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Abstract We tracked temporal changes in protist diversity at the Long Term Ecological Research (LTER) station MareChiara in the Gulf of Naples (Mediterranean Sea) on eight dates in 2011 using a metabarcoding approach. Illumina analysis of the V4 and V9 fragments of the 18S rDNA produced 869 522 and 1 410 071 sequences resulting in 6517 and 6519 OTUs, respectively. Marked compositional variations were recorded across the year, with less than 2% of OTUs shared among all samples and similar patterns for the two marker tags. Alveolata, Stramenopiles and Rhizaria were the most represented groups. A comparison with light microscopy data indicated an over-representation of Dinophyta in the sequence dataset, whereas Bacillariophyta showed comparable taxonomic patterns between sequence and light microscopy data. Shannon diversity values were stable from February to September, increasing thereafter with a peak in December. Community variance was mainly explained by seasonality (as temperature), trophic status (as chlorophyll a), and influence of coastal waters (as salinity). Overall, the background knowledge of the system provided a sound context for the result interpretation, showing that LTER sites provide an ideal setting for high-throughput sequencing (HTS) metabarcoding characterisation of protist assemblages and their relationships with environmental variations. Temporal diversity and community structure of the entire protist assemblage from the Gulf of Naples assessed using high throughput sequencing and light microscopy.

An in situ imaging technique has been used to show that large rhizarian plankton represent a much larger biomass than previously thought, meaning that they are likely to make an important contribution to ocean ecosystems. Rhizaria are major players in ocean ecology Ocean ecosystems are inhabited by planktonic organisms spanning a wide size range, with large zooplankton feeding on smaller species and thereby contributing to the marine food web and carbon cycling. However, our understanding of the role and contribution of fragile and large zooplankton to the marine ecosystem is limited. Using data collected by an in situ imaging system during the Tara Oceans global survey, Tristan Biard et al . quantified the respective contributions of Rhizaria (a broad phylogenetic group of marine protists) and other zooplankton larger than 600 μm, finding that they represent a much larger biomass than previously appreciated, contributing up to 5.2% of the total oceanic biota carbon reservoir. These findings highlight the important contribution of Rhizaria to plankton biomass, primary productivity and other biogeochemical processes in the oceans. Planktonic organisms play crucial roles in oceanic food webs and global biogeochemical cycles 1 , 2 . Most of our knowledge about the ecological impact of large zooplankton stems from research on abundant and robust crustaceans, and in particular copepods 3 , 4 . A number of the other organisms that comprise planktonic communities are fragile, and therefore hard to sample and quantify, meaning that their abundances and effects on oceanic ecosystems are poorly understood. Here, using data from a worldwide in situ imaging survey of plankton larger than 600 μm, we show that a substantial part of the biomass of this size fraction consists of giant protists belonging to the Rhizaria, a super-group of mostly fragile unicellular marine organisms that includes the taxa Phaeodaria and Radiolaria (for example, orders Collodaria and Acantharia). Globally, we estimate that rhizarians in the top 200 m of world oceans represent a standing stock of 0.089 Pg carbon, equivalent to 5.2% of the total oceanic biota carbon reservoir 5 . In the vast oligotrophic intertropical open oceans, rhizarian biomass is estimated to be equivalent to that of all other mesozooplankton (plankton in the size range 0.2–20 mm). The photosymbiotic association of many rhizarians with microalgae may be an important factor in explaining their distribution. The previously overlooked importance of these giant protists across the widest ecosystem on the planet 6 changes our understanding of marine planktonic ecosystems.

Passive sinking of particulate organic matter (POM) is the main mechanism through which the biological pump transports surface primary production to the ocean interior. However, the contribution and variability of different biological sources to vertical export is not fully understood. Here, we use DNA metabarcoding of the 18S rRNA gene and particle interceptor traps (PITs) to characterize the taxonomic composition of particles sinking out of the photic layer in the California Current Ecosystem (CCE), a productive system with high export potential. The PITs included formalin-fixed and ‘live’ traps to investigate eukaryotic communities involved in the export and remineralization of sinking particles. Sequences affiliated with Radiolaria dominated the eukaryotic assemblage in fixed traps (90%), with Dinophyta and Metazoa making minor contributions. The prominence of Radiolaria decreased drastically in live traps, possibly due to selective consumption by copepods, heterotrophic nanoflagellates, and phaeodarians that were heavily enriched in these traps. These patterns were consistent across the water masses surveyed extending from the coast to offshore, despite major differences in productivity and trophic st

