylogenetic inertia. Environmental preferences explained up to 49% of the variance for pangenome features, compared with 18% by phylogenetic inertia. This observation was robust when the dataset was extended to 10,100 species (59 phyla). The importance of environmental preferences was further accentuated by convergent evolution of pangenome features in a given habitat type across different phylogenetic clades. For example, the soil environment promotes expansion of pangenome size, while host-associated habitats lead to its reduction. Taken together, we explored the global principles of pangenome evolution, quantified the influence of habitat, and phylogenetic inertia on the evolution of pangenomes and identified criteria governing species ubiquity and habitat specificity.
Journal Article
For long-term sustainable software in bioinformatics
The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. In addition to the financial costs, commercial software often lags behind the capabilities of academic software—a natural consequence of the fact that new ideas are often explored first in academia—and commercial software may not be open source, which poses a barrier for some researchers as it can hinder reproducibility. [...]of thumb, taking code from one level to the next requires a 5- to 10-fold increase in coding effort. [...]I consider that conflating these 2 classes of code deliverables (both of which are common in bioinformatics and computational biology) has hampered progress towards higher standards.
Journal Article
Fast Genome-Wide Functional Annotation through Orthology Assignment by eggNOG-Mapper
Orthology assignment is ideally suited for functional inference. However, because predicting orthology is computationally intensive at large scale, and most pipelines are relatively inaccessible (e.g., new assignments only available through database updates), less precise homology-based functional transfer is still the default for (meta-)genome annotation. We, therefore, developed eggNOG-mapper, a tool for functional annotation of large sets of sequences based on fast orthology assignments using precomputed clusters and phylogenies from the eggNOG database. To validate our method, we benchmarked Gene Ontology (GO) predictions against two widely used homology-based approaches: BLAST and InterProScan. Orthology filters applied to BLAST results reduced the rate of false positive assignments by 11%, and increased the ratio of experimentally validated terms recovered over all terms assigned per protein by 15%. Compared with InterProScan, eggNOG-mapper achieved similar proteome coverage and precision while predicting, on average, 41 more terms per protein and increasing the rate of experimentally validated terms recovered over total term assignments per protein by 35%. EggNOG-mapper predictions scored within the top-5 methods in the three GO categories using the CAFA2 NK-partial benchmark. Finally, we evaluated eggNOG-mapper for functional annotation of metagenomics data, yielding better performance than interProScan. eggNOG-mapper runs ∼15× faster than BLAST and at least 2.5× faster than InterProScan. The tool is available standalone and as an online service at http://eggnog-mapper.embl.de.
Journal Article
A deep siamese neural network improves metagenome-assembled genomes in microbiome datasets across different environments
Metagenomic binning is the step in building metagenome-assembled genomes (MAGs) when sequences predicted to originate from the same genome are automatically grouped together. The most widely-used methods for binning are reference-independent, operating de novo and enable the recovery of genomes from previously unsampled clades. However, they do not leverage the knowledge in existing databases. Here, we introduce SemiBin, an open source tool that uses deep siamese neural networks to implement a semi-supervised approach, i.e. SemiBin exploits the information in reference genomes, while retaining the capability of reconstructing high-quality bins that are outside the reference dataset. Using simulated and real microbiome datasets from several different habitats from GMGCv1 (Global Microbial Gene Catalog), including the human gut, non-human guts, and environmental habitats (ocean and soil), we show that SemiBin outperforms existing state-of-the-art binning methods. In particular, compared to other methods, SemiBin returns more high-quality bins with larger taxonomic diversity, including more distinct genera and species.
Here, the authors present SemiBin, a siamese deep neural network framework that incorporates information from reference genomes, able to extract better metagenome-assembled genomes (MAGs) in several host-associated and environmental habitats.
Journal Article
GUNC: detection of chimerism and contamination in prokaryotic genomes
Genomes are critical units in microbiology, yet ascertaining quality in prokaryotic genome assemblies remains a formidable challenge. We present GUNC (the Genome UNClutterer), a tool that accurately detects and quantifies genome chimerism based on the lineage homogeneity of individual contigs using a genome’s full complement of genes. GUNC complements existing approaches by targeting previously underdetected types of contamination: we conservatively estimate that 5.7% of genomes in GenBank, 5.2% in RefSeq, and 15–30% of pre-filtered “high-quality” metagenome-assembled genomes in recent studies are undetected chimeras. GUNC provides a fast and robust tool to substantially improve prokaryotic genome quality.
