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

Simon Dittami (1) , Enrique Arboleda (2) , J.-C. Auguet (3) , Arite Bigalke (4) , Enora Briand (5) , Paco Cárdenas (6) , Ulisse Cardini (7) , Johan Decelle (8) , Ashwin Engelen (9) , Damien Eveillard (10, 11) , Claire M M Gachon (12) , Sarah Griffiths (13) , Tilmann Harder (14) , Ehsan Kayal (15, 16, 2) , Elena Kazamia (17) , François Lallier (18) , Mónica Medina (19) , Ezequiel M Marzinelli (20, 21, 22) , Teresa Morganti (23) , Laura Núñez Pons (7) , Soizic Prado (24) , José Pintado Valverde (25) , Mahasweta Saha (26, 27) , Marc-Andre Selosse (28, 29) , Derek Skillings (30) , Willem Stock (31) , Shinichi Sunagawa (32) , Eve Toulza (33) , Alexey Vorobev (34) , Catherine Leblanc (1) , Fabrice Not (35)

1 LBI2M - Laboratoire de Biologie Intégrative des Modèles Marins
2 SBR - Station biologique de Roscoff = Roscoff Marine Station
3 UMR MARBEC - MARine Biodiversity Exploitation and Conservation
4 Institute for Inorganic and Analytical Chemistry
5 IFREMER - Institut Français de Recherche pour l'Exploitation de la Mer
6 Department of Medicinal Chemistry, Uppsala University, Sweden
7 SZN - Stazione Zoologica Anton Dohrn
8 LPCV - Laboratoire de physiologie cellulaire végétale
9 CCMAR - Centre of Marine Sciences [Faro]
10 LS2N - Laboratoire des Sciences du Numérique de Nantes
11 LS2N - équipe COMBI - Combinatoire et Bioinformatique
12 SAMS - Scottish Association for Marine Science
13 School of Science and the Environment
14 University of Bremen
15 ABIMS - ABiMS - Informatique et bioinformatique = Analysis and Bioinformatics for Marine Science
16 FR2424 - Fédération de recherche de Roscoff
17 IBENS - Institut de biologie de l'ENS Paris
18 ABICE - Adaptation et Biologie des Invertébrés en Conditions Extrêmes
19 Penn State - Pennsylvania State University
20 Faculty of Science, School of Life and Environmental Sciences
21 SCELSE - Singapore Centre for Environmental Life Sciences Engineering [Singapore]
22 USIMS - University of Sydney Institute of Marine Science
23 Max Planck Institute for Marine Microbiology
24 MCAM - Molécules de Communication et Adaptation des Micro-organismes
25 IIM CSIC
26 GEOMAR - Helmholtz Centre for Ocean Research [Kiel]
27 Department of Biological Sciences, University of Essex
28 OSEB - Origine, structure et évolution de la biodiversité
29 University of Gdansk
30 University of Pennsylvania
31 Laboratory of Protistology & Aquatic Ecology
32 Institute of Microbiology and Swiss Institute of Bioinformatics
33 IHPE - Interactions Hôtes-Pathogènes-Environnements
34 CEA - Commissariat à l'énergie atomique et aux énergies alternatives
35 ADMM - Adaptation et diversité en milieu marin

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.

Domaines: Evolution [q-bio.PE]

Simon Dittami, Enrique Arboleda, J.-C. Auguet, Arite Bigalke, Enora Briand, et al.. A community perspective on the concept of marine holobionts: state-of-the-art, challenges, and future directions. PeerJ Preprints, 2019, 7, pp.e27519v1. ⟨10.7287/peerj.preprints.27519v1⟩. ⟨hal-03166872v1⟩