Diversification Of Eukaryotes Research Articles

Molecular Data Are Transforming Hypotheses on the Origin and Diversification of Eukaryotes

The explosion of molecular data has transformed hypotheses on both the origin of eukaryotes and the structure of the eukaryotic tree of life. Early ideas about the evolution of eukaryotes arose through analyses of morphology by light microscopy and later electron microscopy. Though such studies have proven powerful at resolving more recent events, theories on origins and diversification of eukaryotic life have been substantially revised in light of analyses of molecular data including gene and, increasingly, whole genome sequences. By combining these approaches, progress has been made in elucidating both the origin and diversification of eukaryotes. Yet many aspects of the evolution of eukaryotic life remain to be illuminated.

Ancient diversification of eukaryotic MCM DNA replication proteins

BackgroundYeast and animal cells require six mini-chromosome maintenance proteins (Mcm2-7) for pre-replication complex formation, DNA replication initiation and DNA synthesis. These six individual MCM proteins form distinct heterogeneous subunits within a hexamer which is believed to form the replicative helicase and which associates with the essential but non-homologous Mcm10 protein during DNA replication. In contrast Archaea generally only possess one MCM homologue which forms a homohexameric MCM helicase. In some eukaryotes Mcm8 and Mcm9 paralogues also appear to be involved in DNA replication although their exact roles are unclear.ResultsWe used comparative genomics and phylogenetics to reconstruct the diversification of the eukaryotic Mcm2-9 gene family, demonstrating that Mcm2-9 were formed by seven gene duplication events before the last common ancestor of the eukaryotes. Mcm2-7 protein paralogues were present in all eukaryote genomes studied suggesting that no gene loss or functional replacements have been tolerated during the evolutionary diversification of eukaryotes. Mcm8 and 9 are widely distributed in eukaryotes and group together on the MCM phylogenetic tree to the exclusion of all other MCM paralogues suggesting co-ancestry. Mcm8 and Mcm9 are absent in some taxa, including Trichomonas and Giardia, and appear to have been secondarily lost in some fungi and some animals. The presence and absence of Mcm8 and 9 is concordant in all taxa sampled with the exception of Drosophila species. Mcm10 is present in most eukaryotes sampled but shows no concordant pattern of presence or absence with Mcm8 or 9.ConclusionA multifaceted and heterogeneous Mcm2-7 hexamer evolved during the early evolution of the eukaryote cell in parallel with numerous other acquisitions in cell complexity and prior to the diversification of extant eukaryotes. The conservation of all six paralogues throughout the eukaryotes suggests that each Mcm2-7 hexamer component has an exclusive functional role, either by a combination of unique lock and key interactions between MCM hexamer subunits and/or by a range of novel side interactions. Mcm8 and 9 evolved early in eukaryote cell evolution and their pattern of presence or absence suggests that they may have linked functions. Mcm8 is highly divergent in all Drosophila species and may not provide a good model for Mcm8 in other eukaryotes.

Evolution: Revisiting the Root of the Eukaryote Tree

A recent phylogenomic investigation shows that the enigmatic flagellate Breviata is a distinct anaerobic lineage within the eukaryote super-group Amoebozoa and challenges the unikont-bikont rooting of the tree of eukaryotes.

Large-Scale Phylogenomic Analyses Reveal That Two Enigmatic Protist Lineages, Telonemia and Centroheliozoa, Are Related to Photosynthetic Chromalveolates

Understanding the early evolution and diversification of eukaryotes relies on a fully resolved phylogenetic tree. In recent years, most eukaryotic diversity has been assigned to six putative supergroups, but the evolutionary origin of a few major “orphan” lineages remains elusive. Two ecologically important orphan groups are the heterotrophic Telonemia and Centroheliozoa. Telonemids have been proposed to be related to the photosynthetic cryptomonads or stramenopiles and centrohelids to haptophytes, but molecular phylogenies have failed to provide strong support for any phylogenetic hypothesis. Here, we investigate the origins of Telonema subtilis (a telonemid) and Raphidiophrys contractilis (a centrohelid) by large-scale 454 pyrosequencing of cDNA libraries and including new genomic data from two cryptomonads (Guillardia theta and Plagioselmis nannoplanctica) and a haptophyte (Imantonia rotunda). We demonstrate that 454 sequencing of cDNA libraries is a powerful and fast method of sampling a high proportion of protist genes, which can yield ample information for phylogenomic studies. Our phylogenetic analyses of 127 genes from 72 species indicate that telonemids and centrohelids are members of an emerging major group of eukaryotes also comprising cryptomonads and haptophytes. Furthermore, this group is possibly closely related to the SAR clade comprising stramenopiles (heterokonts), alveolates, and Rhizaria. Our results link two additional heterotrophic lineages to the predominantly photosynthetic chromalveolate supergroup, providing a new framework for interpreting the evolution of eukaryotic cell structures and the diversification of plastids.

