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Insights into biotic and abiotic modulation of ocean mesopelagic communities

View ORCID ProfileJanaina Rigonato, View ORCID ProfileMarko Budinich, Alejandro A. Murillo, Manoela C. Brandão, View ORCID ProfileJuan J. Pierella Karlusich, Yawouvi Dodji Soviadan, Ann C. Gregory, Hisashi Endo, Florian Kokoszka, Dean Vik, Nicolas Henry, Paul Frémont, Karine Labadie, Ahmed A. Zayed, Céline Dimier, Marc Picheral, Sarah Searson, Julie Poulain, Stefanie Kandels, Stéphane Pesant, Eric Karsenti, The Tara Oceans coordinators, Peer Bork, View ORCID ProfileChris Bowler, Samuel Chaffron, Colomban de Vargas, View ORCID ProfileDamien Eveillard, Marion Gehlen, Daniele Iudicone, Fabien Lombard, Hiroyuki Ogata, Lars Stemmann, Matthew B. Sullivan, Shinichi Sunagawa, Patrick Wincker, Olivier Jaillon
doi: https://doi.org/10.1101/2021.02.26.433055
Janaina Rigonato
1Génomique Métabolique, Genoscope, Institut de Biologie François Jacob, Commissariat à l’Energie Atomique (CEA), CNRS, Université Evry, Université Paris-Saclay, 91000 Evry, France
17Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange,75016 Paris, France
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  • ORCID record for Janaina Rigonato
  • For correspondence: jana_rigonato@protonmail.com ojaillon@genoscope.cns.fr
Marko Budinich
2Sorbonne Université, CNRS, Station Biologique de Roscoff, AD2M, UMR 7144, 29680 Roscoff, France
3Université de Nantes, CNRS UMR 6004, LS2N, F-44000 Nantes, France
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Alejandro A. Murillo
4Structural and Computational Biology, European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany
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Manoela C. Brandão
5Sorbonne Université, CNRS, Laboratoire d’Océanographie de Villefranche (LOV), 06230 Villefranche-sur-Mer, France
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Juan J. Pierella Karlusich
6Institut de Biologie de l’ENS (IBENS), Département de biologie, Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
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Yawouvi Dodji Soviadan
5Sorbonne Université, CNRS, Laboratoire d’Océanographie de Villefranche (LOV), 06230 Villefranche-sur-Mer, France
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Ann C. Gregory
7Department of Microbiology, The Ohio State University, Columbus, OH 43214, USA
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Hisashi Endo
8Bioinformatics Center, Institute for Chemical Research Kyoto University, Gokasho, Uji, Kyoto, 611-0011, Japan
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Florian Kokoszka
6Institut de Biologie de l’ENS (IBENS), Département de biologie, Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
9Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy
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Dean Vik
7Department of Microbiology, The Ohio State University, Columbus, OH 43214, USA
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Nicolas Henry
2Sorbonne Université, CNRS, Station Biologique de Roscoff, AD2M, UMR 7144, 29680 Roscoff, France
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Paul Frémont
1Génomique Métabolique, Genoscope, Institut de Biologie François Jacob, Commissariat à l’Energie Atomique (CEA), CNRS, Université Evry, Université Paris-Saclay, 91000 Evry, France
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Karine Labadie
1Génomique Métabolique, Genoscope, Institut de Biologie François Jacob, Commissariat à l’Energie Atomique (CEA), CNRS, Université Evry, Université Paris-Saclay, 91000 Evry, France
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Ahmed A. Zayed
7Department of Microbiology, The Ohio State University, Columbus, OH 43214, USA
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Céline Dimier
2Sorbonne Université, CNRS, Station Biologique de Roscoff, AD2M, UMR 7144, 29680 Roscoff, France
6Institut de Biologie de l’ENS (IBENS), Département de biologie, Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
17Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange,75016 Paris, France
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Marc Picheral
5Sorbonne Université, CNRS, Laboratoire d’Océanographie de Villefranche (LOV), 06230 Villefranche-sur-Mer, France
17Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange,75016 Paris, France
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Sarah Searson
5Sorbonne Université, CNRS, Laboratoire d’Océanographie de Villefranche (LOV), 06230 Villefranche-sur-Mer, France
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Julie Poulain
1Génomique Métabolique, Genoscope, Institut de Biologie François Jacob, Commissariat à l’Energie Atomique (CEA), CNRS, Université Evry, Université Paris-Saclay, 91000 Evry, France
17Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange,75016 Paris, France
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Stefanie Kandels
4Structural and Computational Biology, European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany
10Directors’ Research European Molecular Biology Laboratory Meyerhofstr. 1 69117 Heidelberg Germany
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Stéphane Pesant
11MARUM, Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany
12PANGAEA, Data Publisher for Earth and Environmental Science, University of Bremen, Bremen, Germany
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Eric Karsenti
6Institut de Biologie de l’ENS (IBENS), Département de biologie, Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
10Directors’ Research European Molecular Biology Laboratory Meyerhofstr. 1 69117 Heidelberg Germany
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Peer Bork
6Institut de Biologie de l’ENS (IBENS), Département de biologie, Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
13Department of Bioinformatics, Biocenter, University of Würzburg, Würzburg, Germany
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Chris Bowler
6Institut de Biologie de l’ENS (IBENS), Département de biologie, Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
17Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange,75016 Paris, France
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Samuel Chaffron
3Université de Nantes, CNRS UMR 6004, LS2N, F-44000 Nantes, France
17Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange,75016 Paris, France
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Colomban de Vargas
2Sorbonne Université, CNRS, Station Biologique de Roscoff, AD2M, UMR 7144, 29680 Roscoff, France
17Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange,75016 Paris, France
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Damien Eveillard
3Université de Nantes, CNRS UMR 6004, LS2N, F-44000 Nantes, France
17Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange,75016 Paris, France
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Marion Gehlen
14Institut Pierre Simon Laplace, Laboratoire des Sciences du Climat et de l’Environnement, CEA, CNRS, Université Paris-Saclay, 91191 Gif-sur-Yvette cedex, France
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Daniele Iudicone
9Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy
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Fabien Lombard
5Sorbonne Université, CNRS, Laboratoire d’Océanographie de Villefranche (LOV), 06230 Villefranche-sur-Mer, France
17Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange,75016 Paris, France
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Hiroyuki Ogata
8Bioinformatics Center, Institute for Chemical Research Kyoto University, Gokasho, Uji, Kyoto, 611-0011, Japan
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Lars Stemmann
5Sorbonne Université, CNRS, Laboratoire d’Océanographie de Villefranche (LOV), 06230 Villefranche-sur-Mer, France
17Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange,75016 Paris, France
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Matthew B. Sullivan
7Department of Microbiology, The Ohio State University, Columbus, OH 43214, USA
15Department of Civil, Environmental and Geodetic Engineering, The Ohio State University, Columbus OH 43214 USA
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Shinichi Sunagawa
4Structural and Computational Biology, European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany
16Department of Biology; Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zurich; Zurich, 8093; Switzerland
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Patrick Wincker
1Génomique Métabolique, Genoscope, Institut de Biologie François Jacob, Commissariat à l’Energie Atomique (CEA), CNRS, Université Evry, Université Paris-Saclay, 91000 Evry, France
17Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange,75016 Paris, France
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Olivier Jaillon
1Génomique Métabolique, Genoscope, Institut de Biologie François Jacob, Commissariat à l’Energie Atomique (CEA), CNRS, Université Evry, Université Paris-Saclay, 91000 Evry, France
17Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange,75016 Paris, France
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  • For correspondence: jana_rigonato@protonmail.com ojaillon@genoscope.cns.fr
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Abstract

