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. 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.

Seaweeds influence oyster microbiota and disease susceptibility

“…Although seaweed and oysters do not have direct ecological interactions, they are connected by seawater and share microbes. Our study therefore extends the concept of pathobiome beyond recognized pathogens to other ecosystem components, and contributes to establishing a community perspective of host-pathogen interactions (Dittami et al, 2021). These results are therefore important to better understand the risk of disease in marine ecosystems.…”

The Future Is Big—and Small: Remote Sensing Enables Cross-Scale Comparisons of Microbiome Dynamics and Ecological Consequences

“…Microbiome metrics may be particularly suited to identify and predict large-scale shifts in ecosystem structure and function ( 46 , 50 ). This requires integrating knowledge of how stressors impact hosts, microbes, and host-microbe interactions through time and space ( 51 ), a challenge for aquatic ecosystems, where chemical and microbial diversity—and their dynamics—remain underexplored ( 52 ).…”

The Epistemic Revolution Induced by Microbiome Studies: An Interdisciplinary View

“…Dr. Not illustrated this claim through an analysis of the most recent research on marine microbiomes, making it clear that, fifty years after the work initiated by Lovelock, our understanding of the marine microbiomes had now turned into a major scientific issue, and that, without explicit consideration of these microbiomes, major biogeochemical cycles impacting the planet, in particular the carbon cycle, could not be properly modeled. Yet, Dr. Not also showed that, while microbial studies were starting to unravel the role of microbes in the functioning of oceanic ecosystems, the functions and interactions of a shockingly large proportion of marine microbial genes and species remained problematically unknown [10][11][12][13]. Finally, Dr. Catherine Larose (CNRSEEA/Ampère, Lyon, France), a microbial ecologist, closed the first session by reflecting on the diversity and the evolution of microbial communities in Polar Regions.…”