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      Genomic evidence for global ocean plankton biogeography shaped by large-scale current systems

      research-article
      1 , 2 , 3 , 4 , 5 , 6 , 7 , 5 , 6 , 5 , 6 , 8 , 9 , 10 , 1 , 6 , 11 , 6 , 12 , 5 , 6 , 13 , 14 , 15 , 16 , 17 , 1 , 6 , 6 , 18 , 5 , 6 , 12 , 19 , 19 , 5 , 6 , 1 , 6 , 20 , 1 , 21 , 22 , 23 , 6 , 12 , 6 , 12 , Tara Oceans Coordinators
      , 24 , 25 , 5 , 20 , 26 , 11 , 5 , 6 , 22 , 27 , 28 , 22 , 29 , 6 , 12 , 30 , 31 , 6 , 21 , 21 , 20 , 32 , 33 , 34 , 6 , 21 , 23 , 17 , 1 , 6 , 11 , 5 , 6 , 1 , 6 , , 3 , , 3 , , 5 , 6 ,
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      eLife
      eLife Sciences Publications, Ltd
      plankton biogeography, metagenomics, metabarcoding, microbial oceanography, Other

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          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 debated. Here we assessed the global structure of plankton geography and its relation to the biological, chemical, and physical context of the ocean (the ‘seascape’) by analyzing metagenomes of plankton communities sampled across oceans during the Tara Oceans expedition, in light of environmental data and ocean current transport. Using a consistent approach across organismal sizes that provides unprecedented resolution to measure changes in genomic composition between communities, we report a pan-ocean, size-dependent plankton biogeography overlying regional heterogeneity. We found robust evidence for a basin-scale impact of transport by ocean currents on plankton biogeography, and on a characteristic timescale of community dynamics going beyond simple seasonality or life history transitions of plankton.

          eLife digest

          Oceans are brimming with life invisible to our eyes, a myriad of species of bacteria, viruses and other microscopic organisms essential for the health of the planet. These ‘marine plankton’ are unable to swim against currents and should therefore be constantly on the move, yet previous studies have suggested that distinct species of plankton may in fact inhabit different oceanic regions. However, proving this theory has been challenging; collecting plankton is logistically difficult, and it is often impossible to distinguish between species simply by examining them under a microscope. However, within the last decade, a research schooner called Tara has travelled the globe to gather thousands of plankton samples. At the same time, advances in genomics have made it possible to identify species based only on fragments of their DNA sequence.

          To understand the hidden geography of plankton communities in Earth’s oceans, Richter et al. pored over DNA from the Tara Oceans expedition. This revealed that, despite being unable to resist the flow of water, various planktonic species which live close to the surface manage to occupy distinct, stable provinces shaped by currents. Different sizes of plankton are distributed in different sized provinces, with the smallest organisms tending to inhabit the smallest areas. Comparing DNA similarities and speeds of currents at the ocean surface revealed how these might stretch and mix plankton communities.

          Plankton play a critical role in the health of the ocean and the chemical cycles of planet Earth. These results could allow deeper investigation by marine modellers, ecologists, and evolutionary biologists. Meanwhile, work is already underway to investigate how climate change might impact this hidden geography.

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          Most cited references72

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          Silhouettes: A graphical aid to the interpretation and validation of cluster analysis

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            Microbial biogeography: putting microorganisms on the map.

            We review the biogeography of microorganisms in light of the biogeography of macroorganisms. A large body of research supports the idea that free-living microbial taxa exhibit biogeographic patterns. Current evidence confirms that, as proposed by the Baas-Becking hypothesis, 'the environment selects' and is, in part, responsible for spatial variation in microbial diversity. However, recent studies also dispute the idea that 'everything is everywhere'. We also consider how the processes that generate and maintain biogeographic patterns in macroorganisms could operate in the microbial world.
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              Decoupling function and taxonomy in the global ocean microbiome.

