Early Eukaryotic Evolution Research Articles

Evolutionary trajectory for nuclear functions of ciliary transport complex proteins.

SUMMARYCilia and the nucleus were two defining features of the last eukaryotic common ancestor. In early eukaryotic evolution, these structures evolved through the diversification of a common membrane-coating ancestor, the protocoatomer. While in cilia, the descendants of this protein complex evolved into parts of the intraflagellar transport complexes and BBSome, the nucleus gained its selectivity by recruiting protocoatomer-like proteins to the nuclear envelope to form the selective nuclear pore complexes. Recent studies show a growing number of proteins shared between the proteomes of the respective organelles, and it is currently unknown how ciliary transport proteins could acquire nuclear functions and vice versa. The nuclear functions of ciliary proteins are still observable today and remain relevant for the understanding of the disease mechanisms behind ciliopathies. In this work, we review the evolutionary history of cilia and nucleus and their respective defining proteins and integrate current knowledge into theories for early eukaryotic evolution. We postulate a scenario where both compartments co-evolved and that fits current models of eukaryotic evolution, explaining how ciliary proteins and nucleoporins acquired their dual functions.

Feeding Mechanisms of Pathogenic Protozoa with a Focus on Endocytosis and the Digestive Vacuole

Endocytosis is a quintessential feature of eukaryotes, and the emergence of endocytosis played a major role in the origin and evolution of eukaryotes. During the early evolution of eukaryotes, phagocytosis and the digestion of prey (i.e., bacteria) combined with the endocytosis of macromolecules opened a new source of nutrients beyond osmotrophy. Pathogenic and commensal protozoa have retained endocytosis as a major mechanism of nutrient acquisition even though, in theory, nutrients could be obtained from the host through osmotrophy. Nearly all pathogenic protozoa exhibit endocytosis and have lysosomal-like compartments that function as digestive vacuoles, and endocytosis appears to play a major role in the acquisition of nutrients. Cryptosporidium is a possible exception that may not exhibit endocytosis. Phagotrophy, however, is only observed in parasites of the intestinal lumen and appears to have been lost in blood and tissue parasites. Overall, the basic features of endocytosis and lysosomes are similar to other eukaryotes. Nonetheless, adaptation to the host has generated some novel features that are specific to certain protozoan lineages.

Lateral redox variability in ca. 1.9 Ga marine environments indicated by organic carbon and nitrogen isotope compositions.

The stepwise oxygenation of Earth's surficial environment is thought to have shaped the evolutionary history of life. Microfossil records and molecular clocks suggest eukaryotes appeared during the Paleoproterozoic, perhaps shortly after the Great Oxidation Episode at ca. 2.43 Ga. The mildly oxygenated atmosphere and surface oceans likely contributed to the early evolution of eukaryotes. However, the principal trigger for the eukaryote appearance and a potential factor for their delayed expansion (i.e., intermediate ocean redox conditions until the Neoproterozoic) remain poorly understood, largely owing to a lack of constraints on marine and terrestrial nutrient cycling. Here, we analyzed redox-sensitive element contents and organic carbon and nitrogen isotope compositions of relatively low metamorphic-grade (greenschist facies) black shales preserved in the Flin Flon Belt of central Canada to examine open-marine redox conditions and biological activity around the ca. 1.9 Ga Flin Flon oceanic island arc. The black shale samples were collected from the Reed Lake area in the eastern part of the Flin Flon Belt, and the depositional site was likely distal from the Archean cratons. The black shales have low Al/Ti ratios and are slightly depleted in light rare-earth elements relative to the post-Archean average shale, which is consistent with a limited contribution from felsic igneous rocks in Archean upper continental crust. Redox conditions have likely varied between suboxic and euxinic at the depositional site of the studied section, as suggested by variable U/Al and Mo/Al ratios. Organic carbon and nitrogen isotope compositions of the black shales are approximately -23‰ and +13.7‰, respectively, and these values are systematically higher than those of broadly coeval continental margin deposits (approximately -30‰ for δ13Corg and +5‰ for δ15Nbulk). These elevated values are indicative of high productivity that led to enhanced denitrification (i.e., a high denitrification rate relative to nitrogen influx at the depositional site). Similar geochemical patterns have also been observed in the modern Peruvian oxygen minimum zone where dissolved nitrogen compounds are actively lost from the reservoir via denitrification and anammox, but the large nitrate reservoir of the deep ocean prevents exhaustion of the surface nitrate pool. Nitrogen must have been widely bioavailable in the ca. 1.9 Ga oceans, and its supply to upwelling zones must have supported habitable environments for eukaryotes, even in the middle of oceans around island arcs.

