The deep archaeal roots of eukaryotes

The set of conserved eukaryotic protein-coding genes includes distinct subsets one of which appears to be most closely related to and, by inference, derived from archaea, whereas another one appears to be of bacterial, possibly, endosymbiotic origin. The "archaeal" genes of eukaryotes, primarily, encode components of information-processing systems, whereas the "bacterial" genes are predominantly operational. The precise nature of the archaeo-eukaryotic relationship remains uncertain, and it has been variously argued that eukaryotic informational genes evolved from the homologous genes of Euryarchaeota or Crenarchaeota (the major branches of extant archaea) or that the origin of eukaryotes lies outside the known diversity of archaea. We describe a comprehensive set of 355 eukaryotic genes of apparent archaeal origin identified through ortholog detection and phylogenetic analysis. Phylogenetic hypothesis testing using constrained trees, combined with a systematic search for shared derived characters in the form of homologous inserts in conserved proteins, indicate that, for the majority of these genes, the preferred tree topology is one with the eukaryotic branch placed outside the extant diversity of archaea although small subsets of genes show crenarchaeal and euryarchaeal affinities. Thus, the archaeal genes in eukaryotes appear to descend from a distinct, ancient, and otherwise uncharacterized archaeal lineage that acquired some euryarchaeal and crenarchaeal genes via early horizontal gene transfer.     

The origin of heterochromatin in eukaryotes

This study is an attempt to reconstruct the stages of the evolution of heterochromatin in eukaryotes. According to the hypothesis put forward in the work, the origin of satellite DNAs (stDNAs) was directly related to certain functional characteristics of DNA polymerases, and stDNAs themselves are products of accidental slippage at replication initiation sites. Even at the moment when the stDNAs precursors (protosatellites) appeared, they had properties of selfish DNA. Therefore, specific complex mechanisms of genetic control of their replication and recombination have developed in evolution to restrict the spread of these DNAs over the genome. The host control over protosatellites has led to the appearance of the main heterochromatic characteristics in them, such as late replication, decreased recombination, and denser chromatin packing compared to euchromatin. The next stage of heterochromatin evolution led to the union of protosatellite clusters and ordinary genes if late replication was necessary for these genes or if gene complexes already formed required protection from the destructure effect of crossing over. The known cases of location of certain genes in heterochromatic blocks in Drosophila melanogaster, the eukaryote that has been best studied genetically, confirm this hypothesis.     

Selenoproteins and the metabolic features of the archaeal ancestor of eukaryotes

In all three branches of life, some organisms incorporate the rare amino acid selenocysteine. Selenoproteins are relevant to the controversy over the metabolic features of the archaeal ancestor of eukaryotes because among archaea, several known selenoproteins are involved in methanogenesis and autotrophic growth. Although the eukaryotic selenocysteine-specific translation apparatus and at least one selenoprotein appear to be of archaeal origin, selenoproteins have not been identified among sulfur-metabolizing crenarchaeotes. In this regard, both the phylogeny and function of archaeal selenoproteins are consistent with the argument that the archaeal ancestor was a methanogen. Selenium, however, is abundant in sulfur-rich environments, and some anaerobic bacteria reduce sulfur and have selenoproteins similar to those in archaea. As additional archaeal sequence data becomes available, it will be important to determine whether selenoproteins are present in nonmethanogenic archaea, especially the sulfur-metabolizing crenarchaeotes.     

Potential key bases of ribosomal RNA to kingdom-specific spectra of antibiotic susceptibility and the possible archaeal origin of eukaryotes

In support of the hypothesis of the endosymbiotic origin of eukaryotes, much evidence has been found to support the idea that some organelles of eukaryotic cells originated from bacterial ancestors. Less attention has been paid to the identity of the host cell, although some biochemical and molecular genetic properties shared by archaea and eukaryotes have been documented. Through comparing 507 taxa of 16S-18S rDNA and 347 taxa of 23S-28S rDNA, we found that archaea and eukaryotes share twenty-six nucleotides signatures in ribosomal DNA. These signatures exist in all living eukaryotic organisms, whether protist, green plant, fungus, or animal. This evidence explicitly supports the archaeal origin of eukaryotes. In the ribosomal RNA, besides A2058 in Escherichia coli vs. G2400 in Saccharomyces cerevisiae, there still exist other twenties of sites, in which the bases are kingdom-specific. Some of these sites concentrate in the peptidyl transferase centre (PTC) of the 23S-28S rRNA. The results suggest potential key sites to explain the kingdom-specific spectra of drug resistance of ribosomes.     

