Explore the vast range of titles available.

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.

Mixotrophy, or the ability to acquire carbon from both auto- and heterotrophy, is a widespread ecological trait in marine protists. Using a metabarcoding dataset of marine plankton from the global ocean, 318,054 mixotrophic metabarcodes represented by 89,951,866 sequences and belonging to 133 taxonomic lineages were identified and classified into four mixotrophic functional types: constitutive mixotrophs (CM), generalist non-constitutive mixotrophs (GNCM), endo-symbiotic specialist non-constitutive mixotrophs (eSNCM), and plastidic specialist non-constitutive mixotrophs (pSNCM). Mixotrophy appeared ubiquitous, and the distributions of the four mixotypes were analyzed to identify the abiotic factors shaping their biogeographies. Kleptoplastidic mixotrophs (GNCM and pSNCM) were detected in new zones compared to previous morphological studies. Constitutive and non-constitutive mixotrophs had similar ranges of distributions. Most lineages were evenly found in the samples, yet some of them displayed strongly contrasted distributions, both across and within mixotypes. Particularly divergent biogeographies were found within endo-symbiotic mixotrophs, depending on the ability to form colonies or the mode of symbiosis. We showed how metabarcoding can be used in a complementary way with previous morphological observations to study the biogeography of mixotrophic protists and to identify key drivers of their biogeography.

Grazing rate estimates indicate that approximately half of the bacterivory in oligotrophic oceans is due to mixotrophic flagellates (MFs). However, most estimations have considered algae as a single group. Here we aimed at opening the black-box of the phytoflagellates (PFs) <20 μm. Haptophytes, chlorophytes, cryptophytes and pigmented dinoflagellates were identified using fluorescent in situ hybridization or by standard 4′,6-diamidino-2-phenylindole staining. Their fluctuations in abundance, cell size, biomass and bacterivory rates were measured through an annual cycle in an oligotrophic coastal system. On average, we were able to assign to these groups: 37% of the total pico-PFs and 65% of the nano-PFs composition. Chlorophytes were mostly picoplanktonic and they never ingested fluorescently labeled bacteria. About 50% of the PF <20 μm biomass was represented by mixotrophic algae. Pigmented dinoflagellates were the least abundant group with little impact on bacterioplankton. Cryptophytes were quantitatively important during the coldest periods and explained about 4% of total bacterivory. Haptophytes were the most important mixotrophic group: (i) they were mostly represented by cells 3–5 μm in size present year-round; (ii) cell-specific grazing rates were comparable to those of other bacterivorous non-photosynthetic organisms, regardless of the in situ nutrient availability conditions; (iii) these organisms could acquire a significant portion of their carbon by ingesting bacteria; and (iv) haptophytes explained on average 40% of the bacterivory exerted by MFs and were responsible for 9–27% of total bacterivory at this site. Our results, when considered alongside the widespread distribution of haptophytes in the ocean, indicate that they have a key role as bacterivores in marine ecosystems.

A planetary-scale understanding of the ocean ecosystem, particularly in light of climate change, is crucial. Here, we review the work of Tara Oceans, an international, multidisciplinary project to assess the complexity of ocean life across comprehensive taxonomic and spatial scales. Using a modified sailing boat, the team sampled plankton at 210 globally distributed sites at depths down to 1,000 m. We describe publicly available resources of molecular, morphological and environmental data, and discuss how an ecosystems biology approach has expanded our understanding of plankton diversity and ecology in the ocean as a planetary, interconnected ecosystem. These efforts illustrate how global-scale concepts and data can help to integrate biological complexity into models and serve as a baseline for assessing ecosystem changes and the future habitability of our planet in the Anthropocene epoch.The schooner Tara sailed 140,000 km across the global oceans to sample diverse marine ecosystems and plankton communities. In the Review, members of the Tara Oceans project highlight how resulting data can be used for an integrated understanding of ocean biology.

