Niche partitioning and plastisphere core microbiomes in the two most plastic polluted zones of the world ocean.

Plastics are offering a new niche for microorganisms colonizing their surface, the so-called "plastisphere," in which diversity and community structure remain to be characterized and compared across ocean pelagic regions. Here, we compared the bacterial diversity of microorganisms living on plastic marine debris (PMD) and the surrounding free-living (FL) and organic particle-attached (PA) lifestyles sampled during the Tara expeditions in two of the most plastic polluted zones in the world ocean, i.e., the North Pacific gyre and the Mediterranean Sea. The 16S rRNA gene sequencing analysis confirmed that PMD are a new anthropogenic ocean habitat for marine microbes at the ocean-basin-scale, with clear niche partitioning compared to FL and PA lifestyles. At an ocean-basin-scale, the composition of the plastisphere communities was mainly driven by environmental selection, rather than polymer types or dispersal effect. A plastisphere "core microbiome" could be identified, mainly dominated by Rhodobacteraceae and Cyanobacteria. Predicted functions indicated the dominance of carbon, nitrogen and sulfur metabolisms on PMD that open new questions on the role of the plastisphere in a large number of important ecological processes in the marine ecosystem.

Vibrio spp and other potential pathogenic bacteria associated to microfibers in the North-Western Mediterranean Sea.

Microfibers, whether synthetic or natural, have increased dramatically in the environment, becoming the most common type of particles in the ocean, and exposing aquatic organisms to multiple negative impacts. Using an approach combining morphology (scanning electron microscopy-SEM) and molecular taxonomy (High-Throughput DNA Sequencing- HTS), we investigated the bacterial composition from floating microfibers (MFs) collected in the northwestern Mediterranean Sea. The average number of bacteria in 100 µm2 on the surface of a fiber is 8 ± 5.9 cells; by extrapolating it to a whole fiber, this represents 2663 ± 1981 bacteria/fiber. Attached bacterial communities were dominated by Alteromonadales, Rhodobacterales, and Vibrionales, including the potentially human/animal pathogen Vibrio parahaemolyticus. This study reveals a high rate of bacterial colonization on MFs, and shows that these particles can host numerous bacterial species, including putative pathogens. Even if we cannot confirm its pathogenicity based only on the taxonomy, this is the first description of such pathogenic Vibrio living attached to MFs in the Mediterranean Sea. The identification of MFs colonizers is valuable in assessing health risks, as their presence can be a threat to bathing and seafood consumption. Considering that MFs can serve as vector for potentially pathogenic microorganisms and other pollutants throughout the ocean, this type of pollution can have both ecological and economic consequences.

An integrative assessment of the plastic debris load in the Mediterranean Sea.

The Mediterranean Sea is recognized as one of the most polluted areas by floating plastics. During the Tara Mediterranean expedition, an extensive sampling of plastic debris was conducted in seven ecoregions, from Gibraltar to Lebanon with the aim of providing reliable estimates of regional differences in floating plastic loads and plastic characteristics. The abundance, size, surface, circularity and mass of 75,030 pieces were analyzed and classified in a standardized multi-parameter database. Their average abundance was 2.60 × 105 items km-2 (2.25 × 103 to 8.50 × 106 km-2) resulting in an estimate of about 650 billion plastic particles floating on the surface of the Mediterranean. This corresponds to an average of 660 metric tons of plastic, at the lower end of literature estimates. High concentrations of plastic were observed in the northwestern coastal regions, north of the Tyrrhenian Sea, but also off the western and central Mediterranean basins. The Levantine basin south of Cyprus had the lowest concentrations. A Lagrangian Plastic Pollution Index (LPPI) predicting the concentration of plastic debris was validated using the spatial resolution of the data. The advanced state of plastic degradation detected in the analyses led to the conclusion that stranding/fragmentation/resuspension is the key process in the dynamics of floating plastic in Mediterranean surface waters. This is supported by the significant correlation between pollution sources and areas of high plastic concentration obtained by the LPPI.

Cryptic and abundant marine viruses at the evolutionary origins of Earth's RNA virome.

