Laura Eme

Increasing evidence supports that eukaryotes originated from the symbiosis of an Asgard archaeon, the alphaproteobacterial ancestor of mitochondria, and possibly additional bacterial contributions. Eukaryogenesis likely occurred in redox-transition environments such as microbial mats or shallow sediments ~2 billion years ago, when atmospheric oxygen was far lower than today. We investigated Asgard-enriched microbial mats from the low-oxygen, sulfidic Catherine volcano lake (Afar region, Ethiopia), mimicking early Proterozoic conditions. 16S rRNA gene metabarcoding, metagenomics, and metagenome-assembled genome analyses across redox-stratified layers of in situ and mesocosm-maintained mats revealed that Asgardarchaeota thrived in the sulfate-reduction zone, mainly co-occurring with Desulfurobacterota-Myxococcota, among others. Lokiarchaeia and Thorarchaeia preferred anoxic layers. Within Heimdallarchaeia, Heimdallarchaeales were enriched in upper layers, correlating with oxygen-tolerant hydrogenase and sulfate-reduction genes, and Hodarchaeales, in anoxic layers, correlating with methanogenesis. Although reactive-oxygen-species defense mechanisms were widespread, Asgardarchaeota lacked aerobic respiration. These results support the hypothesis that Asgard archaea engaged primarily in syntrophic interactions with sulfate-reducers under early-Earth-like conditions.

Understanding the phylogenetic relationships among eukaryotic lineages is essential for tracing the evolution of key phenotypic traits and inferring the nature of the Last Eukaryotic Common Ancestor. While phylogenomic analyses have clustered eukaryotic taxa into several well-supported major ‘supergroups’, the relationships among them remain largely uncertain. Phylogenetic signal erosion over deep time and limited available taxon sampling are among the possible causes. However, most previous studies rely on variations of the same core protein dataset, hence containing the same potential systematic biases. Here, we reconstructed the eukaryotic Tree of Life using a largely independent, marker-rich dataset derived from highly conserved Benchmarking Universal Single-Copy Orthologs. Unlike previous collections, our 277-marker supermatrix minimizes ribosomal protein representation and shares less than 25% overlap with previous datasets. State-of-the-art analyses of this dataset confirm most eukaryotic supergroups previously observed, but suggest different positions for some lineages. Notably, Telonemia clusters with Haptophyta rather than SAR (Stramenopiles-Alveolata-Rhizaria), and Ancyromonadida and Malawimonadida form a monophyletic group at the base of the Opimoda. Our results highlight the importance of analyzing independent phylogenomic datasets and support the hypothesis that extant eukaryotic diversity encompasses a small number of high-rank, supergroup lineages.

Summary: The evolutionary origin of red algae‐derived complex plastids remains obscure. Cryptophyta, one of four eukaryotic lineages harboring these plastids, still contains nucleomorphs, which are highly reduced remnants of red algal nuclei. The genes present on nucleomorph genomes can be used for phylogenomic reconstruction in order to unravel the evolutionary origin of red complex plastids and provide data independent from previously analyzed plastid‐encoded proteins. Here, we leverage these genes in a first phylogenomic attempt at pinpointing the position of cryptophyte nucleomorphs within a comprehensive diversity of Rhodophyta, including new sequence representatives from seven deep‐branching red algae. Our analysis, supported by a series of rigorous topology tests, places cryptophyte nucleomorphs as sister to the extremophilic, freshwater subphylum Cyanidiophytina. This conflicts with previously published analyses based on plastidial genes that placed red complex plastids closer to the mesophilic Rhodophytina. While the precise sister group remains debated, our results robustly reject a nucleomorph origin from within any currently recognized class of Rhodophyta, instead suggesting an ancient origin of complex red plastids among the deepest branches of the red algal tree of life.

Retracer l'histoire évolutive des eucaryotes est une question majeure en évolution et fait l'objet de nombreux débats. Le développement de techniques à haut débit, en particulier en protéomique et en génomique, a permis d'obtenir de nombreuses données pouvant être exploitées lors d'analyses évolutives. Dans ce contexte, les structures multiprotéiques eucaryotes (SME) constituent des objets d'intérêt. En effet, ces gros complexes protéiques sont impliqués dans de nombreux processus fondamentaux de la cellule eucaryote, et n'ont pas d'homologues chez les procaryotes (même si les fonctions dans lesquelles ils sont impliqués peuvent exister). Ils ont donc certainement joué un rôle prépondérant dans l'eucaryogénèse. L'analyse phylogénomique de deux SME impliquées dans la division cellulaire (le midbody et l'APC/C) montre que ces systèmes ont une origine évolutive ancienne et étaient déjà présents chez le dernier ancêtre commun des eucaryotes (LECA), tout en étant issus d'innovations eucaryotes. Ceci implique que l'émergence de ces deux SME s'est faite après la divergence de la lignée eucaryote et avant la diversification ayant donné naissance aux lignées actuelles. Au-delà de ces considérations évolutives, l'analyse de ces SME ouvre des pistes sur certains aspects de la biologie de ces systèmes. En effet, si ces systèmes ont été globalement bien conservés au cours de la diversification des eucaryotes, leur analyse révèle une grande plasticité de composition dans certaines lignées de protistes. Ceci suggère des changements récents concernant certaines étapes du cycle cellulaire de ces organismes qu'il serait intéressant d'explorerexpérimentalement.En parallèle, ce travail a montré que, bien qu'étant des protéines opérationnelles, lescomposants de ces SME portent un signal phylogénétique exploitable pour inférer les relations de parentés entre lignées eucaryotes. La construction de supermatrices à partir de ces protéines a permis l'inférence de phylogénies de qualité, même si non totalement résolues, dans lesquelles, par exemple, la monophylie des Excavata ou encore le placement des microsporidies au sein des Fungi est bien supporté. La combinaison de ces données avec celles issues d'analyses basées sur des protéines informationnelles montrent des avancées significatives concernant la résolution des arbres inférés. Ces résultats ouvrent le champ des possibles quant à la recherche d'autres marqueurs encore inexploités parmi les protéines opérationnelles. L'intégration de ces nouveaux marqueurs associée à l'augmentation de l'échantillonnage taxonomique représente une piste prometteuse pour l'avenir.Ce travail illustre l'intérêt de généraliser les approches évolutives intégrées des systèmes biologiques pour l'étude de l'évolution et de la phylogénie des eucaryotes.