An accurate reconstruction of the eukaryotic tree of life is essential to identify the innovations underlying the diversity of microbial and macroscopic (e.g., plants and animals) eukaryotes. Previous work has divided eukaryotic diversity into a small number of high-level “supergroups,” many of which receive strong support in phylogenomic analyses. However, the abundance of data in phylogenomic analyses can lead to highly supported but incorrect relationships due to systematic phylogenetic error. Furthermore, the paucity of major eukaryotic lineages (19 or fewer) included in these genomic studies may exaggerate systematic error and reduce power to evaluate hypotheses. Here, we use a taxon-rich strategy to assess eukaryotic relationships. We show that analyses emphasizing broad taxonomic sampling (up to 451 taxa representing 72 major lineages) combined with a moderate number of genes yield a well-resolved eukaryotic tree of life. The consistency across analyses with varying numbers of taxa (88–451) and levels of missing data (17–69%) supports the accuracy of the resulting topologies. The resulting stable topology emerges without the removal of rapidly evolving genes or taxa, a practice common to phylogenomic analyses. Several major groups are stable and strongly supported in these analyses (e.g., SAR, Rhizaria, Excavata), whereas the proposed supergroup “Chromalveolata” is rejected. Furthermore, extensive instability among photosynthetic lineages suggests the presence of systematic biases including endosymbiotic gene transfer from symbiont (nucleus or plastid) to host. Our analyses demonstrate that stable topologies of ancient evolutionary relationships can be achieved with broad taxonomic sampling and a moderate number of genes. Finally, taxon-rich analyses such as presented here provide a method for testing the accuracy of relationships that receive high bootstrap support (BS) in phylogenomic analyses and enable placement of the multitude of lineages that lack genome scale data.

Phytomyxea (SAR: Rhizaria: Endomyxa) is a group of obligate biotrophic parasitic protists comprised of two orders: Plasmodiophorida, found in terrestrial or freshwater environments, and Phagomyxida, found in marine environments. While Plasmodiophorida has been extensively studied due to its economic importance as plant pathogens, Phagomyxida remains poorly investigated despite its ecological significance in marine ecosystems. During intensive sampling along the Korean coast from April to December 2023, novel parasitoids infecting dinoflagellates were discovered in seawater collected at 10 coastal stations. A total of 23 isolates were successfully established in culture, and the morphology of infected host cells resembled that of known Phagomyxa infections. The newly identified parasitoid exhibits a life cycle that includes zoospore penetration, multinucleate plasmodium development, and formation of a sporangiosorus composed of numerous zoosporangia. Each zoosporangium produces three biflagellate zoospores, and no resting spores were observed. A key morphological feature distinguishing this parasitoid from Phagomyxa species is the presence of a sporangiosorus wall enclosing the zoosporangia. Phylogenetic analysis based on small subunit (SSU) ribosomal DNA (rDNA) revealed that this parasitoid forms a distinct clade with Marinomyxa and the environmental sequence TAGIRI-5, suggesting a disparity between its morphological similarity to Phagomyxa and its molecular phylogenetic position. The SSU rRNA gene sequence of the new parasitoid showed 99.87% identity to the TAGIRI-5 sequence obtained from an anoxic sediment in Kagoshima Bay, Japan. Cross-infection experiments demonstrated that infections occurred only in five dinoflagellate genera among the taxa tested. Based on morphological and molecular data obtained in this study, we propose a new genus and species, Dinopallor comventus n. gen., n. sp., for this newly discovered parasitoid.

The innovation of the eukaryote cytoskeleton enabled phagocytosis, intracellular transport, and cytokinesis, and is largely responsible for the diversity of morphologies among eukaryotes. Still, the relationship between phenotypic innovations in the cytoskeleton and their underlying genotype is poorly understood. To explore the genetic mechanism of morphological evolution of the eukaryotic cytoskeleton, we provide the first single cell transcriptomes from uncultured, free-living unicellular eukaryotes: the polycystine radiolarian Lithomelissa setosa (Nassellaria) and Sticholonche zanclea (Taxopodida). A phylogenomic approach using 255 genes finds Radiolaria and Foraminifera as separate monophyletic groups (together as Retaria), while Cercozoa is shown to be paraphyletic where Endomyxa is sister to Retaria. Analysis of the genetic components of the cytoskeleton and mapping of the evolution of these on the revised phylogeny of Rhizaria reveal lineage-specific gene duplications and neofunctionalization of α and β tubulin in Retaria, actin in Retaria and Endomyxa, and Arp2/3 complex genes in Chlorarachniophyta. We show how genetic innovations have shaped cytoskeletal structures in Rhizaria, and how single cell transcriptomics can be applied for resolving deep phylogenies and studying gene evolution in uncultured protist species.

Rapidly improving DNA sequencing technology has revolutionized our ability to efficiently survey the biodiversity of microbial life. We are now equipped to investigate protistan richness and community dynamics on scales that would not have been imaginable with traditional observational methods. However, for most taxa the relationship between DNA sequences and morphologically-defined species is poorly understood, and morphology has remained the cornerstone of taxonomy for centuries. To better utilize the wealth of sequence data being collected, we must understand how it relates to entities such as individuals, populations, and species. Here we use a combined microscopy and sequencing approach to unveil the striking intragenomic and intraspecies genetic variation in one group of ecologically-important marine protists, the polycystine Radiolaria. Long-read 18S rRNA gene amplicon data from 173 isolated and morphologically-identified radiolarians showed that the vast majority (90%) yielded multiple sequence variants per specimen. Furthermore, every morphospecies analyzed displayed a range of different genetic signatures. Intraspecies genetic variability was expressed as specimens having different assemblages of ASVs, different dominant ASVs, or having no ASVs in common with other specimens of the same morphospecies. By integrating morphological and molecular information, we begin to parse the genetic richness of Radiolaria in ocean environments, as well as illuminate relationships between taxa, and their poorly-known life stages. Our findings emphasize the need to account for protists’ taxon-specific sequence variability, particularly their intragenomic and intraspecies genetic variation, in interpreting metabarcoding diversity survey data.