Journal Article
Structure and function of the global topsoil microbiome
Soils harbour some of the most diverse microbiomes on Earth and are essential for both nutrient cycling and carbon storage. To understand soil functioning, it is necessary to model the global distribution patterns and functional gene repertoires of soil microorganisms, as well as the biotic and environmental associations between the diversity and structure of both bacterial and fungal soil communities
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. Here we show, by leveraging metagenomics and metabarcoding of global topsoil samples (189 sites, 7,560 subsamples), that bacterial, but not fungal, genetic diversity is highest in temperate habitats and that microbial gene composition varies more strongly with environmental variables than with geographic distance. We demonstrate that fungi and bacteria show global niche differentiation that is associated with contrasting diversity responses to precipitation and soil pH. Furthermore, we provide evidence for strong bacterial–fungal antagonism, inferred from antibiotic-resistance genes, in topsoil and ocean habitats, indicating the substantial role of biotic interactions in shaping microbial communities. Our results suggest that both competition and environmental filtering affect the abundance, composition and encoded gene functions of bacterial and fungal communities, indicating that the relative contributions of these microorganisms to global nutrient cycling varies spatially.
Metagenomic, chemical and biomass analyses of topsoil samples from around the world reveal spatial and environmental trends in microbial community composition and genetic diversity.
Journal Article
Drivers and determinants of strain dynamics following fecal microbiota transplantation
Fecal microbiota transplantation (FMT) is a therapeutic intervention for inflammatory diseases of the gastrointestinal tract, but its clinical mode of action and subsequent microbiome dynamics remain poorly understood. Here we analyzed metagenomes from 316 FMTs, sampled pre and post intervention, for the treatment of ten different disease indications. We quantified strain-level dynamics of 1,089 microbial species, complemented by 47,548 newly constructed metagenome-assembled genomes. Donor strain colonization and recipient strain resilience were mostly independent of clinical outcomes, but accurately predictable using LASSO-regularized regression models that accounted for host, microbiome and procedural variables. Recipient factors and donor–recipient complementarity, encompassing entire microbial communities to individual strains, were the main determinants of strain population dynamics, providing insights into the underlying processes that shape the post-FMT gut microbiome. Applying an ecology-based framework to our findings indicated parameters that may inform the development of more effective, targeted microbiome therapies in the future, and suggested how patient stratification can be used to enhance donor microbiota colonization or the displacement of recipient microbes in clinical practice.
Understanding the factors underlying colonization of donor microbes in recipients of fecal microbiota transplantation is a necessary first step to aid development of directed approaches that aim to couple colonization to clinical outcomes.
Journal Article
Microbial abundance, activity and population genomic profiling with mOTUs2
Metagenomic sequencing has greatly improved our ability to profile the composition of environmental and host-associated microbial communities. However, the dependency of most methods on reference genomes, which are currently unavailable for a substantial fraction of microbial species, introduces estimation biases. We present an updated and functionally extended tool based on universal (i.e., reference-independent), phylogenetic marker gene (MG)-based operational taxonomic units (mOTUs) enabling the profiling of >7700 microbial species. As more than 30% of them could not previously be quantified at this taxonomic resolution, relative abundance estimates based on mOTUs are more accurate compared to other methods. As a new feature, we show that mOTUs, which are based on essential housekeeping genes, are demonstrably well-suited for quantification of basal transcriptional activity of community members. Furthermore, single nucleotide variation profiles estimated using mOTUs reflect those from whole genomes, which allows for comparing microbial strain populations (e.g., across different human body sites).
Metagenomic analysis based on universal phylogenetic marker gene (MG)-based operational taxonomic units (mOTUs) is a useful strategy, especially for microbial species without reference genomes. Here, the authors develop mOTUs2, an updated and functionally extended profiling tool for microbial abundance, activity and population profiling.
Journal Article
Towards the biogeography of prokaryotic genes
Microbial genes encode the majority of the functional repertoire of life on earth. However, despite increasing efforts in metagenomic sequencing of various habitats
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, little is known about the distribution of genes across the global biosphere, with implications for human and planetary health. Here we constructed a non-redundant gene catalogue of 303 million species-level genes (clustered at 95% nucleotide identity) from 13,174 publicly available metagenomes across 14 major habitats and use it to show that most genes are specific to a single habitat. The small fraction of genes found in multiple habitats is enriched in antibiotic-resistance genes and markers for mobile genetic elements. By further clustering these species-level genes into 32 million protein families, we observed that a small fraction of these families contain the majority of the genes (0.6% of families account for 50% of the genes). The majority of species-level genes and protein families are rare. Furthermore, species-level genes, and in particular the rare ones, show low rates of positive (adaptive) selection, supporting a model in which most genetic variability observed within each protein family is neutral or nearly neutral.
A survey of species-level genes from 13,174 publicly available metagenomes shows that most species-level genes are specific to a single habitat, encode a small number of protein families and are under low positive (adaptive) pressure.
Journal Article