Eukaryotic organisms in Proterozoic oceans

The geological record of protists begins well before the Ediacaran and Cambrian diversification of animals, but the antiquity of that history, its reliability as a chronicle of evolution and the causal inferences that can be drawn from it remain subjects of debate. Well-preserved protists are known from a relatively small number of Proterozoic formations, but taphonomic considerations suggest that they capture at least broad aspects of early eukaryotic evolution. A modest diversity of problematic, possibly stem group protists occurs in ca 1800-1300 Myr old rocks. 1300-720 Myr fossils document the divergence of major eukaryotic clades, but only with the Ediacaran-Cambrian radiation of animals did diversity increase within most clades with fossilizable members. While taxonomic placement of many Proterozoic eukaryotes may be arguable, the presence of characters used for that placement is not. Focus on character evolution permits inferences about the innovations in cell biology and development that underpin the taxonomic and morphological diversification of eukaryotic organisms.     

Digging deeper: why we need more Proterozoic algal fossils and how to get them

Known Proterozoic algal fossils raise compelling questions about the origin and diversification of cyanobacteria and eukaryotic algae, and their ecological influence in deep time. This Perspectives article describes particular examples of persistent evolutionary and biogeochemical issues whose resolution would be aided by additional algal fossil evidence from Proterozoic deposits, which have been the subjects of recent intensive study. New Proterozoic geosciences literature relevant to the early diversification of algae is surveyed. Previously underappreciated algal traits that might improve taxonomic attributions of fossil remains are highlighted. Processes that phycologists could use to improve detection of algal fossils are recommended. Potential geological sources of new Proterozoic fossils are suggested.     

Contrasting ecosystem-effects of morphologically similar copepods

Organisms alter the biotic and abiotic conditions of ecosystems. They can modulate the availability of resources to other species (ecosystem engineering) and shape selection pressures on other organisms (niche construction). Very little is known about how the engineering effects of organisms vary among and within species, and, as a result, the ecosystem consequences of species diversification and phenotypic evolution are poorly understood. Here, using a common gardening experiment, we test whether morphologically similar species and populations of Diaptomidae copepods (Leptodiaptomus ashlandi, Hesperodiaptomus franciscanus, Skistodiaptomus oregonensis) have similar or different effects on the structure and function of freshwater ecosystems. We found that copepod species had contrasting effects on algal biomass, ammonium concentrations, and sedimentation rates, and that copepod populations had contrasting effects on prokaryote abundance, sedimentation rates, and gross primary productivity. The average size of ecosystem-effect contrasts between species was similar to those between populations, and was comparable to those between fish species and populations measured in previous common gardening experiments. Our results suggest that subtle morphological variation among and within species can cause multifarious and divergent ecosystem-effects. We conclude that using morphological trait variation to assess the functional similarity of organisms may underestimate the importance of species and population diversity for ecosystem functioning.     

龙凤山藻在澄江早寒武世生物群中的发现

主要报道了产自云南昆明海口耳材村早寒武世筇竹寺组玉案山段澄江生物群中可能为自由漂浮生长的宏观藻类化石--心型龙凤山藻(新种)(Longfengshania cordata sp. nov.)和中华豆芽藻(新属、新种)(Plantulaformis sinensis gen. et sp. nov.).这些化石的发现进一步显示了澄江生物群物种多样性,为揭示该生物群爆发性演化提供了新的证据.通过对龙凤山藻属亲缘关系的深入比较研究,进一步证明该类化石应归属宏观藻类以及它们遗传上的稳定性、演化上的保守性和环境上的适应性.     

龙凤山藻在澄江早寒武世生物群中的发现

主要报道了产自云南昆明海口耳材村早寒武世筇竹寺组玉案山段澄江生物群中可能为漂浮生长的宏观藻类化石-心型龙凤山藻（新种）（Longfengshania cordata sp.nov.)和中华豆芽藻（新属、新种）（lantulaformis sinensis gen.et sp.nov)。这些化石的发现进一步显示了澄江生物群种物多样性,为揭示该生物群爆发性演化提供了新的证据。通过对龙凤山藻属亲缘关系的深入比较研究,进一步证明该类化石应归属宏观藻类以及它们遗传上的稳定性、演化上的保守性和环境上的适应性。     

Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom Fungi

The claim that eukaryotic micro-organisms have global geographic ranges, constituting a significant departure from the situation with macro-organisms, has been supported by studies of morphological species from protistan kingdoms. Here, we examine this claim by reviewing examples from another kingdom of eukaryotic microbes, the Fungi. We show that inferred geographic range of a fungal species depends upon the method of species recognition. While some fungal species defined by morphology show global geographic ranges, when fungal species are defined by phylogenetic species recognition they are typically shown to harbour several to many endemic species. We advance two non-exclusive reasons to explain the perceived difference between the size of geographic ranges of microscopic and macroscopic eukaryotic species when morphological methods of species recognition are used. These reasons are that microbial organisms generally have fewer morphological characters, and that the rate of morphological change will be slower for organisms with less elaborate development and fewer cells. Both of these reasons result in fewer discriminatory morphological differences between recently diverged lineages. The rate of genetic change, moreover, is similar for both large and small organisms, which helps to explain why phylogenetic species of large and small organisms show a more similar distribution of geographic ranges. As a consequence of the different rates in fungi of genetic and morphological changes, genetic isolation precedes a recognizable morphological change. The final step in speciation, reproductive isolation, also follows genetic isolation and may precede morphological change.     

The secretory pathway of protists: spatial and functional organization and evolution.

All cells secrete a diversity of macromolecules to modify their environment or to protect themselves. Eukaryotic cells have evolved a complex secretory pathway consisting of several membrane-bound compartments which contain specific sets of proteins. Experimental work on the secretory pathway has focused mainly on mammalian cell lines or on yeasts. Now, some general principles of the secretory pathway have become clear, and most components of the secretory pathway are conserved between yeast cells and mammalian cells. However, the structure and function of the secretory system in protists have been less extensively studied. In this review, we summarize the current knowledge about the secretory pathway of five different groups of protists: Giardia lamblia, one of the earliest lines of eukaryotic evolution, kinetoplastids, the slime mold Dictyostelium discoideum, and two lineages within the "crown" of eukaryotic cell evolution, the alveolates (ciliates and Plasmodium species) and the green algae. Comparison of these systems with the mammalian and yeast system shows that most elements of the secretory pathway were presumably present in the earliest eukaryotic organisms. However, one element of the secretory pathway shows considerable variation: the presence of a Golgi stack and the number of cisternae within a stack. We suggest that the functional separation of the plasma membrane from the nucleus-endoplasmic reticulum system during evolution required a sorting compartment, which became the Golgi apparatus. Once a Golgi apparatus was established, it was adapted to the various needs of the different organisms.     

Experimental taphonomy of giant sulphur bacteria: implications for the interpretation of the embryo-like Ediacaran Doushantuo fossils

The Ediacaran Doushantuo biota has yielded fossils interpreted as eukaryotic organisms, either animal embryos or eukaryotes basal or distantly related to Metazoa. However, the fossils have been interpreted alternatively as giant sulphur bacteria similar to the extant Thiomargarita. To test this hypothesis, living and decayed Thiomargarita were compared with Doushantuo fossils and experimental taphonomic pathways were compared with modern embryos. In the fossils, as in eukaryotic cells, subcellular structures are distributed throughout cell volume; in Thiomargarita, a central vacuole encompasses approximately 98 per cent cell volume. Key features of the fossils, including putative lipid vesicles and nuclei, complex envelope ornament, and ornate outer vesicles are incompatible with living and decay morphologies observed in Thiomargarita. Microbial taphonomy of Thiomargarita also differed from that of embryos. Embryo tissues can be consumed and replaced by bacteria, forming a replica composed of a three-dimensional biofilm, a stable fabric for potential fossilization. Vacuolated Thiomargarita cells collapse easily and do not provide an internal substrate for bacteria. The findings do not support the hypothesis that giant sulphur bacteria are an appropriate interpretative model for the embryo-like Doushantuo fossils. However, sulphur bacteria may have mediated fossil mineralization and may provide a potential bacterial analogue for other macroscopic Precambrian remains.     

