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

Background: Marine holobionts depend on microbial partners for health and nutrient cycling. This is particularly evident amongst cnidarian-Symbiodiniaceae symbioses, where nutrient acquisition is facilitated. However, the symbiosis is sensitive to environmental change - including eutrophication - that cause dysbiosis and host mortality, which 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 (C-13) and nitrate (N-15) and metabarcoding approaches to evaluate nutrient cycling and microbial community composition in symbiotic and aposymbiotic medusae. Results: We found C-cycling within the C. xamachana holobiont to be essential as aposymbiotic medusae continuously lost weight even at high heterotrophic feeding rates. Heterotrophically acquired C and N were readily shared among host and algae. This was in sharp contrast to nitrate assimilation, which was strongly restricted from Symbiodiniaceae. Instead, the bacterial microbiome seemed to play a major role in the holobionts 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 (similar to 90 %) to nitrogen cycling and particularly denitrification. Observed bacterial community structure differed between apo- and symbiotic C. xamachana putatively highlighting enrichment of ammonium oxidizers and denitrifiers and depletion of nitrogen-fixators 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 algae-host relationship even under eutrophic conditions.

Automated summary

The marine holobiont Cassiopea xamachana demonstrates mechanisms to maintain stable symbiotic relationships in eutrophic environments, highlighting the importance of carbon cycling and the role of the bacterial microbiome in nitrogen cycling.