Impact of steroid biosynthesis on the aerobic adaptation ofeukaryotes.

Steroids are indispensable components of the eukaryotic cellular membrane and the acquisition of steroid biosynthesis was a key factor that enabled the evolution of eukaryotes. The polycyclic carbon structures of steroids can be preserved in sedimentary rocks as chemical fossils for billions of years and thus provide invaluable clues to trace eukaryotic evolution from the distant past. Steroid biosynthesis consists of (1) the production of protosteroids and (2) the subsequent modifications toward "modern-type" steroids such as cholesterol and stigmasterol. While protosteroid biosynthesis requires only two genes for the cyclization of squalene, complete modification of protosteroids involves ~10 additional genes. Eukaryotes universally possess at least some of those additional genes and thus produce modern-type steroids as major final products. The geological biomarker records suggest a prolonged period of solely protosteroid production in the mid-Proterozoic before the advent of modern-type steroids in the Neoproterozoic. It has been proposed that mid-Proterozoic protosteroids were produced by hypothetical stem-group eukaryotes that presumably possessed genes only for protosteroid production, even though in modern environments protosteroid production as a final product is found exclusively in bacteria. The host identity of mid-Proterozoic steroid producers is crucial for understanding the early evolution of eukaryotes. In this perspective, we discuss how geological biomarker data and genetic data complement each other and potentially provide a more coherent scenario for the evolution of steroids and associated early eukaryotes. We further discuss the potential impacts that steroids had on the evolution of aerobic metabolism in eukaryotes, which may have been an important factor for the eventual ecological dominance of eukaryotes in many modern environments.

RNA-guided RNA silencing by an Asgard archaeal Argonaute

Argonaute proteins are the central effectors of RNA-guided RNA silencing pathways in eukaryotes, playing crucial roles in gene repression and defense against viruses and transposons. Eukaryotic Argonautes are subdivided into two clades: AGOs generally facilitate miRNA- or siRNA-mediated silencing, while PIWIs generally facilitate piRNA-mediated silencing. It is currently unclear when and how Argonaute-based RNA silencing mechanisms arose and diverged during the emergence and early evolution of eukaryotes. Here, we show that in Asgard archaea, the closest prokaryotic relatives of eukaryotes, an evolutionary expansion of Argonaute proteins took place. In particular, a deep-branching PIWI protein (HrAgo1) encoded by the genome of the Lokiarchaeon ‘Candidatus Harpocratesius repetitus’ shares a common origin with eukaryotic PIWI proteins. Contrasting known prokaryotic Argonautes that use single-stranded DNA as guides and/or targets, HrAgo1 mediates RNA-guided RNA cleavage, and facilitates gene silencing when expressed in human cells and supplied with miRNA precursors. A cryo-EM structure of HrAgo1, combined with quantitative single-molecule experiments, reveals that the protein displays structural features and target-binding modes that are a mix of those of eukaryotic AGO and PIWI proteins. Thus, this deep-branching archaeal PIWI may have retained an ancestral molecular architecture that preceded the functional and mechanistic divergence of eukaryotic AGOs and PIWIs.

Uncoupling the TFIIH Core and Kinase Modules Leads To Misregulated RNA Polymerase II CTD Serine 5 Phosphorylation.

