Published August 23, 2019
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A community perspective on the concept of marine holobionts: current status, challenges, and future directions
Creators
- Dittami, Simon M1
- Arboleda, Enrique2
- Auguet, Jean-Christophe3
- Bigalke, Arite4
- Briand, Enora5
- Cárdenas, Paco6
- Cardini, Ulisse7
- Decelle, Johan8
- Engelen, Aschwin H9
- Eveillard, Damien10
- Gachon, Claire MM11
- Griffiths, Sarah M12
- Harder, Tilmann13
- Kayal, Ehsan2
- Kazamia, Elena14
- Lallier, François H15
- Medina, Mónica16
- Marzinelli, Ezequiel17
- Morganti, Teresa18
- Núñez Pons, Laura19
- Prado, Soizic20
- Pintado, José21
- Saha, Mahasweta22
- Selosse, Marc-André23
- Skillings, Derek24
- Stock, Willem25
- Sunagawa, Shinichi26
- Toulza, Eve27
- Vorobev, Alexey28
- Leblanc, Catherine1
- Not, Fabrice15
- 1. UMR8227, Sorbonne Université, CNRS, Station Biologique de Roscoff, Roscoff, Brittany, France
- 2. FR2424, Sorbonne Université, CNRS, Station Biologique de Roscoff, Roscoff, Brittany, France
- 3. MARBEC, Université de Montpellier, CNRS, IFREMER, IRD, Montpellier, France
- 4. Institute for Inorganic and Analytical Chemistry, Bioorganic Analytics, Friedrich-Schiller-Universität Jena, Jena, Germany
- 5. Laboratoire Phycotoxines, Ifremer, Nantes, France
- 6. Pharmacognosy, Department of Medicinal Chemistry, Uppsala Universitet, Uppsala, Sweden
- 7. Integrative Marine Ecology Department, Stazione Zoologica Anton Dohrn, Napoli, Italy
- 8. Laboratoire de Physiologie Cellulaire et Végétale, Université Grenoble Alpes, CNRS, CEA, INRA, Grenoble, France
- 9. CCMAR, Universidade do Algarve, Faro, Portugal
- 10. Laboratoire des Sciences Numériques de Nantes (LS2N), Université de Nantes, CNRS, Nantes, France
- 11. Scottish Association for Marine Science Scottish Marine Institute, Oban, United Kingdom
- 12. School of Science and the Environment, The Manchester Metropolitan University, Manchester, United Kingdom
- 13. University of Bremen, Bremen, Germany
- 14. Institut de Biologie, Ecole Normale Supérieure, Paris, France
- 15. Adaptation and Diversity in the Marine Environment, Sorbonne Université, CNRS, Station Biologique de Roscoff, Roscoff, Brittany, France
- 16. Department of Biology, Pennsylvania State University, University Park, USA
- 17. School of Life and Environmental Sciences, The University of Sydney, Sydney, Australia; Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, Singapore; Sydney Institute of Marine Science, Mosman, Australia
- 18. Max Planck Institute for Marine Microbiology, Bremen, Germany
- 19. Section Biology and Evolution of Marine Organisms (BEOM), Stazione Zoologica Anton Dohrn (SZN), Napoli, Italy
- 20. Molecules of Communication and Adaptation of Microorganisms (UMR 7245), National Museum of Natural History, CNRS, Paris, France
- 21. Instituto de Investigaciones Marinas (IIM-CSIC), Vigo, Spain
- 22. Benthic Ecology, Helmholtz Center for Ocean Research, Kiel, Germany; Marine Ecology and Biodiversity, Plymouth Marine Laboratory, Plymouth, United Kingdom
- 23. Département Systématique et Evolution, Muséum national d'Histoire naturelle, Paris, France; Faculty of Biology, University of Gdansk, Gdansk, Poland
- 24. Philosophy Department, University of Pennsylvania, Philadelphia, USA
- 25. Laboratory of Protistology & Aquatic Ecology, Department of Biology, Ghent University, Ghent, Belgium
- 26. Department of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zürich, Zürich, Switzerland
- 27. IHPE UMR 5244, Univ. Perpignan Via Domitia, CNRS, IFREMER, Univ. Montpellier, Perpignan, France
- 28. Genoscope, CEA ‐ Institut de Biologie François Jacob, Evry, France
Description
ABSTTRACT
Host-microbe interactions play crucial roles in marine ecosystems, but we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help to describe and understand these complex systems. It posits that a host and its associated microbiota, living together in a stable relationship, form the holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences with comparisons to terrestrial sciences where appropriate. Given the connectivity and the unexplored biodiversity specific to marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances, e.g. the development of controlled experimental model systems for holobionts from all major lineages and the modeling of (info)chemical-mediated interactions between organisms. The most significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This will be crucial to decipher the roles of marine holobionts in biogeochemical cycles, but also developing concrete applications of the holobiont concept e.g. to increase yield or disease resistance in aquacultures or to protect and restore marine ecosystems through management projects.