The origin of eukaryotes: a reappraisal

Ever since the elucidation of the main structural and functional features of eukaryotic cells and subsequent discovery of the endosymbiotic origin of mitochondria and plastids, two opposing hypotheses have been proposed to account for the origin of eukaryotic cells. One hypothesis postulates that the main features of these cells, including their ability to capture food by endocytosis and to digest it intracellularly, were developed first, and later had a key role in the adoption of endosymbionts; the other proposes that the transformation was triggered by an interaction between two typical prokaryotic cells, one of which became the host and the other the endosymbiont. Re-examination of this question in the light of cell-biological and phylogenetic data leads to the conclusion that the first model is more likely to be the correct one.     

Early evolution and the origin of eukaryotes

Our understanding of evolutionary relationships in the eukaryotic world has been revolutionized by molecular systematics. Phylogenies based upon comparisons of rRNAs define five major eukaryotic assemblages plus a series of paraphyletic protist lineages. Comparison of conserved genes that were duplicated prior to the divergence of eubacteria, archaebacteria, and eukaryotes, positions the root of the universal tree within the eubacterial line of descent. In this review a novel model is presented which uses the rRNA and protein based phylogenies to describe the evolutionary origins of eukaryotes.     

Changing perspectives on the origin of eukaryotes

From the initial application of molecular techniques to the study of microbial organisms, three domains of life emerged, with eukaryotes and archaea as sister taxa. However, recent analyses of an expanding molecular data set reveal that the eukaryotic genome is chimeric with respect to archaea and bacteria. Moreover, there is now evidence that the primitive eukaryotic group ‘Archezoa' once harbored mitochondia. These discoveries have challenged the traditional stepwise model of the evolution of eukaryotes, in which the nucleus and microtubules evolve before the acquisition of mitochondria, and consequently compel a revision of existing models of the origin of eukaryotic cells.     

Metabolic symbiosis at the origin of eukaryotes

Thirty years after Margulis revived the endosymbiosis theory for the origin of mitochondria and chloroplasts, two novel symbiosis hypotheses for the origin of eukaryotes have been put forward. Both propose that eukaryotes arose through metabolic symbiosis (syntrophy) between eubacteria and methanogenic Archaea. They also propose that this was mediated by interspecies hydrogen transfer and that, initially, mitochondria were anaerobic. These hypotheses explain the mosaic character of eukaryotes (i.e. an archaeal-like genetic machinery and a eubacterial-like metabolism), as well as distinct eukaryotic characteristics (which are proposed to be products of symbiosis). Combined data from comparative genomics, microbial ecology and the fossil record should help to test their validity.     

The origin and early evolution of eukaryotes in the light of phylogenomics

Phylogenomics of eukaryote supergroups suggest a highly complex last common ancestor of eukaryotes and a key role of mitochondrial endosymbiosis in the origin of eukaryotes.     

Exploring microbial dark matter to resolve the deep archaeal ancestry of eukaryotes

The origin of eukaryotes represents an enigmatic puzzle, which is still lacking a number of essential pieces. Whereas it is currently accepted that the process of eukaryogenesis involved an interplay between a host cell and an alphaproteobacterial endosymbiont, we currently lack detailed information regarding the identity and nature of these players. A number of studies have provided increasing support for the emergence of the eukaryotic host cell from within the archaeal domain of life, displaying a specific affiliation with the archaeal TACK superphylum. Recent studies have shown that genomic exploration of yet-uncultivated archaea, the so-called archaeal ‘dark matter’, is able to provide unprecedented insights into the process of eukaryogenesis. Here, we provide an overview of state-of-the-art cultivation-independent approaches, and demonstrate how these methods were used to obtain draft genome sequences of several novel members of the TACK superphylum, including Lokiarchaeum, two representatives of the Miscellaneous Crenarchaeotal Group (Bathyarchaeota), and a Korarchaeum-related lineage. The maturation of cultivation-independent genomics approaches, as well as future developments in next-generation sequencing technologies, will revolutionize our current view of microbial evolution and diversity, and provide profound new insights into the early evolution of life, including the enigmatic origin of the eukaryotic cell.     

