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

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 to 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 sciences where appropriate. 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. The most significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This will be crucial to decipher the roles of marine holobionts in biogeochemical cycles, but also developing concrete applications of the holobiont concept e.g. to increase yield or disease resistance in aquacultures or to protect and restore marine ecosystems through management projects.