Notes
ACKNOWLEDGEMENTS
This paper is based on the results of a foresight workshop funded by the EuroMarine network, Sorbonne University, and the UMRs 8227 and 7144 of the Roscoff Biological Station. We are grateful to Catherine Boyen for useful advice and helpful discussions. We thank Sylvie Kwayeb-Fagon for workshop facilitation; Maryvonne Saout and Léna Corre for administrative support; and Marc Trousselier, Sébastien Villéger, Arthur Escalas, Yvan Bettarel, Thierry Bouvier for help writing a part of the manuscript. EMM was partially funded by an Australian Research Council Discovery Project (DP180104041), and JP was partially funded by the Galician Innovation Agency (IN607A 2017/4). The work of SD ad CL was partially funded by the ANR project IDEALG (ANR-10-BTBR-04). CG, CL, and SD received funding from the European Union's Horizon 2020 research and innovation program under the Marie Sklodowska- Curie grant agreement number 624575 (ALFF). The work of FN was partially funded by the ANR project IMPEKAB (ANR-15-CE02-001). UC was partially funded by the Research Council of Lithuania project INBALANCE (09.3.3-LMT-K-712-01-0069). JD was supported by the LabEx GRAL (ANR-10-LABX-49-01) and Pȏle CBS from the University of Grenoble Alpes. PC received support from the European Union's Horizon 2020 research and innovation program through the SponGES project (grant agreement No. 679849). EKAZ was funded by a Marie Curie Individual Fellowship (Horizon 2020, IRONCOMM). AHE was supported by Portuguese national funds from FCT - Foundation for Science and Technology through project UID/Multi/04326/2019. This document reflects only the authors' view and the Executive Agency for Small and Medium-sized Enterprises (EASME) is not responsible for any use that may be made of the information it contains.
AUTHOR CONTRIBUTIONS
Simon M Dittami prepared figures and/or tables, authored or reviewed drafts of the paper, approved the final draft.
Enrique Arboleda authored or reviewed drafts of the paper, approved the final draft.
Jean-Christophe Auguet authored or reviewed drafts of the paper, approved the final draft.
Arite Bigalke authored or reviewed drafts of the paper, approved the final draft.
Enora Briand authored or reviewed drafts of the paper, approved the final draft.
Paco Cardenas authored or reviewed drafts of the paper, approved the final draft.
Ulisse Cardini authored or reviewed drafts of the paper, approved the final draft.
Johan Decelle authored or reviewed drafts of the paper, approved the final draft.
Aschwin H Engelen authored or reviewed drafts of the paper, approved the final draft.
Damien Eveillard authored or reviewed drafts of the paper, approved the final draft.
Claire M.M. Gachon authored or reviewed drafts of the paper, approved the final draft.
Sarah M Griffiths authored or reviewed drafts of the paper, approved the final draft.
Tilmann Harder authored or reviewed drafts of the paper, approved the final draft.
Ehsan Kayal authored or reviewed drafts of the paper, approved the final draft.
Elena Kazamia authored or reviewed drafts of the paper, approved the final draft.
François H Lallier authored or reviewed drafts of the paper, approved the final draft.
Mónica Medina authored or reviewed drafts of the paper, approved the final draft.
Ezequiel Marzinelli authored or reviewed drafts of the paper, approved the final draft.
Teresa Morganti authored or reviewed drafts of the paper, approved the final draft.
Laura Núñez Pons authored or reviewed drafts of the paper, approved the final draft.
Soizic Prado authored or reviewed drafts of the paper, approved the final draft.
José Pintado authored or reviewed drafts of the paper, approved the final draft.
Mahasweta Saha authored or reviewed drafts of the paper, approved the final draft.
Marc-André Selosse authored or reviewed drafts of the paper, approved the final draft.
Derek Skillings authored or reviewed drafts of the paper, approved the final draft.
Willem Stock prepared figures and/or tables, authored or reviewed drafts of the paper, approved the final draft.
Shinichi Sunagawa authored or reviewed drafts of the paper, approved the final draft.
Eve Toulza authored or reviewed drafts of the paper, approved the final draft.
Alexey Vorobev authored or reviewed drafts of the paper, approved the final draft.
Catherine Leblanc prepared figures and/or tables, authored or reviewed drafts of the paper, approved the final draft.
Fabrice Not prepared figures and/or tables, authored or reviewed drafts of the paper, approved the final draft.
FUNDING
EMM was partially funded by an Australian Research Council Discovery Project (DP180104041), and JP was partially funded by the Galician Innovation Agency (IN607A 2017/4). The work of SD ad CL was partially funded by the ANR project IDEALG (ANR-10-BTBR-04). CG, CL, and SD received funding from the European Union's Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement number 624575 (ALFF). The work of FN was partially funded by the ANR project IMPEKAB (ANR-15-CE02-001). UC was partially funded by the Research Council of Lithuania project INBALANCE (09.3.3-LMT-K-712-01-0069). JD was supported by the LabEx GRAL (ANR-10-LABX-49-01) and Pȏle CBS from the University of Grenoble Alpes. PC received support from the European Union's Horizon 2020 research and innovation program through the SponGES project (grant agreement No. 679849). EKAZ was funded by a Marie Curie Individual Fellowship (Horizon 2020, IRONCOMM). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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- Preprint: https://peerj.com/preprints/27519/# (URL)
Funding
- SponGES – Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation 679849
- European Commission
- IRONCOMM – Investigating the role of bacteria-produced siderophores in satisfying diatom Fe requirements. 748581
- European Commission