Harnessing the Power of Model Organisms To Unravel Microbial Functions in the Coral Holobiont.

Stony corals build the framework of coral reefs, ecosystems of immense ecological and economic importance. The existence of these ecosystems is threatened by climate change and other anthropogenic stressors that manifest in microbial dysbiosis such as coral bleaching and disease, often leading to coral mortality. Despite a significant amount of research, the mechanisms ultimately underlying these destructive phenomena, and what could prevent or mitigate them, remain to be resolved. This is mostly due to practical challenges in experimentation on corals and the highly complex nature of the coral holobiont that also includes bacteria, archaea, protists, and viruses. While the overall importance of these partners is well recognized, their specific contributions to holobiont functioning and their interspecific dynamics remain largely unexplored. Here, we review the potential of adopting model organisms as more tractable systems to address these knowledge gaps. We draw on parallels from the broader biological and biomedical fields to guide the establishment, implementation, and integration of new and emerging model organisms with the aim of addressing the specific needs of coral research. We evaluate the cnidarian models Hydra, Aiptasia, Cassiopea, and Astrangia poculata; review the fast-evolving field of coral tissue and cell cultures; and propose a framework for the establishment of "true" tropical reef-building coral models. Based on this assessment, we also suggest future research to address key aspects limiting our ability to understand and hence improve the response of reef-building corals to future ocean conditions.

Holobiont nitrogen control and its potential for eutrophication resistance in an obligate photosymbiotic jellyfish.

BACKGROUND: Marine holobionts depend on microbial members for health and nutrient cycling. This is particularly evident in cnidarian-algae symbioses that facilitate energy and nutrient acquisition. However, this partnership is highly sensitive to environmental change-including eutrophication-that causes dysbiosis and contributes to global coral reef decline. Yet, some holobionts exhibit resistance to dysbiosis in eutrophic environments, including the obligate photosymbiotic scyphomedusa Cassiopea xamachana. METHODS: Our aim was to assess the mechanisms in C. xamachana that stabilize symbiotic relationships. We combined labelled bicarbonate (13C) and nitrate (15N) with metabarcoding approaches to evaluate nutrient cycling and microbial community composition in symbiotic and aposymbiotic medusae. RESULTS: C-fixation and cycling by algal Symbiodiniaceae was essential for C. xamachana as even at high heterotrophic feeding rates aposymbiotic medusae continuously lost weight. Heterotrophically acquired C and N were readily shared among host and algae. This was in sharp contrast to nitrate assimilation by Symbiodiniaceae, which appeared to be strongly restricted. Instead, the bacterial microbiome seemed to play a major role in the holobiont's DIN assimilation as uptake rates showed a significant positive relationship with phylogenetic diversity of medusa-associated bacteria. This is corroborated by inferred functional capacity that links the dominant bacterial taxa (~90 %) to nitrogen cycling. Observed bacterial community structure differed between apo- and symbiotic C. xamachana putatively highlighting enrichment of ammonium oxidizers and nitrite reducers and depletion of nitrogen-fixers in symbiotic medusae. CONCLUSION: Host, algal symbionts, and bacterial associates contribute to regulated nutrient assimilation and cycling in C. xamachana. We found that the bacterial microbiome of symbiotic medusae was seemingly structured to increase DIN removal and enforce algal N-limitation-a mechanism that would help to stabilize the host-algae relationship even under eutrophic conditions. Video abstract.