TFIIH is an essential transcription initiation factor for RNA polymerase II (RNApII). This multi-subunit complex comprises two modules that are physically linked by the subunit Tfb3 (MAT1 in metazoans). The TFIIH Core Module, with two DNA-dependent ATPases and several additional subunits, promotes DNA unwinding. The TFIIH Kinase Module phosphorylates Serine 5 of the C-terminal domain (CTD) of RNApII subunit Rpb1, a modification that coordinates exchange of initiation and early elongation factors. While it is not obvious why these two disparate activities are bundled into one factor, the connection may provide temporal coordination during early initiation. Here we show that Tfb3 can be split into two parts to uncouple the TFIIH modules. The resulting cells grow slower than normal, but are viable. Chromatin immunoprecipitation of the split TFIIH shows that the Core Module, but not the Kinase, is properly recruited to promoters. Instead of the normal promoter-proximal peak, high CTD Serine 5 phosphorylation is seen throughout transcribed regions. Therefore, coupling the TFIIH modules is necessary to localize and limit CTD kinase activity to early stages of transcription. These results are consistent with the idea that the two TFIIH modules began as independent functional entities that became connected by Tfb3 during early eukaryotic evolution.

The paleoredox context of early eukaryotic evolution: insights from the Tonian Mackenzie Mountains Supergroup, Canada.

Tonian (ca. 1000-720 Ma) marine environments are hypothesised to have experienced major redox changes coinciding with the evolution and diversification of multicellular eukaryotes. In particular, the earliest Tonian stratigraphic record features the colonisation of benthic habitats by multicellular macroscopic algae, which would have been powerful ecosystem engineers that contributed to the oxygenation of the oceans and the reorganisation of biogeochemical cycles. However, the paleoredox context of this expansion of macroalgal habitats in Tonian nearshore marine environments remains uncertain due to limited well-preserved fossils and stratigraphy. As such, the interdependent relationship between early complex life and ocean redox state is unclear. An assemblage of macrofossils including the chlorophyte macroalga Archaeochaeta guncho was recently discovered in the lower Mackenzie Mountains Supergroup in Yukon (Canada), which archives marine sedimentation from ca. 950-775 Ma, permitting investigation into environmental evolution coincident with eukaryotic ecosystem evolution and expansion. Here we present multi-proxy geochemical data from the lower Mackenzie Mountains Supergroup to constrain the paleoredox environment within which these large benthic macroalgae thrived. Two transects show evidence for basin-wide anoxic (ferruginous) oceanic conditions (i.e., high FeHR/FeT, low Fepy/FeHR), with muted redox-sensitive trace metal enrichments and possible seasonal variability. However, the weathering of sulfide minerals in the studied samples may obscure geochemical signatures of euxinic conditions. These results suggest that macroalgae colonized shallow environments in an ocean that remained dominantly anoxic with limited evidence for oxygenation until ca. 850 Ma. Collectively, these geochemical results provide novel insights into the environmental conditions surrounding the evolution and expansion of benthic macroalgae and the eventual dominance of oxygenated oceanic conditions required for the later emergence of animals.

Meteora sporadica, a protist with incredible cell architecture, is related to Hemimastigophora

"Kingdom-level" branches are being added to the tree of eukaryotes at a rate approaching one per year, with no signs of slowing down.1,2,3,4 Some are completely new discoveries, whereas others are morphologically unusual protists that were previously described but lacked molecular data. For example, Hemimastigophora are predatory protists with two rows of flagella that were known since the 19th century but proved to represent a new deep-branching eukaryote lineage when phylogenomic analyses were conducted.2Meteora sporadica5 is a protist with a unique morphology; cells glide over substrates along a long axis of anterior and posterior projections while a pair of lateral "arms" swing back and forth, a motility system without any obvious parallels. Originally, Meteora was described by light microscopy only, from a short-term enrichment of deep-sea sediment. A small subunit ribosomal RNA (SSU rRNA) sequence was reported recently, but the phylogenetic placement of Meteora remained unresolved.6 Here, we investigated two cultivated Meteora sporadica isolates in detail. Transmission electron microscopy showed that both the anterior-posterior projections and the arms are supported by microtubules originating from a cluster of subnuclear microtubule organizing centers (MTOCs). Neither have a flagellar axoneme-like structure. Sequencing the mitochondrial genome showed this to be among the most gene-rich known, outside jakobids. Remarkably, phylogenomic analyses of 254 nuclear protein-coding genes robustly support a close relationship with Hemimastigophora. Our study suggests that Meteora and Hemimastigophora together represent a morphologically diverse "supergroup" and thus are important for resolving the tree of eukaryote life and early eukaryote evolution.

