Nutrient-rich environments erode host-microbiome stability in a coastal cnidarian.
Anthropogenic nutrient enrichment is intensifying in coastal ecosystems, yet its consequences for host-microbe interactions and animal fitness remain poorly understood. Here, we examine how increased nutrient availability and nutrient composition affect microbiome stability and host responses in the sea anemone Nematostella vectensis. We experimentally enriched seawater with either a complex organic nutrient source or a protein-rich substrate and quantified changes in microbiome composition, host behavior, and population growth. Nutrient enrichment caused pronounced restructuring of the host-associated microbiome, reducing diversity and promoting dominance of fast-growing bacterial taxa, with distinct community outcomes depending on nutrient composition. Despite the absence of overt disease, enriched conditions triggered a previously undescribed ectodermal molting behavior that physically removed surface-associated microbes and selectively shed opportunistic bacteria. This host-mediated response mitigated microbial overgrowth but imposed substantial physiological costs, leading to reduced or negative population growth under nutrient enrichment. Together, these results demonstrate that nutrient enrichment destabilizes host-microbiome homeostasis and reveals molting as a costly yet effective mechanism of microbial regulation, providing mechanistic insight into how eutrophication can drive dysbiosis and erode host fitness even in the absence of disease.