              Microbial metabolism powers biogeochemical cycling in Earth's ecosystems. The taxonomic composition of microbial communities varies substantially between environments, but the ecological causes of this variation remain largely unknown. We analyzed taxonomic and functional community profiles to determine the factors that shape marine bacterial and archaeal communities across the global ocean. By classifying >30,000 marine microorganisms into metabolic functional groups, we were able to disentangle functional from taxonomic community variation. We find that environmental conditions strongly influence the distribution of functional groups in marine microbial communities by shaping metabolic niches, but only weakly influence taxonomic composition within individual functional groups. Hence, functional structure and composition within functional groups constitute complementary and roughly independent "axes of variation" shaped by markedly different processes.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                03 August 2022
                2022
                : 11
                : e78129
                Affiliations
                Department of Marine Biology and Oceanography, Institut de Ciències del Mar (ICM), CSIC ( https://ror.org/05ect0289) BarcelonaSpain
                Structural and Computational Biology, European Molecular Biology Laboratory ( https://ror.org/03mstc592) HeidelbergGermany
                Yonsei Frontier, Yonsei University ( https://ror.org/01wjejq96) SeoulRepublic of Korea
                Department of Bioinformatics, Biocenter, University of Würzburg ( https://ror.org/00fbnyb24) WürzburgGermany
                School of Marine Sciences, University of Maine ( https://ror.org/01adr0w49) OronoUnited States
                Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOSEE ( https://ror.org/03egfjv78) ParisFrance
                Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole Normale Supérieure, CNRS, INSERM, Université PSL ( https://ror.org/013cjyk83) ParisFrance
                European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL‐EBI), Wellcome Trust Genome Campus, Hinxton CambridgeUnited Kingdom
                Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOSEE ( https://ror.org/03egfjv78) ParisFrance
                Sorbonne Université, CNRS, Station Biologique de Roscoff, UMR7144, ECOMAP ( https://ror.org/02en5vm52) RoscoffFrance
                Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOSEE ( https://ror.org/03egfjv78) ParisFrance
                Sorbonne Universités, CNRS, Laboratoire d’Oceanographie de Villefranche, LOV ( https://ror.org/02en5vm52) Villefranche‐sur‐MerFrance
                CNRS, UMR 7232, BIOM, Avenue Pierre Fabre ( https://ror.org/02feahw73) Banyuls‐sur‐MerFrance
                Sorbonne Universités Paris 06, OOB UPMC, Avenue Pierre Fabre ( https://ror.org/02en5vm52) Banyuls‐sur‐MerFrance
                Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOSEE ( https://ror.org/03egfjv78) ParisFrance
                Sorbonne Universités, CNRS, Laboratoire d’Oceanographie de Villefranche, LOV ( https://ror.org/02en5vm52) Villefranche‐sur‐MerFrance
                Aix Marseille Univ., Université de Toulon, CNRS, IRD, MIO UM 110, 13288 ( https://ror.org/02m9kbe37) MarseilleFrance
                Stazione Zoologica Anton Dohrn, Villa Comunale ( https://ror.org/03v5jj203) NaplesItaly
                Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOSEE ( https://ror.org/03egfjv78) ParisFrance
                Génomique Métabolique, Genoscope, Institut de Biologie François Jacob, CEA, CNRS, Université Evry, Université Paris‐Saclay ( https://ror.org/028pnqf58) EvryFrance
                Structural and Computational Biology, European Molecular Biology Laboratory ( https://ror.org/03mstc592) HeidelbergGermany
                Directors’ Research European Molecular Biology Laboratory Meyerhofstr ( https://ror.org/03mstc592) HeidelbergGermany
                School of Marine Sciences, University of Maine ( https://ror.org/01adr0w49) OronoUnited States
                Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOSEE ( https://ror.org/03egfjv78) ParisFrance
                Directors’ Research European Molecular Biology Laboratory Meyerhofstr ( https://ror.org/03mstc592) HeidelbergGermany
                Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l’Ecole Normale Supérieure (IBENS) ( https://ror.org/03mxktp47) ParisFrance
                Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOSEE ( https://ror.org/03egfjv78) ParisFrance
                Sorbonne Université, CNRS, Station Biologique de Roscoff, UMR7144, ECOMAP ( https://ror.org/02en5vm52) RoscoffFrance
                Institute for Chemical Research, Kyoto University, Gokasho ( https://ror.org/02kpeqv85) KyotoJapan
                MARUM, Center for Marine Environmental Sciences, University of Bremen ( https://ror.org/04ers2y35) BremenGermany
                PANGAEA, Data Publisher for Earth and Environmental Science, University of Bremen ( https://ror.org/04ers2y35) BremenGermany
                Department of Microbiology and Immunology, Rega Institute, KU Leuven ( https://ror.org/05f950310) LeuvenBelgium
                VIB Center for Microbiology ( https://ror.org/03xrhmk39) LeuvenBelgium
                Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOSEE ( https://ror.org/03egfjv78) ParisFrance
                Sorbonne Universités, UPMC Université Paris 06, CNRS, Laboratoire d’oceanographie de Villefranche (LOV), Observatoire Océanologique ( https://ror.org/02en5vm52) Villefranche‐sur‐MerFrance
                National Science Foundation ( https://ror.org/021nxhr62) ArlingtonUnited States
                Bigelow Laboratory for Ocean Sciences East Boothbay ( https://ror.org/03v2r6x37) BoothbayUnited States
                Laboratoire de Physique des Océans, UBO‐IUEM, Place Copernic ( https://ror.org/01b8h3982) PlouzanéFrance
                Department of Geosciences, Laboratoire de Météorologie Dynamique (LMD), Ecole Normale Supérieure ( https://ror.org/000ehr937) Paris CedexFrance
                Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOSEE ( https://ror.org/03egfjv78) ParisFrance