Components of iron–Sulfur cluster assembly machineries are robust phylogenetic markers to trace the origin of mitochondria and plastids

Establishing the origin of mitochondria and plastids is key to understand 2 founding events in the origin and early evolution of eukaryotes. Recent advances in the exploration of microbial diversity and in phylogenomics approaches have indicated a deep origin of mitochondria and plastids during the diversification of Alphaproteobacteria and Cyanobacteria, respectively. Here, we strongly support these placements by analyzing the machineries for assembly of iron–sulfur ([Fe–S]) clusters, an essential function in eukaryotic cells that is carried out in mitochondria by the ISC machinery and in plastids by the SUF machinery. We assessed the taxonomic distribution of ISC and SUF in representatives of major eukaryotic supergroups and analyzed the phylogenetic relationships with their prokaryotic homologues. Concatenation datasets of core ISC proteins show an early branching of mitochondria within Alphaproteobacteria, right after the emergence of Magnetococcales. Similar analyses with the SUF machinery place primary plastids as sister to Gloeomargarita within Cyanobacteria. Our results add to the growing evidence of an early emergence of primary organelles and show that the analysis of essential machineries of endosymbiotic origin provide a robust signal to resolve ancient and fundamental steps in eukaryotic evolution.

Molecular and morphological characterization of four new ancyromonad genera and proposal for an updated taxonomy of the Ancyromonadida.

Ancyromonads are small biflagellated protists with a bean-shaped morphology. They are cosmopolitan in marine, freshwater, and soil environments, where they attach to surfaces while feeding on bacteria. These poorly known grazers stand out by their uncertain phylogenetic position in the tree of eukaryotes, forming a deep-branching "orphan" lineage that is considered key to a better understanding of the early evolution of eukaryotes. Despite their ecological and evolutionary interest, only limited knowledge exists about their true diversity. Here, we aimed to characterize ancyromonads better by integrating environmental surveys with behavioral observation and description of cell morphology, for which sample isolation and culturing are indispensable. We studied 18 ancyromonad strains, including 14 new isolates and seven new species. We described three new and genetically divergent genera: Caraotamonas, Nyramonas, and Olneymonas, together encompassing four species. The remaining three new species belong to the already-known genera Fabomonas and Ancyromonas. We also raised Striomonas, formerly a subgenus of Nutomonas, to full genus status, on morphological and phylogenetic grounds. We studied the morphology of diverse ancyromonads under light and electron microscopy and carried out molecular phylogenetic analyses, also including 18S rRNA gene sequences from several environmental surveys. Based on these analyses, we have updated the taxonomy of Ancyromonadida.

Shaping eukaryotic epigenetic systems by horizontal gene transfer.

DNA methylation constitutes one of the pillars of epigenetics, relying on covalent bonds for addition and/or removal of chemically distinct marks within the major groove of the double helix. DNA methyltransferases, enzymes which introduce methyl marks, initially evolved in prokaryotes as components of restriction-modification systems protecting host genomes from bacteriophages and other invading foreign DNA. In early eukaryotic evolution, DNA methyltransferases were horizontally transferred from bacteria into eukaryotes several times and independently co-opted into epigenetic regulatory systems, primarily via establishing connections with the chromatin environment. While C5-methylcytosine is the cornerstone of plant and animal epigenetics and has been investigated in much detail, the epigenetic role of other methylated bases is less clear. The recent addition of N4-methylcytosine of bacterial origin as a metazoan DNA modification highlights the prerequisites for foreign gene co-option into the host regulatory networks, and challenges the existing paradigms concerning the origin and evolution of eukaryotic regulatory systems.