Paleobiological Perspectives on Early Eukaryotic Evolution

Eukaryotic organisms radiated in Proterozoic oceans with oxygenated surface waters, but, commonly, anoxia at depth. Exceptionally preserved fossils of red algae favor crown group emergence more than 1200 million years ago, but older (up to 1600–1800 million years) microfossils could record stem group eukaryotes. Major eukaryotic diversification ∼800 million years ago is documented by the increase in the taxonomic richness of complex, organic-walled microfossils, including simple coenocytic and multicellular forms, as well as widespread tests comparable to those of extant testate amoebae and simple foraminiferans and diverse scales comparable to organic and siliceous scales formed today by protists in several clades. Mid-Neoproterozoic establishment or expansion of eukaryophagy provides a possible mechanism for accelerating eukaryotic diversification long after the origin of the domain. Protists continued to diversify along with animals in the more pervasively oxygenated oceans of the Phanerozoic Eon.Eukaryotic organisms have a long evolutionary history, recorded, in part, by conventional and molecular fossils. For the Phanerozoic Eon (the past 542 million years), eukaryotic evolution is richly documented by the skeletons (and, occasionally, nonskeletal remains) of animals, as well as the leaves, stems, roots, and reproductive organs of land plants. Phylogenetic logic, however, tells us that eukaryotes must have a deeper history, one that began long before the first plant and animal fossils formed. To what extent does the geological record preserve aspects of deep eukaryotic history, and can the chemistry of ancient sedimentary rocks elucidate the environmental conditions under which the eukaryotic cell took shape?     

Genome size of 14 species of fireflies (Insecta,Coleoptera, Lampyridae)

Eukaryotic genome size data are important both as the basis for comparative research into genome evolution and as estimators of the cost and difficulty of genome sequencing programs for non-model organisms.In this study,the genome size of 14 species of fireflies (Lampyridae) (two genera in Lampyrinae,three genera in Luciolinae,and one genus in subfamily incertae sedis) were estimated by propidium iodide (PI)-based flow cytometry.The haploid genome sizes of Lampyridae ranged from 0.42 to 1.31 pg,a 3.1-fold span.Genome sizes of the fireflies varied within the tested subfamilies and genera.Lamprigera and Pyrocoelia species had large and small genome sizes,respectively.No correlation was found between genome size and morphological traits such as body length,body width,eye width,and antennal length.Our data provide additional information on genome size estimation of the firefly family Lampyridae.Furthermore,this study will help clarify the cost and difficulty of genome sequencing programs for non-model organisms and will help promote studies on firefly genome evolution.     

Comparative Genomics of Phylogenetically Diverse Unicellular Eukaryotes Provide New Insights into the Genetic Basis for the Evolution of the Programmed Cell Death Machinery

Programmed cell death (PCD) represents a significant component of normal growth and development in multicellular organisms. Recently, PCD-like processes have been reported in single-celled eukaryotes, implying that some components of the PCD machinery existed early in eukaryotic evolution. This study provides a comparative analysis of PCD-related sequences across more than 50 unicellular genera from four eukaryotic supergroups: Unikonts, Excavata, Chromalveolata, and Plantae. A complex set of PCD-related sequences that correspond to domains or proteins associated with all main functional classes—from ligands and receptors to executors of PCD—was found in many unicellular lineages. Several PCD domains and proteins previously thought to be restricted to animals or land plants are also present in unicellular species. Noteworthy, the yeast, Saccharomyces cerevisiae—used as an experimental model system for PCD research, has a rather reduced set of PCD-related sequences relative to other unicellular species. The phylogenetic distribution of the PCD-related sequences identified in unicellular lineages suggests that the genetic basis for the evolution of the complex PCD machinery present in extant multicellular lineages has been established early in the evolution of eukaryotes. The shaping of the PCD machinery in multicellular lineages involved the duplication, co-option, recruitment, and shuffling of domains already present in their unicellular ancestors. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

A molecular phylogenetic analysis of reproductive trait evolution in the soft coral genus Alcyonium

The soft coral genus Alcyonium is among the most reproductively diverse invertebrate taxa known: The genus includes species that vary both in mode of reproduction (including broadcast spawners, internal brooders, and external brooders) and sexual expression (gonochores, hermaphrodites, and a unisexual parthenogen). Such diversity offers a unique opportunity to examine associations between reproductive and morphological traits in a phylogenetic context. We used an approximately 900-bp sequence of the nuclear ribosomal gene complex spanning the internal transcribed spacer (ITS) regions to construct a molecular phylogeny for 14 European and North American species of Alcyonium onto which we mapped the known distribution of reproductive and morphological traits. The phylogeny suggests that hermaphroditism or parthenogenesis has evolved independently at least twice in this genus, and always in internally brooding species. Broadcast spawning and external brooding only occur in species with large colony size, whereas all species with small colony size brood their larvae internally. Internal brooding and small size appear to be ancestral in this genus; if this is the case, an association between broadcast spawning and large colony size has evolved independently in at least two clades. This tendency of small adults to brood their larvae while large adults broadcast spawn them into the plankton has been observed in a variety of solitary invertebrate taxa, but to date has not been documented in any other colonial invertebrates. Moreoever, it has been suggested that organisms with a colonial growth form should not experience the allometric constraints on brood space that have been proposed to explain the association between adult size and mode of reproduction in solitary organisms. Unlike many other colonial groups, however, module (polyp) size is strongly correlated with colony size in Alcyonium, and constraints on brooding may be imposed by module, rather than colony, allometry. The very close genetic relationship (< 1% sequence divergence) and shared polymorphisms among A. digitatum (a large, gonochoric broadcast spawner), A. siderium, and A. sp. A (intermediate-sized and small hermaphroditic, internal brooders) suggest that evolutionary transitions between broadcast spawning and brooding and between gonochorism and hermaphroditism can occur easily and rapidly in this group.     

