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Manzano-Morales, S.

Publications and source records attributed to Manzano-Morales, S..

4 recordsLinked to original sources

Phylogenomics of Asgard archaea reveals a unique blend of prokaryotic-like horizontal transfer and eukaryotic-like gene duplication.

Asgard archaea hold a pivotal position in the tree of life as the closest known relatives to eukaryotes and are therefore crucial for understanding eukaryogenesis. Earlier genomic analyses revealed that Asgard genomes are remarkably larger than those of other archaea and contain a significant number of genes seemingly acquired from bacteria. However, the precise contributions of horizontal gene transfer and gene duplication in shaping Asgard genomes remain largely unknown. Here, we present a comprehensive phylogenomic analysis to dissect the evolutionary dynamics of Asgard genomes, quantifying gene duplication, loss, and both inter- and intra-domain gene transfer events. Our findings reveal that gene transfer is widespread throughout Asgard evolution, predominantly affecting metabolic genes at the periphery of interaction networks. However, our analyses demonstrate that gene duplications, rather than horizontal gene transfers, are the primary drivers behind the increased genome sizes observed in Asgard archaea. This unique evolutionary signature in Asgard archaea--a blend of pervasive prokaryotic-like gene transfer alongside significant eukaryotic-like gene duplication--is consistent with their phylogenetic placement and offers novel insights into the genomic transitions that likely underpinned eukaryogenesis.

evolutionary biology↗

Diverse ancestries reveal complex symbiotic interactions during eukaryogenesis

Summary paragraphThe origin of eukaryotes remains a central enigma in biology1. Ongoing debates agree on the pivotal role of a symbiosis between an alphaproteobacterium and an Asgard archaeon2,3. However, the nature, timing and contributions of other potential bacterial partners4-6 or the role of interactions with viruses7-9 remain contentious. To address these questions, we employed advanced phylogenomic approaches and comprehensive datasets spanning the known diversity of cellular life and viruses. Our analysis provided an updated reconstruction of the last eukaryotic common ancestor (LECA) proteome, in which we traced the phylogenetic origin of each protein family. We found compelling evidence for multiple waves of horizontal gene transfer from diverse bacterial donors, with some likely preceding the mitochondrial endosymbiosis. We inferred plausible traits of the major donors and their functional contributions to LECA. Our findings underscore the contribution of horizontal gene transfers in shaping the proteomes of pre-LECA ancestors and hint to a facilitating role of Nucleocytoviricota viruses. Altogether, our results suggest that ancient eukaryotes originated within complex microbial ecosystems through a succession of diverse associations that left a footprint of horizontally transferred genes.

evolutionary biology↗

Phylogeny-aware simulations suggest a low impact of unsampled lineages in the inference of gene flow during eukaryogenesis

Gene phylogenies are broadly used to analyse events of horizontal gene transfer, namely, their presence, the potential donor and acceptor lineages, and their relative timing. Recent phylogenomics analyses have reconstructed a relative chronology of gene acquisitions in the lineage leading to the eukaryotes, revealing waves of acquisition from different donors before and after the mitochondrial endosymbiosis. However, a recognised caveat is the potential biases introduced by the presence of incomplete taxon sampling resulting in so-called "ghost" lineages. Here, we assessed the robustness of the gene phylogeny-based branch length ratio method in the inference of the relative ordering of gene acquisition events during eukaryogenesis. We introduce a novel simulation framework that populates a known dated Tree of Life with plausible "ghost" lineages and simulates their gene transfers to the lineage leading to the last eukaryotic common ancestor. Our simulations suggest a generally low probability of misinterpreting the relative order of gene acquisitions from distinct ghost donors. However, we identify specific problematic phylogenetic placements where unsampled lineages are more likely to produce misleading results. Overall, our approach offers valuable guidance for the interpretation of future work on eukaryogenesis, and can be readily adapted to other evolutionary scenarios.

evolutionary biology↗

Operational Gene Clusters and intrinsic uncertainty in pangenome analyses

BackgroundA key step for comparative genomics is to group open reading frames into functionally and evolutionarily meaningful gene clusters. Gene clustering is complicated by intraspecific duplications and horizontal gene transfers, that are frequent in prokaryotes. In consequence, gene clustering methods must deal with a trade-off between identifying vertically transmitted representatives of multi-copy gene families (recognizable by synteny conservation) and retrieving complete sets of species-level orthologs. We studied the implications of adopting homology, orthology, or synteny conservation as formal criteria for gene clustering by performing comparative analyses of 125 prokaryotic pangenomes. ResultsClustering criteria affect pangenome functional characterization, core genome inference, and reconstruction of ancestral gene content to different extents. Species-wise estimates of pangenome and core genome sizes change by the same factor when using different clustering criteria, which allows for robust cross-species comparisons regardless of the clustering criterion. However, cross-species comparisons of genome plasticity and functional profiles are substantially affected by inconsistencies among clustering criteria. Such inconsistencies are driven not only by mobile genetic elements, but also by genes involved in defense, secondary metabolism, and other accessory functions. In some pangenome features, the variability attributed to methodological inconsistencies can even exceed the effect sizes of ecological and phylogenetic variables. ConclusionsChoosing an appropriate criterion for gene clustering is critical to conduct unbiased pangenome analyses. We provide practical guidelines to choose the right method depending on the research goals and the quality of genome assemblies, and a benchmarking dataset to assess the robustness and reproducibility of future comparative studies.

genomics↗