Macroscopic carbonaceous compression fossils from the Tonian Liulaobei Formation in the Huainan region of North China

Macroscopic carbonaceous compression fossils are key to understand the early evolution of eukaryotes, explore the development of multicellularity, and strengthen the basis of biostratigraphic correlation during the Tonian Period (ca. 1000–720 Ma). Despite the potential geobiological importance of early macrofossils, the fossil record of Tonian macro-organisms is rarely documented. Here we describe an assemblage of diversified carbonaceous macrofossils from the Tonian Liulaobei Formation in the Huainan region, North China. In this study, we examine a large population of these macrofossils, clarify their taxonomy, and tentatively interpret their phylogenetic affinities. This assemblage consists of thirteen distinct morphotaxa, including eight genera and three new species, showing remarkable taxonomic diversity and domination of coenocytic macroalgae. The new data improve our knowledge about early Neoproterozoic biodiversity, and indicate a Tonian increase in morphological and taxonomic diversity of macrofossils compared to the Mesoproterozoic Era. This study also suggests that macroalgae may have begun to diversify and played a crucial ecological role in Tonian marine ecosystems.

Dynamic seawater redox status in the early Mesoproterozoic: Evidence from trace elements and sulfur isotopic compositions of carbonate associated sulfate in multiple sections

The early Mesoproterozoic (1.6–1.4 Ga) is a critical stage for oxygenation of Earth’s surface and early eukaryote evolution. However, the relationship between both remains uncertain. Here, we provide new carbonate associated sulfate (CAS) sulfur isotopic compositions (δ34SCAS) and trace elements from the 1.6 to 1.55 billion-year-old Gaoyuzhuang Formation in multiple sections within the Yanshan Basin, North China, to investigate the temporal and spatial variation of ocean redox conditions. New and collected δ34SCAS data from five sections (Pingquan, Kuancheng, Qianxi, Jixian and Gan'gou sections) reveal similar sulfur isotopic excursions, but the differences in absolute values indicate spatial heterogeneity of sulfur isotopic compositions, which may reflect marine low-sulfate concentrations and oceanic redox stratification. The most elevated δ34SCAS values appeared at the top of the Second Member of the Gaoyuzhuang Formation, followed by distinct negative excursions at the bottom of the Third Member, suggesting a dynamic sulfur cycle and seawater redox status during this period. Combined with previous reported carbon and sulfur isotopes and some redox proxies (e.g., Ce anomalies, manganese-rich deposit, I/(Mg + Ca) and Fe speciation), we suggest that at least two possible oxygenation events may have occurred in the Gaoyuzhuang Formation: (1) the bottom of the Second Member and (2) the bottom or middle part of the Third Member. Different sections show asynchronous timing of these events, indicating that the redox status was spatial heterogenous within the Yanshan Basin. The spatial heterogeneity may be controlled by facies and paleogeographic locations. Considering that decimeter‐scale multicellular eukaryotes are preserved in the middle part of the Third Member, we argue that oxic bottom water condition may be a critical factor for early eukaryote evolution.

Expanding the molecular and morphological diversity of Apusomonadida, a deep-branching group of gliding bacterivorous protists.

Apusomonads are cosmopolitan bacterivorous biflagellate protists usually gliding on freshwater and marine sediment or wet soils. These nanoflagellates form a sister lineage to opisthokonts and may have retained ancestral features helpful to understanding the early evolution of this large supergroup. Although molecular environmental analyses indicate that apusomonads are genetically diverse, few species have been described. Here, we morphologically characterize 11 new apusomonad strains. Based on molecular phylogenetic analyses of the rRNA gene operon, we describe four new strains of the known species Multimonas media, Podomonas capensis, Apusomonas proboscidea, and Apusomonas australiensis, and rename Thecamonas oxoniensis as Mylnikovia oxoniensis n. gen., n. comb. Additionally, we describe four new genera and six new species: Catacumbia lutetiensis n. gen. n. sp., Cavaliersmithia chaoae n. gen. n. sp., Singekia montserratensis n. gen. n. sp., Singekia franciliensis n. gen. n. sp., Karpovia croatica n. gen. n. sp., and Chelonemonas dolani n. sp. Our comparative analysis suggests that apusomonad ancestor was a fusiform biflagellate with a dorsal pellicle, a plastic ventral surface, and a sleeve covering the anterior flagellum, that thrived in marine, possibly oxygen-poor, environments. It likely had a complex cell cycle with dormant and multiple fission stages, and sex. Our results extend known apusomonad diversity, allow updating their taxonomy, and provide elements to understand early eukaryotic evolution.