Diversification of unicellular eukaryotes: cryptomonad colonizations of marine and fresh waters inferred from revised 18S rRNA phylogeny

The cryptomonads is a well-defined lineage of unicellular eukaryotes, composed of several marine and freshwater groups. However, the evolutionary relationships among these groups are unclear due to conflicting inferences between morphological and molecular phylogenies. Here, we have inferred the evolutionary relationships among marine and freshwater species in order to better understand the importance of the marine-freshwater boundary on the historical diversification patterns of cryptomonads. We have constructed improved molecular phylogenies by taking into account rate variation both across sites and across sequences (covarion substitutions), and by analysing the vast majority of publicly available cryptomonad 18S rRNA sequences and related environmental phylotypes. The resulting phylogenies included 55 sequences, and revealed two novel freshwater cryptomonad clades (CRY1 and CRY2) and a large hidden diversity of cryptomonads. CRY1 was placed deeply within the cryptomonad phylogeny together with all the major freshwater lineages (i.e. Goniomonas and Cryptomonas), while CRY2 was placed within a lineage of marine species identified as Plagioselmis-like with the aid of a new sequence generated from a cultured species. The inferred phylogenies suggest only few successful marine-freshwater transitions over the history of cryptomonads. Most of the transitions seem to have occurred from marine to fresh waters, but re-colonizations of marine habitats have also taken place. This implies that the differences in the biogeophysical conditions between marine and fresh waters constitute a substantial barrier for the cross-colonization of these environments by cryptomonads.

Inositol derivatives: evolution and functions

Current research on inositols mainly focuses on myo-inositol (Ins) derivatives in eukaryotic cells, and in particular on the many roles of Ins phospholipids and polyphosphorylated Ins derivatives. However, inositols and their derivatives are more versatile than this--they have acquired diverse functions over the course of evolution. Given the central involvement of primordial bacteria and archaea in the emergence of eukaryotes, what is the status of inositol derivatives in these groups of organisms, and how might inositol, inositol lipids and inositol phosphates have become ubiquitous constituents of eukaryotes? And how, later, might the multifarious functions of inositol derivatives have emerged during eukaryote diversification?

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.

A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record

Recent attempts to establish a molecular time-scale of eukaryote evolution failed to provide a congruent view on the timing of the origin and early diversification of eukaryotes. The major discrepancies in molecular time estimates are related to questions concerning the calibration of the tree. To limit these uncertainties, we used here as a source of calibration points the rich and continuous microfossil record of dinoflagellates, diatoms and coccolithophorids. We calibrated a small-subunit ribosomal RNA tree of eukaryotes with four maximum and 22 minimum time constraints. Using these multiple calibration points in a Bayesian relaxed molecular clock framework, we inferred that the early radiation of eukaryotes occurred near the Mesoproterozoic-Neoproterozoic boundary, about 1100 million years ago. Our results indicate that most Proterozoic fossils of possible eukaryotic origin cannot be confidently assigned to extant lineages and should therefore not be used as calibration points in molecular dating.