Picoeukaryotes play prominent roles in the biogeochemical cycles in marine ecosystems. However, their molecular diversity studies have been confined in marine surface waters or shallow coastal sediments. Here, we investigated the diversity and metabolic activity of picoeukaryotic communities at depths ranging from the surface to the abyssopelagic zone in the western Pacific Ocean above the north and south slopes of the Mariana Trench. This was achieved by amplifying and sequencing the V4 region of both 18S ribosomal DNA and cDNA using Illumina HiSeq sequencing. Our study revealed: (1) Four super-groups (i.e., Alveolata, Opisthokonta, Rhizaria and Stramenopiles) dominated the picoeukaryote assemblages through the water column, although they accounted for different proportions at DNA and cDNA levels. Our data expand the deep-sea assemblages from current bathypelagic to abyssopelagic zones. (2) Using the cDNA-DNA ratio as a proxy of relative metabolic activity, the highest activity for most subgroups was usually found in the mesopelagic zone; and (3) Population shift along the vertical scale was more prominent than that on the horizontal differences, which might be explained by the sharp physicochemical gradients along the water depths. Overall, our study provides a better understanding of the diversity and metabolic activity of picoeukaryotes in water columns of the deep ocean in response to varying environmental conditions.

The biostratigraphically important Permian radiolarian genera Pseudoalbaillella sensu stricto and Follicucullus (Follicucullidae, Polycystinea) are discriminated by morphological gaps in their wings and segmentation. Previous statistical analyses demonstrated that Longtanella fills morphological gaps between these two genera. Longtanella has long been regarded as a junior synonym of Parafollicucullus , and only a few species have been described. Herein several true Longtanella species are recognized from South China, and eight new species and five indeterminate species are described and illustrated to prove the validity of the genus Longtanella . In addition, a new genus, Parafollicucullinoides gen. nov., is described. Their palaeogeographic distributions and living environments are explored by applying correspondence analysis (CA), with occurrence datasets of selected fusulinacean genera from the Japanese Islands, China and Sundaland. CA results indicate that Longtanella was present to a limited extent in warmer conditions in the fusulinacean Province B and C during Kungurian–Roadian time, and possibly lived above the thermocline and below the deepest limit of fusulinaceans. The Pseudoalbaillella and the Follicucullus group preferred open ocean conditions, living below the thermocline and distributed not only in the ‘Equatorial Warm Water Province’, but also the northern peri-Gondwana Cool Water Province and the southern North Cool Water Province.

Background Recent phylogenomic analyses have revolutionized our view of eukaryote evolution by revealing unexpected relationships between and within the eukaryotic supergroups. However, for several groups of uncultivable protists, only the ribosomal RNA genes and a handful of proteins are available, often leading to unresolved evolutionary relationships. A striking example concerns the supergroup Rhizaria, which comprises several groups of uncultivable free-living protists such as radiolarians, foraminiferans and gromiids, as well as the parasitic plasmodiophorids and haplosporids. Thus far, the relationships within this supergroup have been inferred almost exclusively from rRNA, actin, and polyubiquitin genes, and remain poorly resolved. To address this, we have generated large Expressed Sequence Tag (EST) datasets for 5 species of Rhizaria belonging to 3 important groups: Acantharea ( Astrolonche sp., Phyllostaurus sp. ), Phytomyxea ( Spongospora subterranea, Plasmodiophora brassicae ) and Gromiida ( Gromia sphaerica ). Results 167 genes were selected for phylogenetic analyses based on the representation of at least one rhizarian species for each gene. Concatenation of these genes produced a supermatrix composed of 36,735 amino acid positions, including 10 rhizarians, 9 stramenopiles, and 9 alveolates. Phylogenomic analyses of this large dataset revealed a strongly supported clade grouping Foraminifera and Acantharea. The position of this clade within Rhizaria was sensitive to the method employed and the taxon sampling: Maximum Likelihood (ML) and Bayesian analyses using empirical model of evolution favoured an early divergence, whereas the CAT model and ML analyses with fast-evolving sites or the foraminiferan species Reticulomyxa filosa removed suggested a derived position, closely related to Gromia and Phytomyxea. In contrast to what has been previously reported, our analyses also uncovered the presence of the rhizarian-specific polyubiquitin insertion in Acantharea. Finally, this work reveals another possible rhizarian signature in the 60S ribosomal protein L10a. Conclusions Our study provides new insights into the evolution of Rhizaria based on phylogenomic analyses of ESTs from three groups of previously under-sampled protists. It was enabled through the application of a recently developed method of transcriptome analysis, requiring very small amount of starting material. Our study illustrates the potential of this method to elucidate the early evolution of eukaryotes by providing large amount of data for uncultivable free-living and parasitic protists.