Origins and evolution of the formin multigene family that is involved in the formation of actin filaments

In eukaryotes, the assembly and elongation of unbranched actin filaments is controlled by formins, which are long, multidomain proteins. These proteins are important for dynamic cellular processes such as determination of cell shape, cell division, and cellular interaction. Yet, no comprehensive study has been done about the origins and evolution of this gene family. We therefore performed extensive phylogenetic and motif analyses of the formin genes by examining 597 prokaryotic and 53 eukaryotic genomes. Additionally, we used three-dimensional protein structure data in an effort to uncover distantly related sequences. Our results suggest that the formin homology 2 (FH2) domain, which promotes the formation of actin filaments, is a eukaryotic innovation and apparently originated only once in eukaryotic evolution. Despite the high degree of FH2 domain sequence divergence, the FH2 domains of most eukaryotic formins are predicted to assume the same fold and thus have similar functions. The formin genes have experienced multiple taxon-specific duplications and followed the birth-and-death model of evolution. Additionally, the formin genes experienced taxon-specific genomic rearrangements that led to the acquisition of unrelated protein domains. The evolutionary diversification of formin genes apparently increased the number of formin's interacting molecules and consequently contributed to the development of a complex and precise actin assembly mechanism. The diversity of formin types is probably related to the range of actin-based cellular processes that different cells or organisms require. Our results indicate the importance of gene duplication and domain acquisition in the evolution of the eukaryotic cell and offer insights into how a complex system, such as the cytoskeleton, evolved.     

Genomic signatures of evolution in Nautilus—An endangered living fossil

Living fossils are survivors of previously more diverse lineages that originated millions of years ago and persisted with little morphological change. Therefore, living fossils are model organisms to study both long‐term and ongoing adaptation and speciation processes. However, many aspects of living fossil evolution and their persistence in the modern world remain unclear. Here, we investigate three major aspects of the evolutionary history of living fossils: cryptic speciation, population genetics and effective population sizes, using members of the genera Nautilus and Allonautilus as classic examples of true living fossils. For this, we analysed genomewide ddRAD‐Seq data for all six currently recognized nautiloid species throughout their distribution range. Our analyses identified three major allopatric Nautilus clades: a South Pacific clade, subdivided into three subclades with no signs of admixture between them; a Coral Sea clade, consisting of two genetically distinct populations with significant admixture; and a widespread Indo‐Pacific clade, devoid of significant genetic substructure. Within these major clades, we detected five Nautilus groups, which likely correspond to five distinct species. With the exception of Nautilus macromphalus, all previously described species are at odds with genomewide data, testifying to the prevalence of cryptic species among living fossils. Detailed F_ST analyses further revealed significant genome‐wide and locus‐specific signatures of selection between species and differentiated populations, which is demonstrated here for the first time in a living fossil. Finally, approximate Bayesian computation (ABC) simulations suggest large effective population sizes, which may explain the low levels of population differentiation commonly observed in living fossils.     

On the constructive possibilities of the Riphean microfossils Eosaccharomyces

Yeast-like microfossils from the Meso-Neoproterozoic boundary beds of the Neruyen Formation (southeastern Siberia) are studied. The structural features of the fossil organisms the life cycle of which started with the development of single budding cells that subsequently formed complex multicellular microcolonies are described. Ancient yeast-like cells possessed a number of adaptive strategies. The ability of revertation (backward growth) led to the formation of a closed space. The pseudomycelial structure was improved by means of its modular organization. The morphological change and enlargement of some cells in a colony were regulated by cooperation between cells. The presence of Riphean yeast-like fossils in billion-year-old rocks may suggest the radiation of Ascomycota in the Mesoproterozoic Eon.     