Major features of protistan evolution: controversies, problems and a few answers

The major features of protist evolution are fraught with controversies, problems and few answers, especially in early Earth history. In general they are based on molecular data and fossil evidence that respectively provide a scaffold and details of eukaryotic phylogenetic and ecologic histories. 1. Their origin, inferred from molecular sequences, occurred very early (>;3Ga). They are a chimera of different symbiont-derived organelles, including possibly the nucleus. 2. The initial diversification of eukaryotes may have occurred early in geologic time. Six supergroups exist today, each with fossils known from the Proterozoic and Phanerozoic. 3. Sex, considered an important development, may have been inherited from bacteria. 4. Precambrian protists were largely pelagic cyst-bearing taxa, but benthic forms were probably quite diverse and abundant. 5. Protists gave rise to animals long before 600 Ma through the choanoflagellates, for which no fossil record exists. 6. Acritarchs and skeletonized protists radiated in the Cambrian (544-530 my). From then on, they radiated and became extinct at all the major events recorded in the metazoan fossil record. 7. Protists dominated major environments (shelves and reefs) starting with a significant radiation in the Ordovician, followed by extinctions and other radiations until most died out at the end of the Permian. 8. In the Mesozoic, new planktic protozoa and algae appeared and radiated in pelagic environments. 9. Modern protists are important at all trophic levels in the oceans and a huge number terrestrial, parasitic and symbiotic protists must have existed for much of geologic time as well. 10. The future of protists is likely in jeopardy, just like most reefal, benthic, and planktic metazoans. An urgent need to understand the role of protists in modern threatened oceans should be addressed soon.

Saccamminid foraminifers from anoxic sediments: implications for Proterozoic ecosystem dynamics

Eukaryote origin and earliest diversification occurred in the Proterozoic when Earth's atmosphere was undoubtedly different from that of today. Atmospheric oxygen levels were increasing from the primordial anoxic atmosphere due, for example, to cyanobacterial oxygenic photosynthesis. Late Proterozoic (∼0.6–0.9 Gya) deep‐ocean oxygen concentrations are less certain, but geochemical evidence suggests anoxia and hydrogen‐sulfide enrichment. It can, therefore, be postulated that initial eukaryotic diversification occurred in oxygen‐depleted, sulfide‐enriched environments. Foraminifera are aerobes and, thus, not expected in anoxic settings. Recently, however, we found a saccamminid allogromian in a deep‐water anoxic, sulfidic setting. Samples were collected from Santa Barbara Basin (California) when bottom‐water oxygen was undetectable and sediments smelled strongly of hydrogen sulfide. Foraminiferal SSU rDNA sequences recovered from sediments included one from a previously uncharacterized saccamminid. Ultrastructural analysis indicated the presence of intact Golgi, mitochondria, and prokaryotic endobionts. Saccamminid occurrence in environmental conditions known to exist during the Proterozoic supports the possibility of their origin early in eukaryotic evolution. Extant saccamminids could have competed well in the prokaryote‐dominated Proterozoic benthic ecosystem given their diet includes bacteria, bacterial biofilms and unicellular algae. Thus, Proterozoic foraminifers may have been top carnivores.Funded by NASA NRA‐01‐01‐EXB‐057, the Geological Society of America's W. Storrs Cole Memorial Research Award, and NSF OPP0003639.

The fossil record of early eukaryotic diversification

The Cambrian explosion can be thought of as the culmination of a diversification of eukaryotes that had begun several hundred million years before. Eukaryotes - one of the three domains of life — originated by late Archean time, and probably underwent a long period of stem group evolution during the Paleoproterozoic Era. A suite of taxonomically resolved body fossils and biomarkers, together with estimates of acritarch and compression fossil diversity, suggest that while divergences among major eukaryotic clades or 'super-groups' may have occurred as early as latest Paleoproterozoic through Mesoproterozoic time, the main phase of eukaryotic diversification took place several hundred million years later, during the middle Neoproterozoic Era. Hypotheses for Neoproterozoic diversification must therefore explain why eukaryotic diversification is delayed several hundred million years after the origin of the eukaryotic crown group, and why diversification appears to have occurred independently within several eukaryotic super-groups at the same time. Evolutionary explanations for eukaryotic diversification (the evolution of sex; the acquisition of plastids) fail to account for these patterns, but ecological explanations (the advent of microbial predators) and environmental explanations (changes in ocean chemistry) are both consistent with them. Both ecology and environment may have played a role in triggering or at least fueling Neoproterozoic eukaryotic diversification.

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.

Changes in organic matter production and accumulation as a mechanism for isotopic evolution in the Mesoproterozoic ocean

Mesoproterozoic marine successions worldwide record a shift in average δ13C values from 0 to +3.5‰, with the latter value evident in successions younger than 1250 Ma. New carbon isotope data from the ∼1300 to 1270 Ma Dismal Lakes Group, Arctic Canada, provide further insight into this fundamental transition. Data reveal that the shift to higher δ13C values was gradual and marked by occasional excursions to values less than 0‰. When compared to records from older and younger marine successions, it is evident that the difference between isotopic minima and maxima increased with time, indicating that the marine system evolved to become isotopically more variable. We interpret these patterns to record an increase in the crustal inventory of organic carbon, reflecting eukaryotic diversification and a change in the locus of organic carbon burial to include anoxic deep marine sites where preservation potential was high. We speculate that the release of O2 to Earth's surface environments associated with increased organic carbon storage induced irreversible changes in the Mesoproterozoic biosphere, presaging the more extreme environmental and evolutionary developments of the Neoproterozoic.

