Global Trends in Marine Plankton Diversity across Kingdoms of Life

35 pages, 18 figures, 1 table, supplementary information https://doi.org/10.1016/j.cell.2019.10.008.-- Raw reads of Tara Oceans are deposited at the European Nucleotide Archive (ENA). In particular, newly released 18S rRNA gene metabarcoding reads are available under the number ENA: PRJEB9737. ENA references for the metagenomics reads corresponding to the size fraction < 0.22 μm (for prokaryotic viruses) analyzed in this study are included in Gregory et al. (2019); see their Table S3. ENA references for the metagenomics reads corresponding to the size fraction 0.22-1.6/3 μm (for prokaryotes and giruses) correspond to Salazar et al. (2019) (see https://zenodo.org/record/3473199). Imaging datasets from the nets are available through the collaborative web application and repository EcoTaxa (Picheral et al., 2017) under the address https://ecotaxa.obs-vlfr.fr/prj/412 for regent data, within the 3 projects https://ecotaxa.obs-vlfr.fr/prj/397, https://ecotaxa.obs-vlfr.fr/prj/398, https://ecotaxa.obs-vlfr.fr/prj/395 for bongo data, and within the 2 projects https://ecotaxa.obs-vlfr.fr/prj/377 and https://ecotaxa.obs-vlfr.fr/prj/378 for WP2 data. A table with Shannon values and multiple samples identifiers, plus a table with flow cytometry data split in six groups are available (https://doi.org/10.17632/p9r9wttjkm.1). Contextual data from the Tara Oceans expedition, including those that are newly released from the Arctic Ocean, are available at https://doi.org/10.1594/PANGAEA.875582The 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 conservationTara Oceans (which includes both the Tara Oceans and Tara Oceans Polar Circle expeditions) would not exist without the leadership of the Tara Ocean Foundation and the continuous support of 23 institutes (https://oceans.taraexpeditions.org/). We further thank the commitment of the following sponsors: CNRS (in particular Groupement de Recherche GDR3280 and the Research Federation for the Study of Global Ocean Systems Ecology and Evolution FR2022/Tara Oceans-GOSEE), the European Molecular Biology Laboratory (EMBL), Genoscope/CEA, the French Ministry of Research, and the French Government “Investissements d’Avenir” programs OCEANOMICS (ANR-11-BTBR-0008), FRANCE GENOMIQUE (ANR-10-INBS-09-08), MEMO LIFE (ANR-10-LABX-54), the PSL∗ Research University (ANR-11-IDEX-0001-02), as well as EMBRC-France (ANR-10-INBS-02). Funding for the collection and processing of the Tara Oceans data set was provided by NASA Ocean Biology and Biogeochemistry Program under grants NNX11AQ14G, NNX09AU43G, NNX13AE58G, and NNX15AC08G (to the University of Maine); the Canada Excellence research chair on remote sensing of Canada’s new Arctic frontier; and the Canada Foundation for Innovation. We also thank agnès b. and Etienne Bourgois, the Prince Albert II de Monaco Foundation, the Veolia Foundation, Region Bretagne, Lorient Agglomeration, Serge Ferrari, Worldcourier, and KAUST for support and commitment. The global sampling effort was enabled by countless scientists and crew who sampled aboard the Tara from 2009–2013, and we thank MERCATOR-CORIOLIS and ACRI-ST for providing daily satellite data during the expeditions. We are also grateful to the countries who graciously granted sampling permission. We thank Stephanie Henson for providing ocean carbon export data and are also grateful to the other researchers who kindly made their data available. We thank Juan J. Pierella-Karlusich for advice regarding single-copy genes. C.d.V. and N.H. thank the Roscoff Bioinformatics platform ABiMS (http://abims.sb-roscoff.fr) for providing computational resources. C.B. acknowledges funding from the European Research Council (ERC) under the European Union’s Horizon 2020 Research and Innovation Program (grant agreement 835067) as well as the Radcliffe Institute of Advanced Study at Harvard University for a scholar’s fellowship during the 2016-2017 academic year. M.B.S. thanks the Gordon and Betty Moore Foundation (award 3790) and the National Science Foundation (awards OCE#1536989 and OCE#1829831) as well as the Ohio Supercomputer for computational support. S.G.A. thanks the Spanish Ministry of Economy and Competitiveness (CTM2017-87736-R), and J.M.G. is grateful for project RT2018-101025-B-100. F.L. thanks the Institut Universitaire de France (IUF) as well as the EMBRC platform PIQv for image analysis. M.C.B., D.S., and J.R. received financial support from the French Facility for Global Environment (FFEM) as part of the “Ocean Plankton, Climate and Development” project. M.C.B. also received financial support from the Coordination for the Improvement of Higher Education Personnel of Brazil (CAPES 99999.000487/2016-03)Peer Reviewe

