Andrew J Roger

Dalhousie University | Dal · Department of Biochemistry and Molecular Biology

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 complexi...

In prokaryotes lateral gene transfer (LGT) is a key mechanism leading to intra-species variability in gene content and the phenomenon of pangenomes. In microbial eukaryotes, however, the extent to which LGT-driven pangenomes exist is unclear. Pelagophytes are ecologically important marine algae that include Aureococcus anophagefferens – a species n...

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 ev...

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 evolut...

Metamonads are a large and exclusively anaerobic group of protists. Additionally, they are one of the three clades proposed to ancestrally possess an “excavate” cell morphology, with a conspicuous ventral groove accompanied by a posterior flagellum with a vane. Here, we cultivate and characterize four anaerobic bacterivorous flagellates from hypers...

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...

Metamonads are a diverse group of heterotrophic microbial eukaryotes adapted to living in hypoxic environments. All metamonads but one harbour metabolically altered ‘mitochondrion-related organelles’ (MROs) with reduced functions, however the degree of reduction varies. Here, we generate high-quality draft genomes, transcriptomes, and predicted pro...

Mitochondria and related organelles—hydrogenosomes, mitosomes and other mitochondrion-related organelles (MROs)—are essential compartments in almost all eukaryotic cells. Although mitochondria are renowned for their role in high-efficiency ATP synthesis via oxidative phosphorylation, they have a wide spectrum of other functions within eukaryotic ce...

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 set of amino acid exchange rates (a matrix of exchangeabilities) and distinct sets of equilibrium amino acid frequencies known as profiles. Comb...

Extremely halophilic archaea (Haloarchaea, Nanohaloarchaeota, Methanonatronarchaeia and Halarchaeoplasmatales) thrive in saturating salt concentrations where they must maintain osmotic equilibrium with their environment. The evolutionary history of adaptations enabling salt tolerance remains poorly understood, in particular because the phylogeny of...

Metamonads are a large and exclusively anaerobic clade of protists. Additionally, metamonads are one of the three clades with a proposed 'excavate' ancestral cell morphology, characterised by a conspicuous ventral groove often accompanied by a posterior flagellum with a vane. Here, we characterise four isolates of an anaerobic bacterivorous flagell...

Whole-genome shotgun (WGS) metagenomic sequencing of microbial communities allows us to discover the functions, physiologies, and evolutionary histories of microbial prokaryote and eukaryote members of diverse ecosystems. Despite their importance, metagenomic studies of microbial eukaryotes lag behind those of prokaryotes, due to the difficulty in...

Inteins are self-splicing protein elements found in viruses and all three domains of life. How the DNA encoding these selfish elements spreads within and between genomes is poorly understood, particularly in eukaryotes where inteins are scarce. Here, we show that the nuclear genomes of three strains of Anaeramoeba encode between 45 and 103 inteins,...

Archamoebae comprises free-living or endobiotic amoebiform protists that inhabit anaerobic or microaerophilic environments and possess mitochondrion-related organelles (MROs) adapted to function anaerobically. We compared in silico reconstructed MRO proteomes of eight species (six genera) and found that the common ancestor of Archamoebae possessed...

Biochemical constraints on the admissible amino acids at specific sites in proteins lead to heterogeneity of the amino acid substitution process over sites in alignments. It is well known that phylogenetic models of protein sequence evolution that do not account for site heterogeneity are prone to long-branch attraction (LBA) artifacts. Profile mix...

′Kingdom-level′ branches are being added to the tree of eukaryotes at a rate approaching one per year, with no signs of slowing down ¹⁻⁴ . Some are completely new discoveries, while others are morphologically unusual protists that were previously described but lacked molecular data. For example, Hemimastigophora are predatory protists with two rows...

Several archaeal lineages thrive in high, saturating salt concentrations. These extremely halophilic archaea, including Halobacteria, Nanohaloarchaeota, Methanonatronarchaeia, and Haloplasmatales, must maintain osmotic equilibrium with their environment. For this, they use a 'salt-in' strategy, which involves pumping molar concentrations of potassi...

Metamonads are a diverse group of heterotrophic microbial eukaryotes adapted to living in hypoxic environments. All metamonads but one harbour metabolically altered 'mitochondrion-related organelles' (MROs) with reduced functions relative to aerobic mitochondria, however the degree of reduction varies markedly over the metamonad tree. To further in...

We have uncovered a role for the promyelocytic leukemia (PML) gene and novel PML-like DEDDh exonucleases in the maintenance of genome stability through the restriction of LINE-1 (L1) retrotransposition in jawed vertebrates. Although the mammalian PML protein forms nuclear bodies, we found that the spotted gar PML ortholog and related proteins in fi...