Whereas DNA viruses are known to be abundant, diverse, and commonly key ecosystem players, RNA viruses are insufficiently studied outside disease settings. In this study, we analyzed ≈28 terabases of Global Ocean RNA sequences to expand Earth's RNA virus catalogs and their taxonomy, investigate their evolutionary origins, and assess their marine biogeography from pole to pole. Using new approaches to optimize discovery and classification, we identified RNA viruses that necessitate substantive revisions of taxonomy (doubling phyla and adding >50% new classes) and evolutionary understanding. "Species"-rank abundance determination revealed that viruses of the new phyla "Taraviricota," a missing link in early RNA virus evolution, and "Arctiviricota" are widespread and dominant in the oceans. These efforts provide foundational knowledge critical to integrating RNA viruses into ecological and epidemiological models.

Chemical composition of microplastics floating on the surface of the Mediterranean Sea.

The Mediterranean Sea is one of the most studied regions in the world in terms of microplastic (MP) contamination. However, only a few studies have analysed the chemical composition of MPs at the Mediterranean Sea surface. In this context, this study aims to describe the chemical composition as a function of particle size, mass and number concentrations of MPs collected in the surface waters of the Mediterranean Sea. The chemical composition showed a certain homogeneity at the Mediterranean Sea scale. The main polymers identified by Fourier Transform Infra-Red (FTIR) spectroscopy were poly(ethylene) (67.3 ± 2.4%), poly(propylene) (20.8 ± 2.1%) and poly(styrene) (3.0 ± 0.9%). Nevertheless, discrepancies, confirmed by the literature, were observed at a mesoscale level. Thus, in the North Tyrrhenian Sea, the proportion of poly(ethylene) was significantly lower than the average value of the Mediterranean Sea (57.9 ± 10.5%). Anthropic sources, rivers, or polymer ageing are assumed to be responsible for the variations observed.

Diel cycle of sea spray aerosol concentration.

Sea spray aerosol (SSA) formation have a major role in the climate system, but measurements at a global-scale of this micro-scale process are highly challenging. We measured high-resolution temporal patterns of SSA number concentration over the Atlantic Ocean, Caribbean Sea, and the Pacific Ocean covering over 42,000 km. We discovered a ubiquitous 24-hour rhythm to the SSA number concentration, with concentrations increasing after sunrise, remaining higher during the day, and returning to predawn values after sunset. The presence of dominating continental aerosol transport can mask the SSA cycle. We did not find significant links between the diel cycle of SSA number concentration and diel variations of surface winds, atmospheric physical properties, radiation, pollution, nor oceanic physical properties. However, the daily mean sea surface temperature positively correlated with the magnitude of the day-to-nighttime increase in SSA concentration. Parallel diel patterns in particle sizes were also detected in near-surface waters attributed to variations in the size of particles smaller than ~1 µm. These variations may point to microbial day-to-night modulation of bubble-bursting dynamics as a possible cause of the SSA cycle.

Macroscale patterns of oceanic zooplankton composition and size structure.

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 CO2 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.

Tara Oceans: towards global ocean ecosystems biology.

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.

Changes in the Floating Plastic Pollution of the Mediterranean Sea in Relation to the Distance to Land.

The composition, size distribution, and abundance of floating plastic debris in surface waters of the Mediterranean Sea were analyzed in relation to distance to land. We combined data from previously published reports with an intensive sampling in inshore waters of the Northwestern Mediterranean. The highest plastic concentrations were found in regions distant from from land as well as in the first kilometer adjacent to the coastline. In this nearshore water strip, plastic concentrations were significantly correlated with the nearness to a coastal human population, with local areas close to large human settlements showing hundreds of thousands of plastic pieces per km2. The ratio of plastic to plankton abundance reached particularly high values for the coastal surface waters. Polyethylene, polypropylene and polyamides were the predominant plastic polymers at all distances from coast (86 to 97% of total items), although the diversity of polymers was higher in the 1-km coastal water strip due to a higher frequency of polystyrene or polyacrylic fibers. The plastic size distributions showed a gradual increase in abundance toward small sizes indicating an efficient removal of small plastics from the surface. Nevertheless, the relative abundance of small fragments (< 2 mm) was higher within the 1-km coastal water strip, suggesting a rapid fragmentation down along the shoreline, likely related with the washing ashore on the beaches. This study constitutes a first attempt to determine the impact of plastic debris in areas closest to Mediterranean coast. The presence of a high concentration of plastic including tiny plastic items could have significant environmental, health and economic impacts.

