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

Type Article
Date 2021-02
Language English
Author(s) Dittami Simon M1, Arboleda Enrique2, Auguet Jean-Christophe3, Bigalke Arite4, Briand EnoraORCID5, Cardenas Paco6, Cardini Ulisse7, Decelle Johan8, Engelen Aschwin9, Eveillard Damien10, Gachon Claire Mm11, Griffiths Sarah12, Harder Tilmann13, Kayal Ehsan2, Kazamia Elena14, Lallier François H15, Media Monica16, Marzinelli Ezequiel M17, 18, 19, Morganti Teresa20, Nunez Pons Laura21, Prado Soizik22, Pintado José23, Saha Mahasweta24, 25, Selosse Marc-André26, 27, Skillings Derek28, Stock Willem29, Sunagawa Shinichi30, Toulza Eve31, Vorobev Alexey32, Leblanc Catherine1, Not Fabrice15
Affiliation(s) 1 : UMR8227, Sorbonne Université, CNRS, Station Biologique de Roscoff, Roscoff, France
2 : FR2424, Sorbonne Université, CNRS, Station Biologique de Roscoff, Roscoff, 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, 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
Source Peerj (2167-8359) (PeerJ), 2021-02 , Vol. 9 , P. e10911 (34p.)
DOI 10.7717/peerj.10911
WOS© Times Cited 42
Keyword(s) Evolution, Ecosystem services, Symbiosis, Host-microbiota interactions, Marine holobionts, Dysbiosis
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.

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Dittami Simon M, Arboleda Enrique, Auguet Jean-Christophe, Bigalke Arite, Briand Enora, Cardenas Paco, Cardini Ulisse, Decelle Johan, Engelen Aschwin, Eveillard Damien, Gachon Claire Mm, Griffiths Sarah, Harder Tilmann, Kayal Ehsan, Kazamia Elena, Lallier François H, Media Monica, Marzinelli Ezequiel M, Morganti Teresa, Nunez Pons Laura, Prado Soizik, Pintado José, Saha Mahasweta, Selosse Marc-André, Skillings Derek, Stock Willem, Sunagawa Shinichi, Toulza Eve, Vorobev Alexey, Leblanc Catherine, Not Fabrice (2021). A community perspective on the concept of marine holobionts: current status, challenges, and future directions. Peerj, 9, e10911 (34p.). Publisher's official version : https://doi.org/10.7717/peerj.10911 , Open Access version : https://archimer.ifremer.fr/doc/00480/59209/