1. Below-ground microbiota play an important role in mediating environmental conditions with important consequences for plant performance. Micro-organisms involved in plant-soil interactions may be associated with roots or bulk soil; however, the relative influence of these below-ground microbial assemblages on plant performance is poorly known, particularly for marine plants.2. We separately manipulated the root and sediment microbial assemblages of the seagrass Zostera muelleri in a fully factorial experiment to determine how these assemblages determined plant response (e.g. growth) to nutrient enrichment, a major stressor in marine systems.3. Under ambient nutrient conditions, seagrass growth was maintained regardless of root microbial assemblage disruption. Under high nutrient stress, however, seagrasses with disrupted root microbiota had reduced growth, whereas growth was maintained in seagrasses with an intact root microbiota. Disruption of bulksediment microbiota did not affect seagrass growth. Nutrient elevation was correlated with enhanced abundances of several putatively beneficial microbial taxa (e.g. sulphide-oxidising Beggiatoaceae and denitrifying Geofilum rubicundum) associated with roots. 4. Synthesis. Our results suggest that under ambient nutrient conditions microorganisms play a reduced role in influencing plant performance, but under more stressful conditions positive plant-root micro-organism interactions strengthened. These results are among the first to experimentally determine that interactions between marine plants and the root-associated microbiota are key drivers of seagrass performance under human-induced environmental changes. This suggests that as in terrestrial systems, marine plant resilience depends on the stress-mitigating functions of their root-associated microbiota and disturbance to those plant-microbiota interactions can be deleterious for plant performance.Improving our understanding of these plant-micro-organism interactions may be critical for understanding the functioning and resilience of threatened marine plants and developing more effective restoration strategies for them.

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