The origin of the eukaryotic cell. IV. The general hypothesis of the autogenous origin of eukaryotes

The general hypothesis of autogenous (non-symbiotic) origin of the eukaryotic cell summarises some hypotheses explaining possible ways of the origin of main components and organelles of such a cell (the primary unicellular protist). Six hypothesises are suggested. Arising of the eukaryotic surface membrane of protist (cell) as a result of modification of its lipidoacidic composition, when most of synblocks and ensembles of eukaryotic enzymes sink into the cytoplasm (due to membrane vesiculation). Establishment of eukaryotic cytoplasm on the basis of successive formation of two locomotory-supporting apparates: the primary one (microtrabecular system), and the second one (cytoskeleton). Arising of the nucleus from a polyheteronomous nucleoid of proeukaryotes. A combinatorical hypothesis of mitosis formation. Polyheteronucleoid hypothesis of the origin of the mitochondria and chloroplasts. Arising of the flagellum from the contractile tentacle-like organelle, whose axoneme is made of single microtubules. A close interrelation and interaction in the process of evolution is noted between surface membranes, the cytoplasm and the nucleus. In accord a principles of block-construction and heterochrony (see: Seravin, 1986r), the author explains the preservation of prokaryotic signs of organization in some components (and organelles) of eukaryotic cell (and protists).     

A genomic timescale for the origin of eukaryotes

Background  

Genomic sequence analyses have shown that horizontal gene transfer occurred during the origin of eukaryotes as a consequence of symbiosis. However, details of the timing and number of symbiotic events are unclear. A timescale for the early evolution of eukaryotes would help to better understand the relationship between these biological events and changes in Earth's environment, such as the rise in oxygen. We used refined methods of sequence alignment, site selection, and time estimation to address these questions with protein sequences from complete genomes of prokaryotes and eukaryotes.     

The origin of eukaryotes: the difference between prokaryotic and eukaryotic cells.

Eukaryotes have long been thought to have arisen by evolving a nucleus, endomembrane, and cytoskeleton. In contrast, it was recently proposed that the first complex cells, which were actually proto-eukaryotes, arose simultaneously with the acquisition of mitochondria. This so-called symbiotic association hypothesis states that eukaryotes emerged when some ancient anaerobic archaebacteria (hosts) engulfed respiring alpha-proteobacteria (symbionts), which evolved into the first energy-producing organelles. Therefore, the intracellular compartmentalization of the energy-converting metabolism that was bound originally to the plasma membrane appears to be the key innovation towards eukaryotic genome and cellular organization. The novel energy metabolism made it possible for the nucleotide synthetic apparatus of cells to be no longer limited by subsaturation with substrates and catalytic components. As a consequence, a considerable increase has occurred in the size and complexity of eukaryotic genomes, providing the genetic basis for most of the further evolutionary changes in cellular complexity. On the other hand, the active uptake of exogenous DNA, which is general in bacteria, was no longer essential in the genome organization of eukaryotes. The mitochondrion-driven scenario for the first eukaryotes explains the chimera-like composition of eukaryotic genomes as well as the metabolic and cellular organization of eukaryotes.     

A molecular timeline for the origin of photosynthetic eukaryotes

The appearance of photosynthetic eukaryotes (algae and plants) dramatically altered the Earth's ecosystem, making possible all vertebrate life on land, including humans. Dating algal origin is, however, frustrated by a meager fossil record. We generated a plastid multi-gene phylogeny with Bayesian inference and then used maximum likelihood molecular clock methods to estimate algal divergence times. The plastid tree was used as a surrogate for algal host evolution because of recent phylogenetic evidence supporting the vertical ancestry of the plastid in the red, green, and glaucophyte algae. Nodes in the plastid tree were constrained with six reliable fossil dates and a maximum age of 3,500 MYA based on the earliest known eubacterial fossil. Our analyses support an ancient (late Paleoproterozoic) origin of photosynthetic eukaryotes with the primary endosymbiosis that gave rise to the first alga having occurred after the split of the Plantae (i.e., red, green, and glaucophyte algae plus land plants) from the opisthokonts sometime before 1,558 MYA. The split of the red and green algae is calculated to have occurred about 1,500 MYA, and the putative single red algal secondary endosymbiosis that gave rise to the plastid in the cryptophyte, haptophyte, and stramenopile algae (chromists) occurred about 1,300 MYA. These dates, which are consistent with fossil evidence for putative marine algae (i.e., acritarchs) from the early Mesoproterozoic (1,500 MYA) and with a major eukaryotic diversification in the very late Mesoproterozoic and Neoproterozoic, provide a molecular timeline for understanding algal evolution.     