Lateral gene transfers and the evolution of eukaryotes: theories and data.

Vertical transmission of heritable material, a cornerstone of the Darwinian theory of evolution, is inadequate to describe the evolution of eukaryotes, particularly microbial eukaryotes. This is because eukaryotic cells and eukaryotic genomes are chimeric, having evolved through a combination of vertical (parent to offspring) and lateral (trans-species) transmission. Observations on widespread chimerism in eukaryotes have led to new and revised hypothesis for the origin and diversification of eukaryotes that provide specific predictions on the tempo (early vs continuous transfers) and mode (nature of donor and recipient lineages) of lateral gene transfers (LGTs). Analyses of available data indicate that LGTs in eukaryotes largely fall into two categories: (1) LGTs from organelles to the nucleus, only a few of which appear to have occurred at the time of the origin of eukaryotes, and (2) anomalous LGTs involving diverse donor and recipient lineages. Further testing of hypotheses on the origin and diversification of eukaryotes will require complete genome sequences from a number of diverse eukaryotes and prokaryotes combined with sequences of targeted genes from a broad phylogenetic sample.

Phosphatized biotas from the Neoproterozoic Doushantuo Formation on the Yangtze Platform

The Doushantuo Formation in South China was deposited after the Nantuo glaciation but before the evolution of complex Ediacaran metazoans. It contains multiple taphonomic windows, in its cherts, carbonaceous shales, and phosphorites, onto the late Neoproterozoic biosphere. The phosphatic window is unusually clear; Doushantuo phosphorites at Weng’an (Guizhou Province) are known to exquisitely preserve a multitude of single-celled eukaryotes, multicellular algae, and microscopic animals. Our recent survey reveals that, in addition to the now famous Weng’an locality, Doushantuo phosphorites at Baokang (Hubei), Chadian (Shaanxi), and Shangrao (Jiangxi) also contain diverse eukaryotes preserved at the cellular level. All these phosphorites were deposited in shallow-water environments, typically above fair weather wave base and close to ancient islands. Along with Doushantuo cherts and shales, these phosphorites give us a clearer and more complete picture of late Neoproterozoic biological evolution: there is a remarkable diversification of multicellular eukaryotes shortly after several Neoproterozoic glaciation events.

Morphological and ecological complexity in early eukaryotic ecosystems

Molecular phylogeny and biogeochemistry indicate that eukaryotes differentiated early in Earth history. Sequence comparisons of small-subunit ribosomal RNA genes suggest a deep evolutionary divergence of Eukarya and Archaea; C27-C29 steranes (derived from sterols synthesized by eukaryotes) and strong depletion of 13C (a biogeochemical signature of methanogenic Archaea) in 2,700 Myr old kerogens independently place a minimum age on this split. Steranes, large spheroidal microfossils, and rare macrofossils of possible eukaryotic origin occur in Palaeoproterozoic rocks. Until now, however, evidence for morphological and taxonomic diversification within the domain has generally been restricted to very late Mesoproterozoic and Neoproterozoic successions. Here we show that the cytoskeletal and ecological prerequisites for eukaryotic diversification were already established in eukaryotic microorganisms fossilized nearly 1,500 Myr ago in shales of the early Mesoproterozoic Roper Group in northern Australia.

Neoproterozoic fossils from the Franklin Mountains, northwestern Canada: stratigraphic and palaeobiological implications

