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...
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.
SummaryThe ocean is home to myriad small planktonic organisms that underpin the functioning of marine ecosystems. However, their spatial patterns of diversity and the underlying drivers remain poorly known, precluding projections of their responses to global changes. Here we investigate the latitudinal gradients and global predictors of plankton diversity across archaea, bacteria, eukaryotes, and major virus clades using both molecular and imaging data from Tara Oceans. We show a decline of diversity for most planktonic groups toward the poles, mainly driven by decreasing ocean temperatures. Projections into the future suggest that severe warming of the surface ocean by the end of the 21st century could lead to tropicalization of the diversity of most planktonic groups in temperate and polar regions. These changes may have multiple consequences for marine ecosystem functioning and services and are expected to be particularly significant in key areas for carbon sequestration, fisheries, and marine conservation.Video Abstract
Biogeographical studies have traditionally focused on readily visible organisms, but recent technological advances are enabling analyses of the large-scale distribution of microscopic organisms, whose biogeographical patterns have long been debated1,2. The most prominent global biogeography of marine plankton was derived by Longhurst3 based on parameters principally associated with photosynthetic plankton. Localized studies of selected plankton taxa or specific organismal sizes1,4–7 have mapped community structure and begun to assess the roles of environment and ocean current transport in shaping these patterns2,8. Here we assess global plankton biogeography and its relation to the biological, chemical and physical context of the ocean (the ‘seascape’) by analyzing 24 terabases of metagenomic sequence data and 739 million metabarcodes from the Tara Oceans expedition in light of environmental data and simulated ocean current transport. In addition to significant local heterogeneity, viral, prokaryotic and eukaryotic plankton communities all display near steady-state, large-scale, size-dependent biogeographical patterns. Correlation analyses between plankton transport time and metagenomic or environmental dissimilarity reveal the existence of basin-scale biological and environmental continua emerging within the main current systems. Across oceans, there is a measurable, continuous change within communities and environmental factors up to an average of 1.5 years of travel time. Modulation of plankton communities during transport varies with organismal size, such that the distribution of smaller plankton best matches Longhurst biogeochemical provinces, whereas larger plankton group into larger provinces. Together these findings provide an integrated framework to interpret plankton community organization in its physico-chemical context, paving the way to a better understanding of oceanic ecosystem functioning in a changing global environment.
Nucleocytoplasmic large DNA viruses (NCLDVs) are ubiquitous in marine environments and infect diverse eukaryotes. However, little is known about their biogeography and ecology in the ocean. By leveraging the Tara Oceans pole-to-pole metagenomic data set, we investigated the distribution of NCLDVs across size fractions, depths and biomes, as well as their associations with eukaryotic communities. Our analyses revealed a heterogeneous distribution of NCLDVs across oceans, with an elevated uniqueness in polar biomes. The community structures of NCLDV families were correlated with specific eukaryotic lineages including many photosynthetic groups.NCDLV communities were generally distinct between surface and mesopelagic zones, but at some locations, they exhibited a high similarity between the two depths. This vertical similarity was correlated to surface phytoplankton biomass but not to physical mixing processes, suggesting the potential role of vertical export in structuring mesopelagic NCLDV communities. These results underscore the importance of the coupling between NCLDVs and eukaryotes in biogeochemical processes in the ocean.
Remote deep-ocean sediment (DOS) ecosystems are among the least explored biomes on Earth. Genomic assessments of their biodiversity have failed to separate indigenous benthic organisms from sinking plankton. Here, we compare global-scale eukaryotic DNA metabarcoding datasets (18 S -V9) from abyssal and lower bathyal surficial sediments and euphotic and aphotic ocean pelagic layers to distinguish plankton from benthic diversity in sediment material. Based on 1685 samples collected throughout the world ocean, we show that DOS diversity is at least threefold that in pelagic realms, with nearly two-thirds represented by abundant yet unknown eukaryotes. These benthic communities are spatially structured by ocean basins and particulate organic carbon (POC) flux from the upper ocean. Plankton DNA reaching the DOS originates from abundant species, with maximal deposition at high latitudes. Its seafloor DNA signature predicts variations in POC export from the surface and reveals previously overlooked taxa that may drive the biological carbon pump.
Marine plankton form complex communities of interacting organisms at the base of the food web, which sustain oceanic biogeochemical cycles and help regulate climate. Although global surveys are starting to reveal ecological drivers underlying planktonic community structure and predicted climate change responses, it is unclear how community-scale species interactions will be affected by climate change. Here, we leveraged Tara Oceans sampling to infer a global ocean cross-domain plankton co-occurrence network—the community interactome—and used niche modeling to assess its vulnerabilities to environmental change. Globally, this revealed a plankton interactome self-organized latitudinally into marine biomes (Trades, Westerlies, Polar) and more connected poleward. Integrated niche modeling revealed biome-specific community interactome responses to environmental change and forecasted the most affected lineages for each community. These results provide baseline approaches to assess community structure and organismal interactions under climate scenarios while identifying plausible plankton bioindicators for ocean monitoring of climate change.
Summary The study of protistan functional diversity is crucial to understand the dynamics of oceanic ecological processes. We combined the metabarcoding data of various coastal ecosystems and a newly developed trait‐based approach to study the link between taxonomic and functional diversity across marine protistan communities of different size‐classes. Environmental DNA was extracted and the V4 18S rDNA genomic region was amplified and sequenced. In parallel, we tried to annotate the operational taxonomic units (OTUs) from our metabarcoding dataset to 30 biological traits using published and accessible information on protists. We then developed a method to study trait correlations across protists (i.e. trade‐offs) in order to build the best functional groups. Based on the annotated OTUs and our functional groups, we demonstrated that the functional diversity of marine protist communities varied in parallel with their taxonomic diversity. The coupling between functional and taxonomic diversity was conserved across different protist size classes. However, the smallest size‐fraction was characterized by wider taxonomic and functional groups diversity, corroborating the idea that nanoplankton and picoplankton are part of a more stable ecological background on which larger protists and metazoans might develop.
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