Marine plankton mitigate anthropogenic greenhouse gases, modulate biogeochemical cycles, and provide fishery resources. Plankton is distributed across a stratified ecosystem of sunlit surface waters and a vast, though understudied, mesopelagic ‘dark ocean’. In this study, we mapped viruses, prokaryotes, and pico-eukaryotes across 32 globally-distributed cross-depth samples collected during the Tara Oceans Expedition, and assessed their ecologies. Based on depth and O2 measurements, we divided the marine habitat into epipelagic, oxic mesopelagic, and oxygen minimum zone (OMZ) eco-regions. We identified specific communities associated with each marine habitat, and pinpoint environmental drivers of dark ocean communities. Our results indicate that water masses primarily control mesopelagic community composition. Through co-occurrence network inference and analysis, we identified signature communities strongly associated with OMZ eco-regions. Mesopelagic communities appear to be constrained by a combination of factors compared to epipelagic communities. Thus, variations in a given abiotic factor may cause different responses in sunlit and dark ocean communities. This study expands our knowledge about the ecology of planktonic organisms inhabiting the mesopelagic zone.

Competing Interest Statement

The authors have declared no competing interest.

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Insights into biotic and abiotic modulation of ocean mesopelagic communities
Janaina Rigonato, Marko Budinich, Alejandro A. Murillo, Manoela C. Brandão, Juan J. Pierella Karlusich, Yawouvi Dodji Soviadan, Ann C. Gregory, Hisashi Endo, Florian Kokoszka, Dean Vik, Nicolas Henry, Paul Frémont, Karine Labadie, Ahmed A. Zayed, Céline Dimier, Marc Picheral, Sarah Searson, Julie Poulain, Stefanie Kandels, Stéphane Pesant, Eric Karsenti, The Tara Oceans coordinators, Peer Bork, Chris Bowler, Samuel Chaffron, Colomban de Vargas, Damien Eveillard, Marion Gehlen, Daniele Iudicone, Fabien Lombard, Hiroyuki Ogata, Lars Stemmann, Matthew B. Sullivan, Shinichi Sunagawa, Patrick Wincker, Olivier Jaillon
bioRxiv 2021.02.26.433055; doi: https://doi.org/10.1101/2021.02.26.433055
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Insights into biotic and abiotic modulation of ocean mesopelagic communities
Janaina Rigonato, Marko Budinich, Alejandro A. Murillo, Manoela C. Brandão, Juan J. Pierella Karlusich, Yawouvi Dodji Soviadan, Ann C. Gregory, Hisashi Endo, Florian Kokoszka, Dean Vik, Nicolas Henry, Paul Frémont, Karine Labadie, Ahmed A. Zayed, Céline Dimier, Marc Picheral, Sarah Searson, Julie Poulain, Stefanie Kandels, Stéphane Pesant, Eric Karsenti, The Tara Oceans coordinators, Peer Bork, Chris Bowler, Samuel Chaffron, Colomban de Vargas, Damien Eveillard, Marion Gehlen, Daniele Iudicone, Fabien Lombard, Hiroyuki Ogata, Lars Stemmann, Matthew B. Sullivan, Shinichi Sunagawa, Patrick Wincker, Olivier Jaillon
bioRxiv 2021.02.26.433055; doi: https://doi.org/10.1101/2021.02.26.433055

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