Microbes are dominant drivers of biogeochemical processes, yet drawing a global picture of functional diversity, microbial community structure, and their ecological determinants remains a grand challenge. We analyzed 7.2 terabases of metagenomic data from 243 Tara Oceans samples from 68 locations in epipelagic and mesopelagic waters across the globe to generate an ocean microbial reference gene catalog with >40 million nonredundant, mostly novel sequences from viruses, prokaryotes, and picoeukaryotes. Using 139 prokaryote-enriched samples, containing >35,000 species, we show vertical stratification with epipelagic community composition mostly driven by temperature rather than other environmental factors or geography. We identify ocean microbial core functionality and reveal that >73% of its abundance is shared with the human gut microbiome despite the physicochemical differences between these two ecosystems.

Marine plankton support global biological and geochemical processes. Surveys of their biodiversity have hitherto been geographically restricted and have not accounted for the full range of plankton size. We assessed eukaryotic diversity from 334 size-fractionated photic-zone plankton communities collected across tropical and temperate oceans during the circumglobal Tara Oceans expedition. We analyzed 18S ribosomal DNA sequences across the intermediate plankton-size spectrum from the smallest unicellular eukaryotes (protists, >0.8 micrometers) to small animals of a few millimeters. Eukaryotic ribosomal diversity saturated at~150,000 operational taxonomic units, about one-third of which could not be assigned to known eukaryotic groups. Diversity emerged at all taxonomic levels, both within the groups comprising the~11,200 cataloged morphospecies of eukaryotic plankton and among twice as many other deep-branching lineages of unappreciated importance in plankton ecology studies. Most eukaryotic plankton biodiversity belonged to heterotrophic protistan groups, particularly those known to be parasites or symbiotic hosts.T he sunlit surface layer of the world'soceans functionsasagiantbiogeoch emicalmem-brane between the atmosphere and the ocean interior (1). This biome includes plank-ton communities that fix CO 2 and other elements into biological matter, which then enters the food web. This biological matter can be remineralized or exported to the deeper ocean, where it may be sequestered over ecological to geological time scales. Studies of this biome have typically focused on either conspicuous phyto-or zooplankton at the larger end of the organismal size spectrum or microbes (prokaryotes and viruses) at the smaller end. In this work, we studied the taxonomic and ecological diversity of the intermediate size spectrum (from 0.8 mmtoafew millimeters), which includes all unicellular eukary-otes (protists) and ranges from the smallest pro-tistan cells to small animals (2). The ecological biodiversity of marine planktonic protists has been analyzed using Sanger (3-5) and high-throughput (6, 7) sequencing of mainly ribosomal DNA (rDNA) gene markers, on relatively small taxonomic and/or geographical scales, unveiling key new groups of phagotrophs (8), parasites (9), and phototrophs (10). We sequenced 18S rDNA metabarcodes up to local and global saturations from size-fractionated plankton communities sampled systematically across the world tropical and temperate sunlit oceans. A global metabarcoding approachTo explore patterns of photic-zone eukaryotic plankton biodiversity, we generated ~766 million raw rDNA sequence reads from 334 plankton samples collected during the circumglobal Tara Oceans expedition (11). At each of 47 stations, plankton communities were sampled at two water-column depths corresponding to the main hydrographic structures of the photic zone: subsurface mixed-layer waters and the deep chlorophyll maximum (DCM) at the top of the thermocline. A low-shear, nonintrusive peristaltic pump and plankton nets of...

The interrogation of genetic markers in environmental meta-barcoding studies is currently seriously hindered by the lack of taxonomically curated reference data sets for the targeted genes. The Protist Ribosomal Reference database (PR2, http://ssu-rrna.org/) provides a unique access to eukaryotic small sub-unit (SSU) ribosomal RNA and DNA sequences, with curated taxonomy. The database mainly consists of nuclear-encoded protistan sequences. However, metazoans, land plants, macrosporic fungi and eukaryotic organelles (mitochondrion, plastid and others) are also included because they are useful for the analysis of high-troughput sequencing data sets. Introns and putative chimeric sequences have been also carefully checked. Taxonomic assignation of sequences consists of eight unique taxonomic fields. In total, 136 866 sequences are nuclear encoded, 45 708 (36 501 mitochondrial and 9657 chloroplastic) are from organelles, the remaining being putative chimeric sequences. The website allows the users to download sequences from the entire and partial databases (including representative sequences after clustering at a given level of similarity). Different web tools also allow searches by sequence similarity. The presence of both rRNA and rDNA sequences, taking into account introns (crucial for eukaryotic sequences), a normalized eight terms ranked-taxonomy and updates of new GenBank releases were made possible by a long-term collaboration between experts in taxonomy and computer scientists.