                Sorbonne Universités, CNRS, Laboratoire d’Oceanographie de Villefranche, LOV ( https://ror.org/02en5vm52) Villefranche‐sur‐MerFrance
                Department of Microbiology, The Ohio State University ( https://ror.org/020yh1f96) ColumbusUnited States
                EMERGE Biology Integration Institute, The Ohio State University ( https://ror.org/00rs6vg23) ColumbusUnited States
                Center of Microbiome Science, The Ohio State University ( https://ror.org/020yh1f96) ColumbusUnited States
                Department of Civil, Environmental and Geodetic Engineering, The Ohio State University ( https://ror.org/020yh1f96) ColumbusUnited States
                Structural and Computational Biology, European Molecular Biology Laboratory ( https://ror.org/03mstc592) HeidelbergGermany
                Institute of Microbiology, Department of Biology, ETH Zurich, Vladimir‐Prelog‐Weg ( https://ror.org/05a28rw58) ZurichSwitzerland
                Research Federation for the study of Global Ocean systems ecology and evolution, FR2022/Tara GOSEE ( https://ror.org/03egfjv78) ParisFrance
                Génomique Métabolique, Genoscope, Institut de Biologie François Jacob, CEA, CNRS, Université Evry, Université Paris‐Saclay ( https://ror.org/028pnqf58) EvryFrance
                [1 ] Sorbonne Université, CNRS, Station Biologique de Roscoff, UMR7144, ECOMAP ( https://ror.org/02en5vm52) Roscoff France
                [2 ] Institut de Biologia Evolutiva (CSIC‐Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta ( https://ror.org/044mj7r89) Barcelona Spain
                [3 ] Stazione Zoologica Anton Dohrn, Villa Comunale ( https://ror.org/03v5jj203) Naples Italy
                [4 ] CEA, DAM, DIF, F‐91297 ( https://ror.org/00jjx8s55) Arpajon Cedex France
                [5 ] Génomique Métabolique, Genoscope, Institut de Biologie François Jacob, CEA, CNRS, Université Evry, Université Paris‐Saclay ( https://ror.org/028pnqf58) Evry France
                [6 ] Research Federation for the study of Global Ocean systems ecology and evolution, FR2O22/Tara GOSEE ( https://ror.org/03egfjv78) Paris France
                [7 ] Aix Marseille Univ., Université de Toulon, CNRS, IRD, MIO UM ( https://ror.org/02feahw73) Marseille France
                [8 ] Changing Ocean Research Unit, Institute for the Oceans and Fisheries, University of British Columbia. Aquatic Ecosystems Research Lab ( https://ror.org/03rmrcq20) Vancouver Canada
                [9 ] Ecology and Evolutionary Biology, Yale University ( https://ror.org/00zm4rq24) New Haven, CT United States
                [10 ] Institut pasteur, Université Paris Cité, Bioinformatics and Biostatistics Hub ( https://ror.org/0495fxg12) Paris France
                [11 ] Univ Rennes, CNRS, Inria, IRISA-UMR 6074 ( https://ror.org/01m84wm78) Rennes France
                [12 ] Sorbonne Universités, CNRS, Laboratoire d’Oceanographie de Villefranche, LOV ( https://ror.org/02en5vm52) Villefranche‐sur‐Mer France
                [13 ] Lundbeck Foundation GeoGenetics Centre, GLOBE Institute, University of Copenhagen ( https://ror.org/035b05819) Copenhagen Denmark
                [14 ] MARUM, Center for Marine Environmental Sciences, University of Bremen ( https://ror.org/04ers2y35) Bremen Germany
                [15 ] Max Planck Institute for Marine Microbiology ( https://ror.org/02385fa51) Bremen Germany
                [16 ] Dipartimento di Fisica e Astronomia ‘G. Galilei’ & CNISM, INFN, Università di Padova ( https://ror.org/00240q980) Padova Italy
                [17 ] MaIAGE, INRAE, Université Paris‐Saclay ( https://ror.org/03xjwb503) Jouy‐en‐Josas France
                [18 ] Nantes Université, Ecole Centrale Nantes, CNRS, LS2N ( https://ror.org/03gnr7b55) Nantes France
                [19 ] Genoscope, Institut de biologie François‐Jacob, Commissariat à l'Energie Atomique (CEA), Université Paris‐Saclay ( https://ror.org/03xjwb503) Evry France
                [20 ] Department of Microbiology, The Ohio State University ( https://ror.org/00rs6vg23) Columbus United States
                [21 ] Institut de Biologie de l’Ecole Normale Supérieure (IBENS), Ecole Normale Supérieure, CNRS, INSERM, Université PSL ( https://ror.org/013cjyk83) Paris France
                [22 ] Structural and Computational Biology, European Molecular Biology Laboratory ( https://ror.org/03mstc592) Heidelberg Germany
                [23 ] Directors’ Research European Molecular Biology Laboratory ( https://ror.org/03mstc592) Heidelberg Germany
                [24 ] MARUM, Center for Marine Environmental Sciences, University of Bremen ( https://ror.org/04ers2y35) Bremen Germany
                [25 ] PANGAEA, Data Publisher for Earth and Environmental Science, University of Bremen ( https://ror.org/04ers2y35) Bremen Germany
                [26 ] Department of Oceanography and Coastal Sciences, Louisiana State University ( https://ror.org/05ect4e57) Baton Rouge United States
                [27 ] Yonsei Frontier Lab, Yonsei University ( https://ror.org/01wjejq96) Seoul Republic of Korea
                [28 ] Department of Bioinformatics, Biocenter, University of Würzburg ( https://ror.org/00fbnyb24) Würzburg Germany
                [29 ] Institute of Microbiology, Department of Biology, ETH Zurich, Vladimir‐Prelog‐Weg ( https://ror.org/02p1jz666) Zurich Switzerland
                [30 ] Institut Universitaire de France (IUF) ( https://ror.org/055khg266) Paris France
                [31 ] School of Marine Sciences, University of Maine ( https://ror.org/01adr0w49) Orono United States
                [32 ] EMERGE Biology Integration Institute, The Ohio State University ( https://ror.org/00rs6vg23) Columbus United States
                [33 ] Center of Microbiome Science, The Ohio State University ( https://ror.org/00rs6vg23) Columbus United States
                [34 ] Department of Civil, Environmental and Geodetic Engineering, The Ohio State University ( https://ror.org/020yh1f96) Columbus United States
                University of Oregon ( https://ror.org/0293rh119) United States
                University of Zurich ( https://ror.org/02crff812) Switzerland
                University of Oregon ( https://ror.org/0293rh119) United States
                University of Oregon ( https://ror.org/0293rh119) United States
                Author notes
                [†]