Symbiotic relationships drive evolutionary change and are important sources of novelty. Here we demonstrate a highly structured syntrophic symbiosis between species of the anaerobic protist Anaeramoeba (Anaeramoebae, Metamonada) and bacterial ectosymbionts. We dissected this symbiosis with long-read metagenomics, transcriptomics of host and symbion...

Mitochondrial cristae expand the surface area of respiratory membranes and ultimately allow for the evolutionary scaling of respiration with cell volume across eukaryotes. The discovery of Mic60 homologs among alphaproteobacteria, the closest extant relatives of mitochondria, suggested that cristae might have evolved from bacterial intracytoplasmic...

Background Blastocystis is one of the most common eukaryotic microorganisms colonizing the intestines of both humans and animals, but the conditions under which it may be a pathogen are unclear. Methods To study the genomic characteristics of circulating subtypes (ST) in Colombia, we established nine xenic cultures from Blastocystis isolated from...

The evolution of streptophytes had a profound impact on life on Earth. They brought forth those photosynthetic eukaryotes that today dominate the macroscopic flora: the land plants (Embryophyta).¹ There is convincing evidence that the unicellular/filamentous Zygnematophyceae—and not the morphologically more elaborate Coleochaetophyceae or Charophyc...

We have uncovered a novel role for the promyelocytic leukemia (PML) gene and novel PML-like DEDDh exonucleases in the maintenance of genome stability through the restriction of LINE-1 (L1) retrotransposition in jawed vertebrates. Although the PML tumour suppressor protein in mammals is SUMOylated and forms nuclear bodies, we found that the spotted...

The evolution of streptophytes had a profound impact on life on Earth. They brought forth those photosynthetic eukaryotes that today dominate the macroscopic flora: the land plants (Embryophyta) [1]. There is convincing evidence that the unicellular/filamentous Zygnematophyceae--and not the morphologically more elaborate Coleochaetophyceae or Charo...

Mitochondrial cristae expand the surface area of respiratory membranes and ultimately allow for the evolutionary scaling of respiration with cell volume across eukaryotes. The discovery of Mic60 homologs among alphaproteobacteria, the closest extant relatives of mitochondria, suggested that cristae might have evolved from bacterial intracytoplasmic...

Determining the phylogenetic origin of mitochondria is key to understanding the ancestral mitochondrial symbiosis and its role in eukaryogenesis. However, the precise evolutionary relationship between mitochondria and their closest bacterial relatives remains hotly debated. The reasons include pervasive phylogenetic artefacts as well as limited pro...

A bstract Site heterogeneity of the amino acid substitution process accounts for the biochemical constraints on the range of admissible amino acids at specific sites. Phylogenetic models of protein sequence evolution that do not account for site heterogeneity are more prone to long-branch attraction artifacts. Profile mixture models are used to mod...

Microbial eukaryotes display a stunning diversity of feeding strategies, ranging from generalist predators to highly specialised parasites. The unicellular protoplast feeders represent a fascinating mechanistic intermediate, as they penetrate other eukaryotic cells (algae, fungi) like some parasites, but then devour their cell contents by phagocyto...

Cells replicate and segregate their DNA with precision. Previous studies showed that these regulated cell-cycle processes were present in the last eukaryotic common ancestor and that their core molecular parts are conserved across eukaryotes. However, some metamonad parasites have secondarily lost components of the DNA processing and segregation ap...

Two recent high profile studies have attempted to use edge (branch) length ratios from large sets of phylogenetic trees to determine the relative ages of genes of different origins in the evolution of eukaryotic cells. This approach can be straightforwardly justified if substitution rates are constant over the tree for a given protein. However, suc...

Discoveries of diverse microbial eukaryotes and their inclusion in comprehensive phylogenomic analyses have crucially re-shaped the eukaryotic tree of life in the 21st century.¹ At the deepest level, eukaryotic diversity comprises 9–10 “supergroups.” One of these supergroups, the Metamonada, is particularly important to our understanding of the evo...

Background Comparing a parasitic lineage to its free-living relatives is a powerful way to understand how that evolutionary transition to parasitism occurred. Giardia intestinalis (Fornicata) is a leading cause of gastrointestinal disease world-wide and is famous for its unusual complement of cellular compartments, such as having peripheral vacuole...

Amino acid preferences vary across sites and time. While variation across sites is widely accepted, the extent and frequency of temporal shifts are contentious. Our understanding of the drivers of amino acid preference change is incomplete: To what extent are temporal shifts driven by adaptive versus nonadaptive evolutionary processes? We review ph...

Phylogenomic analyses of hundreds of protein-coding genes aimed at resolving phylogenetic relationships is now a common practice. However, no software currently exists that includes tools for dataset construction and subsequent analysis with diverse validation strategies to assess robustness. Furthermore, there are no publicly available high-qualit...