Uncovering Pseudogenes and Intergenic Protein-coding Sequences in TriTryps' Genomes.

Trypanosomatids belong to a remarkable group of unicellular, parasitic organisms of the order Kinetoplastida, an early diverging branch of the phylogenetic tree of eukaryotes, exhibiting intriguing biological characteristics affecting gene expression (intronless polycistronic transcription, trans-splicing, and RNA editing), metabolism, surface molecules, and organelles (compartmentalization of glycolysis, variation of the surface molecules, and unique mitochondrial DNA), cell biology and life cycle (phagocytic vacuoles evasion and intricate patterns of cell morphogenesis). With numerous genomic-scale data of several trypanosomatids becoming available since 2005 (genomes, transcriptomes, and proteomes), the scientific community can further investigate the mechanisms underlying these unusual features and address other unexplored phenomena possibly revealing biological aspects of the early evolution of eukaryotes. One fundamental aspect comprises the processes and mechanisms involved in the acquisition and loss of genes throughout the evolutionary history of these primitive microorganisms. Here, we present a comprehensive in silico analysis of pseudogenes in three major representatives of this group: Leishmania major, Trypanosoma brucei, and Trypanosoma cruzi. Pseudogenes, DNA segments originating from altered genes that lost their original function, are genomic relics that can offer an essential record of the evolutionary history of functional genes, as well as clues about the dynamics and evolution of hosting genomes. Scanning these genomes with functional proteins as proxies to reveal intergenic regions with protein-coding features, relying on a customized threshold to distinguish statistically and biologically significant sequence similarities, and reassembling remnant sequences from their debris, we found thousands of pseudogenes and hundreds of open reading frames, with particular characteristics in each trypanosomatid: mutation profile, number, content, density, codon bias, average size, single- or multi-copy gene origin, number and type of mutations, putative primitive function, and transcriptional activity. These features suggest a common process of pseudogene formation, different patterns of pseudogene evolution and extant biological functions, and/or distinct genome organization undertaken by those parasites during evolution, as well as different evolutionary and/or selective pressures acting on distinct lineages.

Redbed formation in the redox-stratified mid-Proterozoic ocean

Deposition of iron-enriched redbeds occurred episodically on different continents throughout the mid-Proterozoic, but their origin remains unclear. Since these sediments host abundant Fe oxides, their occurrence potentially represents changes in ocean-redox state, a hypothesis having significant implications for the evolution of early aerobic eukaryotes. In the present study, we report Fe speciation and isotopes, major and trace elements, organic carbon contents, and mineralogy of the 1.6-Ga Cuizhuang and 1.4-Ga Xiamaling redbeds and intercalated non-redbeds in North China to investigate their depositional environments. As expected, the redbeds show significantly higher total Fe contents (FeT), FeT/Al, and FeHR/FeT ratios (FeHR: highly reactive Fe) than the adjacent non-redbeds (mean FeT: 5.0 % vs. 2.9 %), with 73–97 % of the FeHR in the form of Fe oxides (Feox), accounting for the difference in FeHR/FeT ratios. However, almost all other major (e.g., Al and Ti, typically associated with the detrital fraction) and trace elements show no obvious difference in concentrations between the redbeds and non-redbeds, supporting a single, shared detrital source. The FeT/Al and FeHR/FeT ratios of the redbeds are higher than their respective thresholds for anoxic conditions, whereas the non-redbeds show the opposite. We thus infer that the non-redbeds were deposited in a shallow oxic setting and the redbeds in a deep anoxic setting, separated by a pronounced Fe-redoxcline. The iron was mainly sourced from seafloor hydrothermal fluids and then partially oxidized and precipitated in shallow environments, resulting in positive Fe-isotope values (+0.24 to +0.57‰). Preservation of large amounts of Fe-(hydr)oxides within an anoxic setting can be explained through low-productivity conditions, as inferred from low TOC (mean 0.1 %) and P (mean 452 ppm) contents in both redbeds and non-redbeds. Based on this scenario, modeling indicates that the degree of fractionation of FeHR isotopes (+0.36 to +1.38‰) in the redbeds is consistent with oxidation of 66–98 % of the hydrothermally supplied Fe in waters with an average photic-zone O2 concentration of <0.1 μmol/L (equivalent to atmospheric pO2 < 0.1 % PAL), providing further evidence for extremely low O2 levels during the mid-Proterozoic.