                These authors contributed equally to this work.

                Author information
                https://orcid.org/0000-0002-9238-5571
                https://orcid.org/0000-0002-7702-1382
                https://orcid.org/0000-0002-8679-490X
                https://orcid.org/0000-0001-8689-9907
                https://orcid.org/0000-0002-8162-7360
                https://orcid.org/0000-0002-6669-5744
                https://orcid.org/0000-0002-4721-0027
                https://orcid.org/0000-0003-1718-3010
                https://orcid.org/0000-0003-3065-0314
                https://orcid.org/0000-0003-3835-6187
                https://orcid.org/0000-0002-1643-1759
                https://orcid.org/0000-0002-6476-6019
                https://orcid.org/0000-0002-7237-9596
                Article
                78129
                10.7554/eLife.78129
                9348854
                35920817
                a56b1186-373d-4b59-b50a-e2115cca5851
                © 2022, Richter, Watteaux, Vannier et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 23 February 2022
                : 06 June 2022
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: HYDROGEN/ANR-14-CE23-0001
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: OCEANOMICS/ANR-11-BTBR-0008
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: OCE-1536989
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000780, European Commission;
                Award ID: MicroB3/287589
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council;
                Award ID: INMARE/634486
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100006489, Commissariat à l'Énergie Atomique et aux Énergies Alternatives;
                Award ID: Graduate Student Fellowship
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100017697, Graphene Flagship;
                Award ID: RITMARE
                Award Recipient :
                Funded by: Premiale;
                Award ID: MIUR NEMO
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100004584, Conseil Régional de Bretagne;
                Award ID: Postdoctoral Fellowship
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100014373, Institute for Bioengineering of Catalonia;
                Award ID: Beatriu de Pinós Postdoctoral Fellowship
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100010434, “la Caixa” Foundation;
                Award ID: LCF/BQ/PI19/11690008
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council;
                Award ID: 949745
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: OCE-1829831
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000936, Gordon and Betty Moore Foundation;
                Award ID: 3709
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100017186, Ohio Super Computer Center;
                Award ID: HPC support
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Ecology
                Genetics and Genomics
                Custom metadata
                Analysis of genomic DNA composition of surface plankton communities reveals a stable, ocean basin-scale plankton biogeography that emerges from the intertwined effects of environmental variations and currents.

                Life sciences
                plankton biogeography,metagenomics,metabarcoding,microbial oceanography,other
                Life sciences
                plankton biogeography, metagenomics, metabarcoding, microbial oceanography, other

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