Andrew Roger commemorates the life and work of evolutionary biologist Thomas Cavalier-Smith, who synthesized evidence from diverse disciplines into bold, testable hypotheses explaining the major transitions in the evolution of life and inspired generations of scientists worldwide with his ideas.

Determining the phylogenetic origin of mitochondria is key to understanding the ancestral mitochondrial symbiosis and its role in eukaryogenesis. However, the precise evolutionary relationship between mitochondria and their closest bacterial relatives remains hotly debated. The reasons include pervasive phylogenetic artefacts, as well as limited pr...

Cells must replicate and segregate their DNA with precision. In eukaryotes, these processes are part of a regulated cell-cycle that begins at S-phase with the replication of DNA and ends after M-phase. Previous studies showed that these processes were present in the last eukaryotic common ancestor and the core parts of their molecular systems are c...

Determination and comparisons of complete mitochondrial genomes (mitogenomes) are important to understand the origin and evolution of mitochondria. Mitogenomes of unicellular protists are particularly informative in this regard because they are gene-rich and display high structural diversity. Ciliates are a highly diverse assemblage of protists and...

Comparing a parasitic lineage to its free-living relatives is a powerful way to understand how the evolutionary transition to parasitism occurred. Giardia intestinalis (Fornicata) is a leading cause of gastrointestinal disease world-wide and is famous for its unusual complement of cellular compartments, such as having peripheral vacuoles instead of...

The transition of free-living organisms to parasitic organisms is a mysterious process that occurs in all major eukaryotic lineages. Parasites display seemingly unique features associated with their pathogenicity; however, it is important to distinguish ancestral preconditions to parasitism from truly new parasite-specific functions. Here, we seque...

Long branch attraction is a prevalent form of bias in phylogenetic estimation but the reasons for it are only partially understood. We argue here that it is largely due to differences in the sizes of the model spaces corresponding to different trees. Trees with long branches together allow much more flexible internal branch-length parameter estimat...

Timing the events in the evolution of eukaryotic cells is crucial to understanding this major transition. A recent study reconstructs the origins of thousands of gene families ancestral to eukaryotes and, using a controversial approach, aims to order the events of eukaryogenesis.

Two recent high profile studies have attempted to use edge (branch) length ratios from large sets of phylogenetic trees to determine the relative ages of genes of different origins in the evolution of eukaryotic cells. This approach can be straightforwardly justified if substitution rates are constant over the tree for a given protein. However, suc...

The most fundamental form of epistasis occurs between residues within a protein. Epistatic interactions can have significant consequences for evolutionary dynamics. For example, a substitution to a deleterious amino acid may be compensated for by replacements at other sites which increase its propensity (a function of its average fitness) over time...

The most fundamental form of epistasis occurs between residues within a protein. Epistatic interactions can have significant consequences for evolutionary dynamics. For example, a substitution to a deleterious amino acid may be compensated for by replacements at other sites which increase its propensity (a function of its average fitness) over time...

Lateral gene transfer (LGT) is well known as an important driver of genome evolution in bacteria and archaea, but its importance in eukaryote evolution has yet to be fully elucidated. There is now abundant evidence indicating that LGT has played a role in the adaptation of eukaryotes to new environments and conditions, including host–parasite inter...

To survive in low‐oxygenic environments, microbial organisms employ anaerobic respiration. In certain organisms, the terpenoid quinone known as rhodoquinone (RQ) plays a key role in this process, though few details are known about how RQ itself is produced or what impact it may have on the cellular respiration process from a biomedical standpoint....

The primary process of energy production for most eukaryotes involves oxidative respiration via the electron transport chain (ETC). In the ETC, electrons are moved by the electron carrier ubiquinone through membrane‐bound protein complexes that pump protons across the mitochondrial membrane, which creates a proton chemical gradient. This gradient i...

Background: Comparative analyses have indicated that the mitochondrion of the last eukaryotic common ancestor likely possessed all the key core structures and functions that are widely conserved throughout the domain Eucarya. To date, such studies have largely focused on animals, fungi, and land plants (primarily multicellular eukaryotes); relativ...

The information criteria AIC, AICc and BIC are widely used for model selection in phylogenetics, however their theoretical justification and performance have not been carefully examined in this setting. Here we investigate these methods under simple and complex phylogenetic models. We show that AIC can give a biased estimate of its intended target,...

We describe Idionectes vortex gen. nov., sp. nov., a unicellular microeukaryote that swims by continuous inversion of its surface, similar to a vortex ring. This previously unreported mode of motility approximates a hypothetical concept called the ‘toroidal swimmer’, in which a doughnut-shaped object rotates around its circular axis and travels in...

