A community perspective on the concept of marine holobionts: state-of-the-art, challenges, and future directions

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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
18 Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, Singapore
19 Sydney Institute of Marine Science, Mosman, Australia
20 Max Planck Institute for Marine Microbiology, Bremen, Germany
21 Section Biology and Evolution of Marine Organisms (BEOM), Stazione Zoologica Anton Dohrn (SZN), Napoli, Italy
22 Molecules of Communication and Adaptation of Microorganisms (UMR 7245), National Museum of Natural History, CNRS, Paris, France
23 Instituto de Investigaciones Marinas (IIM-CSIC), Vigo, Spain
24 Benthic Ecology, Helmholtz Center for Ocean Research, Kiel, Germany
25 School of Biological Sciences, University of Essex, Essex, United Kingdom
26 Département Systématique et Evolution, Muséum national d’Histoire naturelle, Paris, France
27 Faculty of Biology, University of Gdansk, Gdansk, Poland
28 Philosophy Department, University of Pennsylvania, Philadelphia, USA
29 Laboratory of Protistology & Aquatic Ecology, Department of Biology, Ghent University, Ghent, Belgium
30 Department of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zürich, Zürich, Switzerland
31 IHPE UMR 5244, Univ. Perpignan Via Domitia, CNRS, IFREMER, Univ. Montpellier, Perpignan, France
32 Genoscope, CEA ‐ Institut de Biologie François Jacob, Evry, France
DOI
10.7287/peerj.preprints.27519v1
Published
Accepted
Subject Areas
Ecology, Marine Biology, Microbiology
Keywords
Evolution, Ecosystem services, Symbiosis, Host-microbiota interactions, Marine holobionts, Dysbiosis
Copyright
© 2019 Dittami et al.
Licence
This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ Preprints) and either DOI or URL of the article must be cited.
Cite this article
Dittami SM, Arboleda E, Auguet J, Bigalke A, Briand E, Cárdenas P, Cardini U, Decelle J, Engelen A, Eveillard D, Gachon CMM, Griffiths S, Harder T, Kayal E, Kazamia E, Lallier FH, Media M, Marzinelli EM, Morganti T, Núñez Pons L, Prado S, Pintado J, Saha M, Selosse M, Skillings D, Stock W, Sunagawa S, Toulza E, Vorobev A, Leblanc C, Not F. 2019. A community perspective on the concept of marine holobionts: state-of-the-art, challenges, and future directions. PeerJ Preprints 7:e27519v1

Abstract

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 describe and understand these complex systems. It posits that a host and its associated microbiota, living together in a long-lasting relationship, form the holobiont, and have to be studied together, as a coherent biological and functional unit, in order to understand the biology, ecology and evolution of the organisms. 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 science whenever appropriate. A deeper understanding of such complex systems, however, will require further technological and conceptual advances. The most significant challenge will be to bridge functional research on simple and tractable model systems and global approaches. This will require scientists to work together as an (inter)active community in order to address, for instance, ecological and evolutionary questions and the roles of holobionts in biogeochemical cycles.

Author Comment

The results described in this manuscript are derived from a foresight workshop hosted at the Roscoff Biological Station in March 2018, which brought together an interdisciplinary group of 31 scientists (philosophy, evolution, computer sciences, marine biology, ecology, chemistry, microscopy, and microbiology) working on different model systems (from phytoplankton, via macroalgae, corals, and sponges, to bacterial communities of hydrothermal vents) for a two-day brainstorming session on the topic of "marine holobionts: concepts and challenges".