Mosaic origin of the heme biosynthesis pathway in photosynthetic eukaryotes

Heme biosynthesis represents one of the most essential metabolic pathways in living organisms, providing the precursors for cytochrome prosthetic groups, photosynthetic pigments, and vitamin B(12). Using genomic data, we have compared the heme pathway in the diatom Thalassiosira pseudonana and the red alga Cyanidioschyzon merolae to those of green algae and higher plants, as well as to those of heterotrophic eukaryotes (fungi, apicomplexans, and animals). Phylogenetic analyses showed the mosaic character of this pathway in photosynthetic eukaryotes. Although most of the algal and plant enzymes showed the expected plastid (cyanobacterial) origin, at least one of them (porphobilinogen deaminase) appears to have a mitochondrial (alpha-proteobacterial) origin. Another enzyme, glutamyl-tRNA synthase, obviously originated in the eukaryotic nucleus. Because all the plastid-targeted sequences consistently form a well-supported cluster, this suggests that genes were either transferred from the primary endosymbiont (cyanobacteria) to the primary host nucleus shortly after the primary endosymbiotic event or replaced with genes from other sources at an equally early time, i.e., before the formation of three primary plastid lineages. The one striking exception to this pattern is ferrochelatase, the enzyme catalyzing the first committed step to heme and bilin pigments. In this case, two red algal sequences do not cluster either with the other plastid sequences or with cyanobacterial sequences and appear to have a proteobacterial origin like that of the apicomplexan parasites Plasmodium and Toxoplasma. Although the heterokonts also acquired their plastid via secondary endosymbiosis from a red alga, the diatom has a typical plastid-cyanobacterial ferrochelatase. We have not found any remnants of the plastidlike heme pathway in the nonphotosynthetic heterokonts Phytophthora ramorum and Phytophthora sojae.     

The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation

Determining the relationships among and divergence times for the major eukaryotic lineages remains one of the most important and controversial outstanding problems in evolutionary biology. The sequencing and phylogenetic analyses of ribosomal RNA (rRNA) genes led to the first nearly comprehensive phylogenies of eukaryotes in the late 1980s, and supported a view where cellular complexity was acquired during the divergence of extant unicellular eukaryote lineages. More recently, however, refinements in analytical methods coupled with the availability of many additional genes for phylogenetic analysis showed that much of the deep structure of early rRNA trees was artefactual. Recent phylogenetic analyses of a multiple genes and the discovery of important molecular and ultrastructural phylogenetic characters have resolved eukaryotic diversity into six major hypothetical groups. Yet relationships among these groups remain poorly understood because of saturation of sequence changes on the billion-year time-scale, possible rapid radiations of major lineages, phylogenetic artefacts and endosymbiotic or lateral gene transfer among eukaryotes. Estimating the divergence dates between the major eukaryote lineages using molecular analyses is even more difficult than phylogenetic estimation. Error in such analyses comes from a myriad of sources including: (i) calibration fossil dates, (ii) the assumed phylogenetic tree, (iii) the nucleotide or amino acid substitution model, (iv) substitution number (branch length) estimates, (v) the model of how rates of evolution change over the tree, (vi) error inherent in the time estimates for a given model and (vii) how multiple gene data are treated. By reanalysing datasets from recently published molecular clock studies, we show that when errors from these various sources are properly accounted for, the confidence intervals on inferred dates can be very large. Furthermore, estimated dates of divergence vary hugely depending on the methods used and their assumptions. Accurate dating of divergence times among the major eukaryote lineages will require a robust tree of eukaryotes, a much richer Proterozoic fossil record of microbial eukaryotes assignable to extant groups for calibration, more sophisticated relaxed molecular clock methods and many more genes sampled from the full diversity of microbial eukaryotes.     

Host origin of plastid solute transporters in the first photosynthetic eukaryotes

Background  

It is generally accepted that a single primary endosymbiosis in the Plantae (red, green (including land plants), and glaucophyte algae) common ancestor gave rise to the ancestral photosynthetic organelle (plastid). Plastid establishment necessitated many steps, including the transfer and activation of endosymbiont genes that were relocated to the nuclear genome of the 'host' followed by import of the encoded proteins into the organelle. These innovations are, however, highly complex and could not have driven the initial formation of the endosymbiosis. We postulate that the re-targeting of existing host solute transporters to the plastid fore-runner was critical for the early success of the primary endosymbiosis, allowing the host to harvest endosymbiont primary production.