Estimating diversity of crabs (Decapoda: Brachyura) in a no-take marine protected area of the SW Atlantic coast through DNA barcoding of larvae

<p>DNA barcoding was used to identify crab larvae from the Marine Biological Reserve of Arvoredo, encompassing a coastal archipelago off the SW Atlantic coast (27°S, 48°W). Partial mitochondrial COI or 16S rRNA gene sequences were obtained for 488 larvae, leading to the identification of 20 species. The COI sequences generated 13 barcode index numbers (BINs) within Barcode of Life Data Systems (BOLD), among which 11 were concordant with single species. DNA from ∼ 6% of the larvae did not amplify using the primers tested; based on external morphological characteristics, these larvae represented four possible additional operational taxonomic units (OTUs) at the family level. Intraspecific variation for the COI and 16S rRNA genes was found to be < 2.6% and < 2.1% respectively (Kimura 2-parameter distance), whereas interspecific divergence ranged from 7.9% to 21.5% and 6.4% to 14.5%, respectively. These results imply that both genes are suitable for use in species identification of brachyuran crabs of this area. Molecular identification of this group successfully enabled the diagnosis of larvae of closely related species, including congeners in <i>Mithrax</i>, <i>Achelous</i> and <i>Callinectes</i>. In addition, eight out of 20 species recognized represent new records for the reserve suggesting that the brachyuran fauna in the area has been underestimated based on traditional biodiversity measures. The availability of primers suited to the targeted species, and the development of a taxonomically comprehensive DNA barcoding database are the major recommendations to improve the accuracy and feasibility of using DNA barcoding for species identification of SW Atlantic brachyuran crabs.</p

Does the transport of larvae throughout the south Atlantic support the genetic and morphometric diversity of the Sally Lightfoot Crabs Grapsus grapsus (Linnaeus, 1758) and Grapsus adscensionis (Osbeck, 1765) (Decapoda Grapsidae) among the oceanic islands?

International audiencerapsus grapsus and Grapsus adscensionis are supralittoral crabs that are known to inhabit oceanic islands and depend on surface currents to recruit in the rocky shores. The ornamentation of the cephalothorax is very distinct among species, but morphological differences are controversial, and integrative studies with different approaches are needed. This study investigated the genetic variation among the populations of G. grapsus from Saint Peter and Saint Paul Archipelago (SP), Fernando de Noronha (FN), Rocas Atoll (RA) and Trindade Island (TR) in the western Atlantic, and G. adscensionis from the islands of Ascension (AI) and Saint Helena (SH) in the mid-Atlantic. Morphology was assessed by geometric morphometric analyses of the carapace and chelae, and numerical analyses of tubercles in the frontal plate of SP, FN, RA, TR and AI populations. In addition, dispersal of the larvae in the Atlantic Ocean was simulated performing a Lagrangian analysis using HYCOM reanalysis dataset as the ocean surface velocity field. The data obtained for the mitochondrial D-loop gene confirmed the distinctness of the two putative species and demonstrated the connectivity between the populations of G. grapsus from the three equatorial islands. The TR population presented unique haplotypes, as well as AI and SH. The geometric morphometric analyses showed differentiation between the carapace shapes for G. grapsus and G. adscensionis, however, the chelae shape does not allow to distinguish between the species or the population. The morphometric and molecular results were consistent with the pattern of particles dispersion in the Atlantic ocean. The larvae of SP, FN and RA mix after two months of drift, while the larvae of TR, AI, SH circulate only around the respective islands. The results reinforce the validation of the two species and the isolation of populations of G. grapsus in TR and of G. adscensionis in AI and SH. The populations of these islands might be maintained by self-recruitment, through larval behavior associated with the local current system, and therefore should be the target of conservation measures