Mesoproterozoic oxygenation event: From shallow marine to atmosphere

AbstractOxygen availability is crucial for the evolution of eukaryotes in geological history, but the redox conditions of the mid-Proterozoic atmospheric-oceanic system remain vigorously debated. Previous geochemical studies suggested a very low mid-Proterozoic atmospheric oxygen level of probably below 0.1%–1% of the present atmospheric level (PAL) with weakly oxygenated surface ocean, which may have suppressed the early evolution of eukaryotes in the ocean. A recent study, however, revealed a pulsed oxygenation event that was recorded in shallow marine carbonate of the middle Gaoyuzhuang Formation (at ca. 1.57 Ga, North China) with atmospheric pO2 of up to ≥4% PAL based on iodine speciation. This event is associated with the earliest known multi-cellular eukaryotic fossils. To elucidate whether this pulsed oxygenation was limited to shallow local seawaters or could also reflect an increase in atmospheric oxygen, chromium (Cr), and carbonate-associated sulfate (CAS), sulfur isotopes in the middle Gaoyuzhuang Formation were studied in two sections of the North China Platform. The results show a positive shift in authigenic Cr isotope from −0.18‰ to +0.66‰, which was followed by a decline to −0.16‰. This suggests a rise in atmospheric oxygen sufficient to initiate oxic Cr cycling and isotope fractionation (pO2 &amp;gt; 0.1%–1% PAL). This positive Cr isotope excursion was associated with a transient positive shift in δ34SCAS from ~20‰ to ~50‰ and a subsequent decline to ~10‰, which provides independent evidence of atmospheric oxygenation. This oxygenation may have enhanced oxidative terrestrial weathering and increased sulfate input to the ocean, thus stimulating bacterial sulfate reduction and pyrite burial in deep anoxic seawaters. This is broadly consistent with previous results of carbonate I/(Ca + Mg) and Ce anomaly but also reveals a lag between shallow seawater and atmospheric oxygenation. Fluctuated redox conditions and decoupled oxygenation between shallow seawater and atmosphere during the mid-Proterozoic may help to account for the current debate.

Characteristics of the carbon cycle in late Mesoproterozoic: Evidence from carbon isotope composition of paired carbonate and organic matter of the Shennongjia Group in South China

