A community perspective on the concept of marine holobionts: current status, challenges, and future directions

UMR8227, Sorbonne Université, CNRS, Station Biologique de Roscoff, Roscoff, Brittany, France
FR2424, Sorbonne Université, CNRS, Station Biologique de Roscoff, Roscoff, Brittany, France
MARBEC, Université de Montpellier, CNRS, IFREMER, IRD, Montpellier, France
Institute for Inorganic and Analytical Chemistry, Bioorganic Analytics, Friedrich-Schiller-Universität Jena, Jena, Germany
Laboratoire Phycotoxines, Ifremer, Nantes, France
Pharmacognosy, Department of Medicinal Chemistry, Uppsala Universitet, Uppsala, Sweden
Integrative Marine Ecology Department, Stazione Zoologica Anton Dohrn, Napoli, Italy
Laboratoire de Physiologie Cellulaire et Végétale, Université Grenoble Alpes, CNRS, CEA, INRA, Grenoble, France
CCMAR, Universidade do Algarve, Faro, Portugal
Laboratoire des Sciences Numériques de Nantes (LS2N), Université de Nantes, CNRS, Nantes, France
Scottish Association for Marine Science Scottish Marine Institute, Oban, United Kingdom
School of Science and the Environment, The Manchester Metropolitan University, Manchester, United Kingdom
University of Bremen, Bremen, Germany
Institut de Biologie, Ecole Normale Supérieure, Paris, France
Adaptation and Diversity in the Marine Environment, Sorbonne Université, CNRS, Station Biologique de Roscoff, Roscoff, Brittany, France
Department of Biology, Pennsylvania State University, University Park, USA
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
Max Planck Institute for Marine Microbiology, Bremen, Germany
Section Biology and Evolution of Marine Organisms (BEOM), Stazione Zoologica Anton Dohrn (SZN), Napoli, Italy
Molecules of Communication and Adaptation of Microorganisms (UMR 7245), National Museum of Natural History, CNRS, Paris, France
Instituto de Investigaciones Marinas (IIM-CSIC), Vigo, Spain
Benthic Ecology, Helmholtz Center for Ocean Research, Kiel, Germany
School of Biological Sciences, University of Essex, Essex, United Kingdom
Département Systématique et Evolution, Muséum national d’Histoire naturelle, Paris, France
Faculty of Biology, University of Gdansk, Gdansk, Poland
Philosophy Department, University of Pennsylvania, Philadelphia, USA
Laboratory of Protistology & Aquatic Ecology, Department of Biology, Ghent University, Ghent, Belgium
Department of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zürich, Zürich, Switzerland
IHPE UMR 5244, Univ. Perpignan Via Domitia, CNRS, IFREMER, Univ. Montpellier, Perpignan, France
Genoscope, CEA ‐ Institut de Biologie François Jacob, Evry, France
DOI
10.7287/peerj.preprints.27519v2
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 AH, Eveillard D, Gachon CMM, Griffiths SM, 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: current status, challenges, and future directions. PeerJ Preprints 7:e27519v2

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 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 science wherever appropriate. Given the connectivity and the unexplored biodiversity of marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances. For the marine scientific community, the most significant challenge is to bridge functional research on tractable and original model systems and global approaches addressing ecological and evolutionary questions. This will be crucial for establishing the roles of marine holobionts in biogeochemical cycles, but also developing concrete applications of the holobiont concept in aquaculture and marine ecosystem management projects.

Author Comment

Reorganization of manuscript, additional references, improved figures, numerous smaller corrections following a first round of peer review.