Functional division between root endosphere and rhizosphere microbiomes supports seagrass holobiont resilience under high nutrient and sulfide exposure

Coastal eutrophication leads to the co-occurrence of high nutrient loading and sulfide exposure, posing severe threats to the health of seagrass ecosystems. Yet the underlying adaptive mechanisms of the seagrass holobiont remain poorly understood. Here, we conducted a large-scale field investigation along a tropical natural gradient of nutrient and sulfide to examine the adaptive mechanisms of seagrass holobiont. By integrating plant physiology, stable isotopes, metabolomics, 16S rRNA amplicon, and shotgun metagenomics, we particularly explored the interaction between seagrass host and associated microbiome. The seagrass host exhibited physiological and metabolic patterns consistent with a growth-defense trade-off, with high nutrient conditions showing a more growth-related metabolite profile and sulfide exposure coinciding with a stronger antioxidant defense-related metabolite profile. The metabolic reprogramming was accompanied by changes in the relative abundance of several root exudates, including flavonoids and phenylpropanoids, rather than a significant bulk compositional shift. These differential exudates showed compartment-specific relationships with microbiome composition, with nitrogen-cycling taxa preferentially associated with the root endosphere under high nutrient conditions and sulfur-cycling taxa preferentially enriched in the rhizosphere under sulfide exposure. Notably, this putative functional division of labor appeared to be reconfigured under dual pressure, with endosphere communities showing greater representation of taxa putatively related to sulfur cycling. In addition, the rhizosphere microbiome showed stressor-tailored genomic potential, with sulfur oxidation and transfer related genes (e.g., fccBA and dsrEF ) more prominent under sulfide exposed conditions and redundant ammonia assimilation potential (e.g., gltD) under nutrient-enriched conditions, potentially relevant to nutrient stress mitigation. This work suggests that seagrass holobiont resilience to co-occurring nutrient and sulfide exposure may be associated with host changes in root exudation and compartmentalized microbiome functional potential. We propose that the putative functional division of root microbiota provides a useful ecological framework for developing microbiome-informed seagrass restoration and conservation strategies. Video Abstract