The late Mesoproterozoic Era (1300–1000 Ma) was a critical period that witnessed the origin and early evolution of multicellular eukaryotes. Multiple studies have reported observations that the carbon isotope composition of carbonate (δ13Ccarb) underwent a substantial increase after ca. 1250 Ma. The high δ13Ccarb values suggest that the fraction of organic carbon burial (forg) had increased, which, consequently, might have promoted the oxidation of surface environments and the diversification of multicellular eukaryotes. However, details of the carbon cycle during this critical time interval remain elusive, which is pivotal to testing this hypothesis. In this study, we analyzed the stable carbon isotope composition of paired organic matter (δ13Corg) and carbonate, as well as the thermal characteristics of the organic matter, from the Shennongjia Group in South China, which has been constrained to an age of ∼ 1340–1150 Ma. A gradual increase in δ13Ccarb, from ∼–2‰ to >+4‰, is observed in the interval from the middle Shennongjia Group. Above which, the δ13Ccarb declines to ∼–2‰ in the uppermost. The paired δ13Corg values show an extensive range of compositions, from ∼ –22 to –32‰. Raman spectral data revealed that the organic matter in the Shennongjia Group experienced a wide range of thermal history, which might be ascribed to the involvement of detrital organic matter. We reconstructed the Δ13Ccarb-org and forg values in two different scenarios: one included all the δ13Corg data, while the other screened the δ13Corg data to minimize the possible effects of detrital organic matter. The results of these two reconstructions show similar temporal trends. Intriguingly, the Δ13Ccarb-org values are generally larger than the modern counterpart, which can be attributed to higher pCO2. The calculated forg of the Shennongjia Group is generally lower than the modern value, 20%. However, the forg experienced a substantial increase between ca. 1250 and 1190 Ma, suggesting enhanced oxidation of surface environments, which might have paved the way for the diversification of multicellular eukaryotes.

New chronological and paleontological evidence for Paleoproterozoic eukaryote distribution and stratigraphic correlation between the Yanliao and Xiong’er basins, North China Craton

North China Craton is one of the old cratons preserved continues recording of the early evolution of eukaryotes. Organic wall microfossils (OWMs) of eukaryotic affinity have been found in the late Paleoproterozoic sediments from the Yanliao and Xiong’er basins that located in the northern and southern margins of the North China Craton. However, accurate Paleoproterozoic stratigraphic correlation of these two basins still lacks precise chronological and convincing paleontological evidence. Here, we report a SIMS zircon U-Pb age (1647.8 ± 4.3 Ma) from a tuffite layer at the bottom of the Cuizhuang Formation of the Xiong’er Basin, which provides direct chronological evidence for its isochronous deposition with the Chuanlinggou Formation in the Yanliao Basin. Besides, abundant OWMs were recovered from red shales of the Chuanlinggou Formation from the present Taihang Mountains, which is located in the southern branch of the Yanliao Basin and close to the Xiong’er Basin. They are primarily spheroidal microfossils and contain at least one unambiguous unicellular eukaryotic taxa (Valeria lophostriata) and three probable eukaryotic taxa (Schizofusa sinica, Dongyesphaera tenuispina?, large Leiosphaeridia spp.). Our finding further confirms the appearance of unicellular eukaryotes in the Paleoproterozoic ocean and the expanding of their living scopes from the cratonic marginal basin to the intracratonic basin. However, the absence of eukaryotic OWMs in black shales and green shales with more hypoxic depositional waters than those of red shales, indicates that the oxygenated water is probably a key factor to the survival of eukaryotes and even their preservation as OWMs.

Systematic evaluation of horizontal gene transfer between eukaryotes and viruses.

Gene exchange between viruses and their hosts acts as a key facilitator of horizontal gene transfer and is hypothesized to be a major driver of evolutionary change. Our understanding of this process comes primarily from bacteria and phage co-evolution, but the mode and functional importance of gene transfers between eukaryotes and their viruses remain anecdotal. Here we systematically characterized viral-eukaryotic gene exchange across eukaryotic and viral diversity, identifying thousands of transfers and revealing their frequency, taxonomic distribution and projected functions. Eukaryote-derived viral genes, abundant in the Nucleocytoviricota, highlighted common strategies for viral host-manipulation, including metabolic reprogramming, proteolytic degradation and extracellular modification. Furthermore, viral-derived eukaryotic genes implicate genetic exchange in the early evolution and diversification of eukaryotes, particularly through viral-derived glycosyltransferases, which have impacted structures as diverse as algal cell walls, trypanosome mitochondria and animal tissues. These findings illuminate the nature of viral-eukaryotic gene exchange and its impact on the evolution of viruses and their eukaryotic hosts.