While our knowledge about the roles of microbes and viruses in the ocean has increased tremendously due to recent advances in genomics and metagenomics, research on marine microbial eukaryotes and zooplankton has benefited much less from these new technologies because of their larger genomes, their enormous diversity, and largely unexplored physiologies. Here, we use a metatranscriptomics approach to capture expressed genes in open ocean Tara Oceans stations across four organismal size fractions. The individual sequence reads cluster into 116 million unigenes representing the largest reference collection of eukaryotic transcripts from any single biome. The catalog is used to unveil functions expressed by eukaryotic marine plankton, and to assess their functional biogeography. Almost half of the sequences have no similarity with known proteins, and a great number belong to new gene families with a restricted distribution in the ocean. Overall, the resource provides the foundations for exploring the roles of marine eukaryotes in ocean ecology and biogeochemistry. Marine microbial eukaryotes and zooplankton display enormous diversity and largely unexplored physiologies. Here, the authors use metatranscriptomics to analyze four organismal size fractions from open-ocean stations, providing the largest reference collection of eukaryotic transcripts from any single biome.

Biosilicification (the formation of biological structures from silica) occurs in diverse eukaryotic lineages, plays a major role in global biogeochemical cycles, and has significant biotechnological applications. Silicon (Si) uptake is crucial for biosilicification, yet the evolutionary history of the transporters involved remains poorly known. Recent evidence suggests that the SIT family of Si transporters, initially identified in diatoms, may be widely distributed, with an extended family of related transporters (SIT-Ls) present in some nonsilicified organisms. Here, we identify SITs and SIT-Ls in a range of eukaryotes, including major silicified lineages (radiolarians and chrysophytes) and also bacterial SIT-Ls. Our evidence suggests that the symmetrical 10-transmembrane-domain SIT structure has independently evolved multiple times via duplication and fusion of 5-transmembrane-domain SIT-Ls. We also identify a second gene family, similar to the active Si transporter Lsi2, that is broadly distributed amongst siliceous and nonsiliceous eukaryotes. Our analyses resolve a distinct group of Lsi2-like genes, including plant and diatom Si-responsive genes, and sequences unique to siliceous sponges and choanoflagellates. The SIT/SIT-L and Lsi2 transporter families likely contribute to biosilicification in diverse lineages, indicating an ancient role for Si transport in eukaryotes. We propose that these Si transporters may have arisen initially to prevent Si toxicity in the high Si Precambrian oceans, with subsequent biologically induced reductions in Si concentrations of Phanerozoic seas leading to widespread losses of SIT, SIT-L, and Lsi2-like genes in diverse lineages. Thus, the origin and diversification of two independent Si transporter families both drove and were driven by ancient ocean Si levels.

The role of the Arctic Ocean ecosystem in climate regulation may depend on the responses of marine microorganisms to environmental change. We applied genome-resolved metagenomics to 41 Arctic seawater samples, collected at various depths in different seasons during the Tara Oceans Polar Circle expedition, to evaluate the ecology, metabolic potential and activity of resident bacteria and archaea. We assembled 530 metagenome-assembled genomes (MAGs) to form the Arctic MAGs catalogue comprising 526 species. A total of 441 MAGs belonged to species that have not previously been reported and 299 genomes showed an exclusively polar distribution. Most Arctic MAGs have large genomes and the potential for fast generation times, both of which may enable adaptation to a copiotrophic lifestyle in nutrient-rich waters. We identified 38 habitat generalists and 111 specialists in the Arctic Ocean. We also found a general prevalence of 14 mixotrophs, while chemolithoautotrophs were mostly present in the mesopelagic layer during spring and autumn. We revealed 62 MAGs classified as key Arctic species, found only in the Arctic Ocean, showing the highest gene expression values and predicted to have habitat-specific traits. The Artic MAGs catalogue will inform our understanding of polar microorganisms that drive global biogeochemical cycles. Using genome-resolved metagenomics for 41 Arctic seawater samples, this ecogenomic analysis of 530 metagenome-assembled genomes (MAGs) from the polar Arctic Ocean reveals uncultured Arctic bacterial and archaeal MAGs, their gene expression patterns, habitat preferences and metabolic potential.