Eukaryotes originated from the symbiosis of an Asgard archaeon, the alphaproteobacterial ancestor of mitochondria, and possibly additional bacterial contributions. This transition occurred in redox-transition environments such as microbial mats or shallow sediments ~2 billion years ago, when atmospheric oxygen was far lower than today. We investigated Asgard-enriched microbial mats from the low-oxygen, sulfidic Catherine volcano lake (Afar region, Ethiopia), mimicking early Proterozoic conditions. 16S rRNA gene metabarcoding, metagenomics, and metagenome-assembled genome analyses across redox-stratified layers of in situ and mesocosm-maintained mats revealed that Asgardarchaeota thrived in the sulfate-reduction zone, mainly co-occurring with Desulfurobacterota-Myxococcota, among others. Lokiarchaeia and Thorarchaeia preferred anoxic layers. Within Heimdallarchaeia, Heimdallarchaeales were enriched in upper layers, correlating with oxygen-tolerant hydrogenase and sulfate-reduction genes, and Hodarchaeales, in anoxic layers, correlating with methanogenesis. Although reactive-oxygen-species defense mechanisms were widespread, Asgardarchaeota lacked aerobic respiration. These results support the idea that Asgard archaea engaged primarily in syntrophic interactions with sulfate-reducers under early-Earth-like conditions.

Understanding the origin of eukaryotic cells is one of the most difficult problems in all of biology. A key challenge relevant to the question of eukaryogenesis is reconstructing the gene repertoire of the last eukaryotic common ancestor (LECA). As data sets grow, sketching an accurate genomics-informed picture of early eukaryotic cellular complexity requires provision of analytical resources and a commitment to data sharing. Here, we summarise progress towards understanding the biology of LECA and outline a community approach to inferring its wider gene repertoire. Once assembled, a robust LECA gene set will be a useful tool for evaluating alternative hypotheses about the origin of eukaryotes and understanding the evolution of traits in all descendant lineages, with relevance in diverse fields such as cell biology, microbial ecology, biotechnology, agriculture, and medicine. In this Consensus View, we put forth the status quo and an agreed path forward to reconstruct LECA’s gene content.

SUMMARY: The eukaryote Tree of Life (eToL) depicts the relationships among all eukaryotic organisms; its root represents the last eukaryotic common ancestor (LECA) from which all extant complex lifeforms are descended. Locating this root is crucial for reconstructing the features of LECA, both as the endpoint of eukaryogenesis and the start-point for the evolution of the myriad complex traits underpinning the diversification of living eukaryotes. However, the position of the root remains contentious due to pervasive phylogenetic artefacts stemming from inadequate evolutionary models, poor taxon sampling, and limited phylogenetic signal. Here, we estimate the root of the eToL with unprecedented resolution based on a new, much larger, dataset of mitochondrial proteins which includes all known eukaryotic supergroups. Our comprehensive analyses with state-of-the-art phylogenetic models reveal that the eukaryotic root lies between two multi-supergroup assemblages: ‘Opimoda+’ and ‘Diphoda+’. Compellingly, this position is consistently supported across different models and robustness analyses. Notably, groups containing ‘typical excavates’ are placed on both sides of the root, suggesting the complex features of the ‘excavate’ cell architecture trace back to LECA. This study is the most comprehensive phylogenetic investigation of the eukaryote root to date, shedding light on the ancestral cells from which extant eukaryotes arose and providing a crucial framework for investigating the origin and evolution of canonical eukaryotic features.

Profile mixture models capture distinct biochemical constraints on the amino acid substitution process at different sites in proteins. These models feature a mixture of time-reversible models with a common matrix of exchangeabilities and distinct sets of equilibrium amino acid frequencies known as profiles. Combining the exchangeability matrix with each profile generates the matrix of instantaneous rates of amino acid exchange for that profile. Currently, empirically estimated exchangeability matrices (e.g. the LG matrix) are widely used for phylogenetic inference under profile mixture models. However, these were estimated using a single profile and are unlikely optimal for profile mixture models. Here, we describe the GTRpmix model that allows maximum likelihood estimation of a common exchangeability matrix under any profile mixture model. We show that exchangeability matrices estimated under profile mixture models differ from the LG matrix, dramatically improving model fit and topological estimation accuracy for empirical test cases. Because the GTRpmix model is computationally expensive, we provide two exchangeability matrices estimated from large concatenated phylogenomic-supermatrices to be used for phylogenetic analyses. One, called Eukaryotic Linked Mixture (ELM), is designed for phylogenetic analysis of proteins encoded by nuclear genomes of eukaryotes, and the other, Eukaryotic and Archaeal Linked mixture (EAL), for reconstructing relationships between eukaryotes and Archaea. These matrices, combined with profile mixture models, fit data better and have improved topology estimation relative to the LG matrix combined with the same mixture models. Starting with version 2.3.1, IQ-TREE2 allows users to estimate linked exchangeabilities (i.e. amino acid exchange rates) under profile mixture models.