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

34 pages, 4 figures.-- Distributed under Creative Commons CC-BY 4.0

Host-microbe interactions play crucial roles in marine ecosystems. However, 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 with which it interacts, form a 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. 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. Here we propose that one significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This first step is crucial to decipher the main drivers of the dynamics and evolution of holobionts and to account for the holobiont concept in applied areas, such as the conservation, management, and exploitation of marine ecosystems and resources, where practical solutions to predict and mitigate the impact of human activities are more important than ever

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. Ezequiel M. Marzinelli was funded by an Australian Research Council Discovery Project (DP180104041), and José Pintado Valverde was funded by the Galician Innovation Agency (IN607A 2017/4). The work of Simon M. Dittami ad Catherine Leblanc was funded by the ANR project IDEALG (ANR-10-TBR-04). Claire M.M. Gachon, Catherine Leblanc, and SimonMDittami 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 Fabrice Not was funded by the ANR project IMPEKAB (ANR-15-CE02-001). Ulisse Cardini was funded by the Research Council of Lithuania project INBALANCE (09.3.3-LMT-K-712-01-0069). Johan Decelle was supported by the CNRS and the ATIP-Avenir program, the LabEx GRAL (ANR-10-LABX-49-01) and Pôle Dittami et CBS from the University of Grenoble Alpes. Paco Cardenas received support from the European Union's Horizon 2020 research and innovation program through the SponGES project (grant agreement No. 679849). Elena Kazamia was funded by a Marie Curie Individual Fellowship (Horizon 2020, IRONCOMM). Aschwin H Engelen was supported by Portuguese national funds from FCT - Foundation for Science and Technology through projects UID/Multi/04326/2019 and UIDB/04326/2020

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