For 15 years, the eukaryote Tree of Life (eToL) has been divided into five to eight major groupings, known as 'supergroups'. However, the tree has been profoundly rearranged during this time. The new eToL results from the widespread application of phylogenomics and numerous discoveries of major lineages of eukaryotes, mostly free-living heterotroph...

The discovery that the protist Monocercomonoides exilis completely lacks mitochondria demonstrates that these organelles are not absolutely essential to eukaryotic cells. However, the degree to which the metabolism and cellular systems of this organism have adapted to the loss of mitochondria is unknown. Here we report an extensive analysis of the...

The discovery that the protist Monocercomonoides exilis completely lacks mitochondria demonstrates that these organelles are not absolutely essential to eukaryotic cells. However, the degree to which the metabolism and cellular systems of this organism have adapted to the loss of mitochondria is unknown. Here we report an extensive analysis of the...

Large taxa-rich genome-scale data sets are often necessary for resolving ancient phylogenetic relationships. But accurate phylogenetic inference requires that they are analyzed with realistic models that account for the heterogeneity in substitution patterns amongst the sites, genes and lineages. Two kinds of adjustments are frequently used: models...

The Alphaproteobacteria is an extraordinarily diverse and ancient group of bacteria. Previous attempts to infer its deep phylogeny have been plagued with methodological artefacts. To overcome this, we analyzed a dataset of 200 single-copy and conserved genes and employed diverse strategies to reduce compositional artefacts. Such strategies include...

Almost all eukaryote life forms have now been placed within one of five to eight supra-kingdom-level groups using molecular phylogenetics1–4. The ‘phylum’ Hemimastigophora is probably the most distinctive morphologically defined lineage that still awaits such a phylogenetic assignment. First observed in the nineteenth century, hemimastigotes are fr...

Background: The evolution of photosynthesis has been a major driver in eukaryotic diversification. Eukaryotes have acquired plastids (chloroplasts) either directly via the engulfment and integration of a photosynthetic cyanobacterium (primary endosymbiosis) or indirectly by engulfing a photosynthetic eukaryote (secondary or tertiary endosymbiosis)....

The Alphaproteobacteria is an extraordinarily diverse and ancient group of bacteria. Previous attempts to infer its deep phylogeny have been plagued with methodological artefacts. To overcome this, we analyzed a dataset of 200 single-copy and conserved genes and employed diverse strategies to reduce compositional artefacts. Such strategies include...

Mitochondria have evolved diverse forms across eukaryotic diversity in adaptation to anoxia. Mitosomes are the simplest and the least well-studied type of anaerobic mitochondria. Transport of proteins via TIM complexes, composed of three proteins of the Tim17 protein family (Tim17/22/23), is one of the key unifying aspects of mitochondria and mitoc...

As a consequence of structural and functional constraints, proteins tend to have site-specific preferences for particular amino acids. Failing to adjust for heterogeneity of frequencies over sites can lead to artifacts in phylogenetic estimation. Site-heterogeneous mixture-models have been developed to address this problem. However, due to prohibit...

Under hypoxic conditions, some organisms use an electron transport chain consisting of only complex I and II (CII) to generate the proton gradient essential for ATP production. In these cases, CII functions as a fumarate reductase that accepts electrons from a low electron potential quinol, rhodoquinol (RQ). To clarify the origins of RQ-mediated fu...

Topology test output from CONSEL. Trees 1-6 represent trees1-6 from Supplementary file 3; trees 7-106 represent 100 bootstrap trees from the maximum likelihood analysis. Relevant column headers: Obs, observed log-likelihood value; au, topology test p-value; np, bootstrap probability. Details on the column headers can be found at http://stat.sys.i.k...

PDF with all the tree for the Group A phylogenetic analysis and associated topology tests

Excel file with workbooks containing information about the number of genomes surveyed, PFAM domains of putative RquA homologues, gene accession numbers for RquA and Q-utilizing proteins, mitochondrial targeting sequence information, redox half-potentials used for Figure 5, bacterial genes with and without linkage to respiratory complexes.

Topology test output from CONSEL. Trees 1-20 represent trees 2-21 from Supplementary file 2; trees 21-120 represent 100 bootstrap trees from the maximum likelihood analysis. Relevant column headers: Obs, observed log-likelihood value; au, topology test p-value; np, bootstrap probability. Details on the column headers can be found at http://stat.sys...

PDF with all the trees for the full RquA phylogenetic analysis and associated topology tests

PDF with all the tree for the Group B phylogenetic analysis and associated topology tests

Topology test output from CONSEL. Trees 1-5 represent trees 1-5 from Supplementary file 4; trees 6-105 represent 100 bootstrap trees from the maximum likelihood analysis. Relevant column headers: Obs, observed log-likelihood value; au, topology test p-value; np, bootstrap probability. Details on the column headers can be found at http://stat.sys.i....