Functional specialization of the eelgrass rhizosphere microbiome: Root exudate-mediated assembly and implications for degraded meadow rehabilitation

Abstract

Seagrass meadows provide vital coastal ecosystem services but face accelerated degradation due to anthropogenic stressors. While rhizosphere microbes are recognized for enhancing nutrient cycling and supporting meadow resilience, the mechanisms by which seagrasses recruit functional groups critical for stress mitigation from bulk sediment via root exudates remain poorly understood. This study employed metagenomics and metabolomics to characterize Zostera marina root exudates and compare microbial (bacterial, fungal, archaeal) composition, diversity, and metabolic functions between bulk sediment and rhizosphere. We demonstrate that root exudates--enriched in organic acids and phenolic compounds--act as ecological filters, selectively enriching rhizosphere taxa with specialized functions relevant to habitat recovery, such as nitrogen/sulfur cycling (key processes for mitigating eutrophication impacts). Rhizosphere communities exhibited reduced diversity but heightened functional specialization aligned with host nutrition and stress tolerance, contrasting sharply with bulk sediment communities dominated by methane production and carbon degradation pathways. Critically, bulk sediment serves as a reservoir of pre-adapted genetic potential for environmental adaptation, supplying niche-adaptive genes to the rhizosphere microbiome. Strong metabolite-microbe correlations confirm host exudates as primary drivers of microbial assembly, synchronizing functional traits with host demands. These findings elucidate host-mediated recruitment strategies underpinning seagrass resilience and provide mechanistic insights for designing microbiome-assisted rehabilitation of degraded seagrass habitats. (Images were created with BioRender).