Metabarcoding is a powerful tool for exploring microbial diversity in the environment, but its accurate interpretation is impeded by diverse technical (e.g. PCR and sequencing errors) and biological biases (e.g. intra-individual polymorphism) that remain poorly understood. To help interpret environmental metabarcoding datasets, we investigated the intracellular diversity of the V4 and V9 regions of the 18S rRNA gene from Acantharia and Nassellaria (radiolarians) using 454 pyrosequencing. Individual cells of radiolarians were isolated, and PCRs were performed with generalist primers to amplify the V4 and V9 regions. Different denoising procedures were employed to filter the pyrosequenced raw amplicons (Acacia, AmpliconNoise, Linkage method). For each of the six isolated cells, an average of 541 V4 and 562 V9 amplicons assigned to radiolarians were obtained, from which one numerically dominant sequence and several minor variants were found. At the 97% identity, a diversity metrics commonly used in environmental surveys, up to 5 distinct OTUs were detected in a single cell. However, most amplicons grouped within a single OTU whereas other OTUs contained very few amplicons. Different analytical methods provided evidence that most minor variants forming different OTUs correspond to PCR and sequencing artifacts. Duplicate PCR and sequencing from the same DNA extract of a single cell had only 9 to 16% of unique amplicons in common, and alignment visualization of V4 and V9 amplicons showed that most minor variants contained substitutions in highly-conserved regions. We conclude that intracellular variability of the 18S rRNA in radiolarians is very limited despite its multi-copy nature and the existence of multiple nuclei in these protists. Our study recommends some technical guidelines to conservatively discard artificial amplicons from metabarcoding datasets, and thus properly assess the diversity and richness of protists in the environment.

Collodaria are heterotrophic marine protists that exist either as large colonies composed of hundreds of cells or as large solitary cells. All described species so far harbour intracellular microalgae as photosymbionts. Although recent environmental diversity surveys based on molecular methods demonstrated their consistently high contribution to planktonic communities and their worldwide occurrence, our understanding of their diversity and biogeography is still very limited. Here we estimated the 18S ribosomal DNA (rDNA) gene copies per collodarian cell for solitary (5770±1960 small subunit (SSU) rDNA copies) and colonial specimens (37 474±17 799 SSU rDNA copies, for each individual cell within a colony) using single-specimen quantitative PCR. We then investigated the environmental diversity of Collodaria within the photic zone through the metabarcoding survey from the Tara Oceans expedition and found that the two collodarian families Collosphaeridae and Sphaerozoidae contributed the most to the collodarian diversity and encompassed mostly cosmopolitan taxa. Although the biogeographical patterns were homogeneous within each biogeochemical biome considered, we observed that coastal biomes were consistently less diverse than oceanic biomes and were dominated by the Sphaerozoidae while the Collosphaeridae were dominant in the open oceans. The significant relationships with six environmental variables suggest that collodarian diversity is influenced by the trophic status of oceanic provinces and increased towards more oligotrophic regions.

Ocean plankton comprise organisms from viruses to fish larvae that are fundamental to ecosystem functioning and the provision of marine services such as fisheries and CO 2 sequestration. The latter services are partly governed by variations in plankton community composition and the expression of traits such as body size at community-level. While community assembly has been thoroughly studied for the smaller end of the plankton size spectrum, the larger end comprises ectotherms that are often studied at the species, or group-level, rather than as communities. The body size of marine ectotherms decreases with temperature, but controls on community-level traits remain elusive, hindering the predictability of marine services provision. Here, we leverage Tara Oceans datasets to determine how zooplankton community composition and size structure varies with latitude, temperature and productivity-related covariates in the global surface ocean. Zooplankton abundance and median size decreased towards warmer and less productive environments, as a result of changes in copepod composition. However, some clades displayed the opposite relationships, which may be ascribed to alternative feeding strategies. Given that climate models predict increasingly warmed and stratified oceans, our findings suggest that zooplankton communities will shift towards smaller organisms which might weaken their contribution to the biological carbon pump.