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

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 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.

Revisiting Australian Ectocarpus subulatus (Phaeophyceae) From the Hopkins River: Distribution, Abiotic Environment, and Associated Microbiota

“…In a context of the development of new laboratory models for the study of marine holobionts (Dittami et al. ), a targeted examination of these potential changes (e.g., by following the evolution of alga‐associated microbiomes in the field as well as over several cultivation cycles) may yield important insights on possible limitations of laboratory model systems. If confirmed, such biases would underline the necessity of devising targeted experiments to test the validity of laboratory findings in the field.…”

Revisiting australianectocarpus subulatus(phaeophyceae) from the hopkins river: distribution, abiotic environment, and associated microbiota

“…Nevertheless, the profoundness of the observed differences suggests that either the microbiome of E. subulatus in the Hopkins River has evolved and diversified over time or that the cultivation of algae in the laboratory has impacted its microbiome, leading to a reduction of diversity and a change in composition. In a context of the development of new laboratory models for the study of marine holobionts (Dittami et al 2019, preprint), a targeted examination of these potential changes, e.g. by following the evolution of alga-associated microbiomes in the field as well as over several cultivation cycles may yield important insights on possible limitations of laboratory model systems.…”

The Seagrass Holobiont: What We Know and What We Still Need to Disclose for Its Possible Use as an Ecological Indicator

“…Host-microbes interactions play crucial roles in biological and ecological functions, thus, organisms are better considered as a network of interactions between the host and all the associated microorganisms (bacteria, fungi and viruses), with which the host establishes transient or lasting complex relationships [40][41][42]. The host and the entirety of microorganisms living in/on its tissues represent a complex functional unit, the holobiont [33].…”