In situ imaging reveals the biomass of giant protists in the global ocean.

Planktonic organisms play crucial roles in oceanic food webs and global biogeochemical cycles. Most of our knowledge about the ecological impact of large zooplankton stems from research on abundant and robust crustaceans, and in particular copepods. 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. 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 changes our understanding of marine planktonic ecosystems.

Plankton networks driving carbon export in the oligotrophic ocean.

The biological carbon pump is the process by which CO2 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 uncharacterized. 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 and 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 a few bacterial and viral genes can predict a significant fraction of the variability in carbon export in these regions.

Open science resources for the discovery and analysis of Tara Oceans data.

The Tara Oceans expedition (2009-2013) sampled contrasting ecosystems of the world oceans, collecting environmental data and plankton, from viruses to metazoans, for later analysis using modern sequencing and state-of-the-art imaging technologies. It surveyed 210 ecosystems in 20 biogeographic provinces, collecting over 35,000 samples of seawater and plankton. The interpretation of such an extensive collection of samples in their ecological context requires means to explore, assess and access raw and validated data sets. To address this challenge, the Tara Oceans Consortium offers open science resources, including the use of open access archives for nucleotides (ENA) and for environmental, biogeochemical, taxonomic and morphological data (PANGAEA), and the development of on line discovery tools and collaborative annotation tools for sequences and images. Here, we present an overview of Tara Oceans Data, and we provide detailed registries (data sets) of all campaigns (from port-to-port), stations and sampling events.

Ocean plankton. Structure and function of the global ocean microbiome.

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.

Ocean plankton. Environmental characteristics of Agulhas rings affect interocean plankton transport.

Agulhas rings provide the principal route for ocean waters to circulate from the Indo-Pacific to the Atlantic basin. Their influence on global ocean circulation is well known, but their role in plankton transport is largely unexplored. We show that, although the coarse taxonomic structure of plankton communities is continuous across the Agulhas choke point, South Atlantic plankton diversity is altered compared with Indian Ocean source populations. Modeling and in situ sampling of a young Agulhas ring indicate that strong vertical mixing drives complex nitrogen cycling, shaping community metabolism and biogeochemical signatures as the ring and associated plankton transit westward. The peculiar local environment inside Agulhas rings may provide a selective mechanism contributing to the limited dispersal of Indian Ocean plankton populations into the Atlantic.

Ocean plankton. Patterns and ecological drivers of ocean viral communities.

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.

Ocean plankton. Eukaryotic plankton diversity in the sunlit ocean.

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.

Ocean plankton. Determinants of community structure in the global plankton interactome.

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.

Comprehensive model of annual plankton succession based on the whole-plankton time series approach.

Ecological succession provides a widely accepted description of seasonal changes in phytoplankton and mesozooplankton assemblages in the natural environment, but concurrent changes in smaller (i.e. microbes) and larger (i.e. macroplankton) organisms are not included in the model because plankton ranging from bacteria to jellies are seldom sampled and analyzed simultaneously. Here we studied, for the first time in the aquatic literature, the succession of marine plankton in the whole-plankton assemblage that spanned 5 orders of magnitude in size from microbes to macroplankton predators (not including fish or fish larvae, for which no consistent data were available). Samples were collected in the northwestern Mediterranean Sea (Bay of Villefranche) weekly during 10 months. Simultaneously collected samples were analyzed by flow cytometry, inverse microscopy, FlowCam, and ZooScan. The whole-plankton assemblage underwent sharp reorganizations that corresponded to bottom-up events of vertical mixing in the water-column, and its development was top-down controlled by large gelatinous filter feeders and predators. Based on the results provided by our novel whole-plankton assemblage approach, we propose a new comprehensive conceptual model of the annual plankton succession (i.e. whole plankton model) characterized by both stepwise stacking of four broad trophic communities from early spring through summer, which is a new concept, and progressive replacement of ecological plankton categories within the different trophic communities, as recognised traditionally.