Ocean-wide comparisons of mesopelagic planktonic community structures

For decades, marine plankton have been investigated for their capacity to modulate biogeochemical cycles and provide fishery resources. Between the sunlit (epipelagic) layer and the deep dark waters, lies a vast and heterogeneous part of the ocean: the mesopelagic zone. How plankton composition is shaped by environment has been well-explored in the epipelagic but much less in the mesopelagic ocean. Here, we conducted comparative analyses of trans-kingdom community assemblages thriving in the mesopelagic oxygen minimum zone (OMZ), mesopelagic oxic, and their epipelagic counterparts. We identified nine distinct types of intermediate water masses that correlate with variation in mesopelagic community composition. Furthermore, oxygen, NO3- and particle flux together appeared as the main drivers governing these communities. Novel taxonomic signatures emerged from OMZ while a global co-occurrence network analysis showed that about 70% of the abundance of mesopelagic plankton groups is organized into three community modules. One module gathers prokaryotes, pico-eukaryotes and Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) from oxic regions, and the two other modules are enriched in OMZ prokaryotes and OMZ pico-eukaryotes, respectively. We hypothesize that OMZ conditions led to a diversification of ecological niches, and thus communities, due to selective pressure from limited resources. Our study further clarifies the interplay between environmental factors in the mesopelagic oxic and OMZ, and the compositional features of communities.ISSN:2730-615

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.ISSN:2045-232

Ubiquity of inverted ’gelatinous’ ecosystem pyramids in the global ocean

Summary paragraph Plankton are essential in marine ecosystems. However, our knowledge of overall community structure is sparse due to inconsistent sampling across their very large organismal size range. Here we use diverse imaging methods to establish complete plankton inventories of organisms spanning five orders of magnitude in size. Plankton community size and trophic structure variation validate a long-held theoretical link between organism size-spectra and ecosystem trophic structures. We found that predator/grazer biomass and biovolume unexpectedly exceed that of primary producers at most (55%) locations, likely due to our better quantification of gelatinous organisms. Bottom- heavy ecosystems (the norm on land) appear to be rare in the ocean. Collectively, gelatinous organisms represent 30% of the total biovolume (8-9% of carbon) of marine plankton communities from tropical to polar ecosystems. Communities can be split into three extreme typologies: diatom/copepod-dominated in eutrophic blooms, rhizarian/chaetognath-dominated in oligotrophic tropical oceans, and gelatinous-dominated elsewhere. While plankton taxonomic composition changes with latitude, functional and trophic structures mostly depend on the amount of prey available for each trophic level. Given future projections of oligotrophication of marine ecosystems, our findings suggest that rhizarian and gelatinous organisms will increasingly dominate the apex position of planktonic ecosystems, leading to significant changes in the ocean’s carbon cycle

Ocean-wide comparisons of mesopelagic planktonic community structures

International audienceFor decades, marine plankton have been investigated for their capacity to modulate biogeochemical cycles and provide fishery resources. Between the sunlit (epipelagic) layer and the deep dark waters, lies a vast and heterogeneous part of the ocean: the mesopelagic zone. How plankton composition is shaped by environment has been well-explored in the epipelagic but much less in the mesopelagic ocean. Here, we conducted comparative analyses of trans-kingdom community assemblages thriving in the mesopelagic oxygen minimum zone (OMZ), mesopelagic oxic, and their epipelagic counterparts. We identified nine distinct types of intermediate water masses that correlate with variation in mesopelagic community composition. Furthermore, oxygen, NO 3 − and particle flux together appeared as the main drivers governing these communities. Novel taxonomic signatures emerged from OMZ while a global co-occurrence network analysis showed that about 70% of the abundance of mesopelagic plankton groups is organized into three community modules. One module gathers prokaryotes, pico-eukaryotes and Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) from oxic regions, and the two other modules are enriched in OMZ prokaryotes and OMZ pico-eukaryotes, respectively. We hypothesize that OMZ conditions led to a diversification of ecological niches, and thus communities, due to selective pressure from limited resources. Our study further clarifies the interplay between environmental factors in the mesopelagic oxic and OMZ, and the compositional features of communities

Global Trends in Marine Plankton Diversity across Kingdoms of Life

The 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 Glades 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 marine conservation