Microbes drive most ecosystems and are modulated by viruses that impact their lifespan, gene flow and metabolic outputs. However, ecosystem-level impacts of viral community diversity remains difficult to assess due to classification issues and few reference genomes. Here we establish a ~12-fold expanded global ocean DNA virome dataset of 195,728 60 viral populations, now including the Arctic Ocean, and validate that these populations form discrete genotypic clusters. Meta-community analyses revealed five ecological zones throughout the global ocean, including two distinct Arctic regions. Across the zones, local and global patterns and drivers in viral community diversity were established for both macrodiversity (interpopulation diversity) and microdiversity (intra-population genetic variation). These patterns 65 sometimes, but not always, paralleled those from macro-organisms and revealed temperate and tropical surface waters and the Arctic as biodiversity hotspots and mechanistic hypotheses to explain them. Such further understanding of ocean viruses is critical for broader inclusion in ecosystem models. Introduction: 70Biodiversity is essential for maintaining ecosystem functions and services (reviewed by Tilman et al., 2014). In the oceans, the vast majority of biodiversity is contained within the microbial fraction containing prokaryotes and eukaryotic microbes, which represents ~60% of its biomass (Bar-On et al., 2018). Meta-analyses looking at changes in marine biodiversity show that biodiversity loss increasingly impairs the ocean's capacity to produce food, maintain water 75 quality, and recover from perturbations (Worm et al., 2006). To date, marine conservation efforts have focused on specific organismal communities, such as fisheries or coral reefs, rather than conserving whole ecosystem biodiversity. However, emerging studies across diverse sampled, global-scale, viruses-to-fish-larvae datasets (de Vargas et al., 2015; Sunagawa et al., 125 2015;Brum et al., 2015;Lima-Mendez et al., 2015;Pesant et al. 2015;Roux et al., 2016), and help establish foundational ecological hypotheses for the field and a roadmap for the broader life sciences community to better study viruses in complex communities. Results & Discussion:The dataset. The Global Ocean Viromes 2.0 (GOV 2.0) dataset is derived from 3.95 Tb 130 of sequencing across 145 samples distributed throughout the world's oceans ( Fig. 1A and Table S3; see Methods). These data build on the prior GOV dataset (Roux et al., 2016) by increased sequencing for mesopelagic samples (defined in our dataset as waters between 150m to 1,000m) and upgrading assemblies, both of which drastically improved sampling of the ocean viruses in these samples (results below). Additionally, we added 41 new samples derived from the Tara 135Oceans Polar Circle (TOPC) expedition, which traveled 25,000 km around the Arctic Ocean in 2013. These 41 Arctic Ocean viromes were generated to represent the most significantly climateimpacted region of the ocean, and an extreme environment. N...

Species interaction networks are shaped by abiotic and biotic factors. Here, as part of the Tara Oceans project, we studied the photic zone interactome using environmental factors and organismal abundance profiles and found that environmental factors are incomplete predictors of community structure. We found associations across plankton functional types and phylogenetic groups to be nonrandomly distributed on the network and driven by both local and global patterns. We identified interactions among grazers, primary producers, viruses, and (mainly parasitic) symbionts and validated network-generated hypotheses using microscopy to confirm symbiotic relationships. We have thus provided a resource to support further research on ocean food webs and integrating biological components into ocean models.

Viruses influence ecosystems by modulating microbial population size, diversity, metabolic outputs, and gene flow. Here, we use quantitative double-stranded DNA (dsDNA) viral-fraction metagenomes (viromes) and whole viral community morphological data sets from 43 Tara Oceans expedition samples to assess viral community patterns and structure in the upper ocean. Protein cluster cataloging defined pelagic upper-ocean viral community pan and core gene sets and suggested that this sequence space is well-sampled. Analyses of viral protein clusters, populations, and morphology revealed biogeographic patterns whereby viral communities were passively transported on oceanic currents and locally structured by environmental conditions that affect host community structure. Together, these investigations establish a global ocean dsDNA viromic data set with analyses supporting the seed-bank hypothesis to explain how oceanic viral communities maintain high local diversity.