Novel Features of Eukaryotic Photosystem II Revealed by Its Crystal Structure Analysis from a Red Alga

Photosystem II (PSII) catalyzes light-induced water splitting, leading to the evolution of molecular oxygen indispensible for life on the earth. The crystal structure of PSII from cyanobacteria has been solved at an atomic level, but the structure of eukaryotic PSII has not been analyzed. Because eukaryotic PSII possesses additional subunits not found in cyanobacterial PSII, it is important to solve the structure of eukaryotic PSII to elucidate their detailed functions, as well as evolutionary relationships. Here we report the structure of PSII from a red alga Cyanidium caldarium at 2.76 Å resolution, which revealed the structure and interaction sites of PsbQ′, a unique, fourth extrinsic protein required for stabilizing the oxygen-evolving complex in the lumenal surface of PSII. The PsbQ′ subunit was found to be located underneath CP43 in the vicinity of PsbV, and its structure is characterized by a bundle of four up-down helices arranged in a similar way to those of cyanobacterial and higher plant PsbQ, although helices I and II of PsbQ′ were kinked relative to its higher plant counterpart because of its interactions with CP43. Furthermore, two novel transmembrane helices were found in the red algal PSII that are not present in cyanobacterial PSII; one of these helices may correspond to PsbW found only in eukaryotic PSII. The present results represent the first crystal structure of PSII from eukaryotic oxygenic organisms, which were discussed in comparison with the structure of cyanobacterial PSII.     

Oldest fossil ciliates from the Cryogenian glacial interlude reinterpreted as possible red algal spores

The Cryogenian Period experienced two long lived global glaciations known as Snowball Earths. While these events were dramatic, eukaryotic life persisted through them, and fossil evidence shows that eukaryotes thrived during the c. 30-million-year interlude between the glaciations. Carbonate successions have become an important taphonomic window for this interval. One of the most notable examples is the c. 662–635 Ma Taishir Formation (Tsagaan Olom Group, Zavkhan Terrane, Mongolia) which has yielded a number of eukaryotic fossil taxa. Here, we examine more closely the morphology and taxonomic affinity of some of these Taishir fossils previously interpreted as remains of ciliate tintinnid loricae (purportedly the oldest fossil ciliates). New morphological and ultrastructural analyses indicate that these fossils are not ciliate tintinnids. Instead, we propose a new interpretation: that they are algal reproductive structures related to coeval macroscopic organic warty sheets described as putative red algae. We report the first occurrence of these fossils in the earliest Ediacaran Ol Formation, indicating that this taxon persisted through the Marinoan Snowball Earth. A new interpretation of these fossils as putative red algal spores has broad implications for our understanding of biodiversity in the Neoproterozoic Era, specifically during the Cryogenian Period, and for the antiquity of ciliates.     

Biodiversity and application of microalgae

The algae are a polyphyletic, artificial assemblage of O₂-evolving, photosynthetic organisms (and secondarily nonphotosynthetic evolutionary descendants) that includes seaweeds (macroalgae) and a highly diverse group of microorganisms known as microalgae. Phycology, the study of algae, developed historically as a discipline focused on the morphological, physiological and ecological similarities of the subject organisms, including the prokaryotic bluegreen algae (cyanobacteria) and prochlorophytes. Eukaryotic algal groups represent at least five distinct evolutionary lineages, some of which include protists traditionally recognized as fungi and protozoa. Ubiquitous in marine, freshwater and terrestrial habitats and possessing broad biochemical diversity, the number of algal species has been estimated at between one and ten million, most of which are microalgae. The implied biochemical diversity is the basis for many biotechnological and industrial applications.     

Rapid Transition towards the Division of Labor via Evolution of Developmental Plasticity

A crucial step in several major evolutionary transitions is the division of labor between components of the emerging higher-level evolutionary unit. Examples include the separation of germ and soma in simple multicellular organisms, appearance of multiple cell types and organs in more complex organisms, and emergence of casts in eusocial insects. How the division of labor was achieved in the face of selfishness of lower-level units is controversial. I present a simple mathematical model describing the evolutionary emergence of the division of labor via developmental plasticity starting with a colony of undifferentiated cells and ending with completely differentiated multicellular organisms. I explore how the plausibility and the dynamics of the division of labor depend on its fitness advantage, mutation rate, costs of developmental plasticity, and the colony size. The model shows that the transition to differentiated multicellularity, which has happened many times in the history of life, can be achieved relatively easily. My approach is expandable in a number of directions including the emergence of multiple cell types, complex organs, or casts of eusocial insects.