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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 ( 13 C) and nitrate ( 15 N) 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 abstractSupplementary Information  The online version contains supplementary material available at 10.1186/s40168-021-01075-0.

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