Over the past three decades, massive bleaching events of zooxanthellate corals have been documented across the range of global distribution. Although the phenomenon is correlated with relatively small increases in sea-surface temperature and enhanced light intensity, the underlying physiological mechanism remains unknown. In this article we demonstrate that thylakoid membrane lipid composition is a key determinate of thermal-stress sensitivity in symbiotic algae of cnidarians. Analyses of thylakoid membranes reveal that the critical threshold temperature separating thermally tolerant from sensitive species of zooxanthellae is determined by the saturation of the lipids. The lipid composition is potentially diagnostic of the differential nature of thermally induced bleaching found in scleractinian corals. Measurements of variable chlorophyll fluorescence kinetic transients indicate that thermally damaged membranes are energetically uncoupled but remain capable of splitting water. Consequently, a fraction of the photosynthetically produced oxygen is reduced by photosystem I through the Mehler reaction to form reactive oxygen species, which rapidly accumulate at high irradiance levels and trigger death and expulsion of the endosymbiotic algae. Differential sensitivity to thermal stress among the various species of Symbiodinium seems to be distributed across all clades. A clocked molecular phylogenetic analysis suggests that the evolutionary history of symbiotic algae in cnidarians selected for a reduced tolerance to elevated temperatures in the latter portion of the Cenozoic.C oral bleaching on a global scale is a growing concern because of both the reduction in essential ecological services provided by zooxanthellate corals within reef communities (1, 2) and the potentially devastating economic impacts accompanying the phenomenon (3). Small, positive deviations in temperature of Ͻ2°C can trigger massive losses of symbiotic algae, Symbiodinium spp., from their cnidarian host cells (4). However, not all corals within a reef are equally susceptible to elevated temperature stress (5, 6). Although elevated temperatures often lead to a reduction in the quantum yield of photochemistry, a concomitant increase in the rate of protein turnover in oxygen-generating reaction center, photosystem (PS)II (7-9), and an increase in the production of reactive oxygen species (ROS) (10-12), no mechanism has been elucidated. Here we show that thermal sensitivity in isolated clones of zooxanthellae and in symbiotic animal hosts is correlated with the degree of saturation of the lipids in the thylakoid membranes in the algal plastids. Our results provide a mechanistic basis for understanding and diagnosing coral bleaching patterns in nature. Materials and MethodsCultures and Corals. Cultures of Symbiodinium spp., obtained from culture collections or isolated from hosts, were grown in F͞2 medium under a 10͞14-h light͞dark cycle and illuminated with 100 mol quanta m Ϫ2 ⅐s Ϫ1 . Corals were grown at 26°C in 800 liters of aquaria with running ...

The biological carbon pump is the process by which CO 2 is transformed to organic carbon via photosynthesis, exported through sinking particles, and finally sequestered in the deep ocean. While the intensity of the pump correlates with plankton community composition, the underlying ecosystem structure driving the process remains largely uncharacterised. Here we use environmental and metagenomic data gathered during the Tara Oceans expedition to improve our understanding of carbon export in the oligotrophic ocean. We show that specific plankton communities, from the surface and deep chlorophyll maximum, correlate with carbon export at 150 m and highlight unexpected taxa such as Radiolaria, alveolate parasites, as well as Synechococcus and their phages, as lineages most strongly associated with carbon export in the subtropical, nutrient-depleted, oligotrophic ocean. Additionally, we show that the relative abundance of just a few bacterial and viral genes can predict most of the variability in carbon export in these regions. Guidi et al. Page 2 Nature. Author manuscript; available in PMC 2016 September 22. Europe PMC Funders Author Manuscripts Europe PMC Funders Author ManuscriptsMarine planktonic photosynthetic organisms are responsible for approximately fifty percent of Earth's primary production and fuel the global ocean biological carbon pump 1 . The intensity of the pump is correlated to plankton community composition 2,3 , and controlled by the relative rates of primary production and carbon remineralisation 4 . About 10% of this newly produced organic carbon in the surface ocean is exported through gravitational sinking of particles. Finally, after multiple transformations, a fraction of the exported material reaches the deep ocean where it is sequestered over thousand-year timescales 5 .Like most biological systems, marine ecosystems in the sunlit upper layer of the ocean (denoted the euphotic zone) are complex 6,7 , characterised by a wide range of biotic and abiotic interactions [8][9][10] and in constant balance between carbon production, transfer to higher trophic levels, remineralisation, and export to the deep layers 11 . The marine ecosystem structure and its taxonomic and functional composition likely evolved to comply with this loss of energy by modifying organism turnover times and by the establishment of complex feedbacks between them 6 and the substrates they can exploit for metabolism 12 .Decades of groundbreaking research have focused on identifying independently the key players involved in the biological carbon pump. Among autotrophs, diatoms are commonly attributed to being important in carbon flux because of their large size and fast sinking rates 13-15 while small autotrophic picoplankton may contribute directly through subduction of surface water 16 or indirectly by aggregating with larger settling particles or consumption by organisms at higher trophic levels 17 . Among heterotrophs, zooplankton such as crustaceans impact carbon flux via production of fast-sinking fecal pellets...