Shales from the Lone Land Formation of the Cap Mountain inlier, southern Franklin Mountains, and ‘pre-Palaeozoic’ horizons of a nearby drillhole (Shell Blackwater Lake G-52) have yielded two distinct fossil assemblages. The presence of Trachyhystrichosphaera aimika (in G-52) and Chuaria circularis (in the Lone Land) identifies both sections as Neoproterozoic; previous lithostratigraphic correlations with Mesoproterozoic strata on the Coppermine Homocline are not supported. Marked differences in thermal alteration of the fossils suggest that the two successions are not related despite their present geographic proximity; whereas the G-52 fossils are medium orange in colour, those in the Lone Land are brown. We argue that the Cap Mountain succession is allochthonous and originated probably to the west of its present position. By contrast, the G-52 assemblage shows marked similarity to a fossil in the Wynniatt Formation (Shaler Supergroup) of Victoria Island. Compound and/or coiled filaments are abundant in the G-52 assemblage and appear to be associated generally with exceptional fossil biotas in the Neoproterozoic; insofar as these are likely to document particular environmental conditions, they may help to identify the locus of early eukaryotic diversification. The tendency of some prokaryotes to aggregate and form compound structures also has implications for interpreting various problematic macrofossils, including putative seaweeds from the Palaeoproterozoic Negaunee Iron Formation. We erect a new genus and species, Gemmuloides doncookii n. gen., n. sp. from the Lone Land Formation.

The Santa Barbara Basin is a symbiosis oasis.

It is generally agreed that the origin and initial diversification of Eucarya occurred in the late Archaean or Proterozoic Eons when atmospheric oxygen levels were low and the risk of DNA damage due to ultraviolet radiation was high. Because deep water provides refuge against ultraviolet radiation and early eukaryotes may have been aerotolerant anaerobes, deep-water dysoxic environments are likely settings for primeval eukaryotic diversification. Fossil evidence shows that deep-sea microbial mats, possibly of sulphur bacteria similar to Beggiatoa, existed during that time. Here we report on the eukaryotic community of a modern analogue, the Santa Barbara Basin (California, USA). The Beggiatoa mats of these severely dysoxic and sulphidic sediments support a surprisingly abundant protistan and metazoan meiofaunal community, most members of which harbour prokaryotic symbionts. Many of these taxa are new to science, and both microaerophilic and anaerobic taxa appear to be represented. Compared with nearby aerated sites, the Santa Barbara Basin is a 'symbiosis oasis' offering a new source of organisms for testing symbiosis hypotheses of eukaryogenesis.

The Tangled Web: Gene Genealogies and the Origin of Eukaryotes.

Accessing data from the genomes of organisms (individual genes) and analyzing these data using sophisticated alignment and phylogenetic methods led to the expectation that we would be able to paint a clear picture of the evolution of eukaryotes. Previous analyses based on morphology and ultrastructure failed to pinpoint both the sister taxon to eukaryotes and the branching order of eukaryotic lineages. However, the expectation that molecular data would provide resolution has not been met since a growing number of gene genealogies present conflicting hypotheses for the origin and diversification of eukaryotes. Instead of reconstructing a simple bifurcating tree of life, these gene genealogies have generated a complex picture of eukaryotic genomes whereby ancient lateral transfers (of individual genes or perhaps even entire genomes) has tangled the evolutionary history of eukaryotes. Resolution of these conflicting genealogies comes in recognizing that eukaryotes are chimeric, containing genetic information from multiple ancestral lineages.

Critical analysis of eukaryotic phylogeny: a case study based on the HSP70 family.

Trichomonads, together with diplomonads and microsporidia, emerge at the base of the eukaryotic tree, on the basis of the small subunit rRNA phylogeny. However, phylogenies based on protein sequences such as tubulin are markedly different with these protists emerging much later. We have investigated 70 kDa heat-shock protein (HSP70), which could be a reliable phylogenetic marker. In eukaryotes, HSP70s are found in cytosol, endoplasmic reticulum, and organelles (mitochondria and chloroplasts). In Trichomonas vaginalis we identified nine different HSP70-encoding genes and sequenced three nearly complete cDNAs corresponding to cytosolic, endoplasmic reticulum, and mitochondrial-type HSP70. Phylogenies of eukaryotes were reconstructed using the classical methods while varying the number of species and characters considered. Almost all the undoubtedly monophyletic groups, defined by ultrastructural characters, were recovered. However, due to the long branch attraction phenomenon, the evolutionary rates were the main factor determining the position of species, even with the use of a close outgroup, which is an important advantage of HSP70 with respect to many other markers. Numerous variable sites are peculiar to Trichomonas and probably generated the artefactual placement of this species at the base of the eukaryotes or as the sister group of fast-evolving species. The inter-phyla relationships were not well supported and were sensitive to the reconstruction method, the number of species; and the quantity of information used. This lack of resolution could be explained by the very rapid diversification of eukaryotes, likely after the mitochondrial endosymbiosis.