Phyllosphere microbes decouple nutrient enrichment from plant productivity

Abstract

Resource limitation theory predicts that nutrient enrichment enhances plant productivity. Yet plant-associated microbes can modify this relationship by facilitating nutrient acquisition, competing for resources, or restructuring the plant-environment interface. These processes generate contrasting predictions for whether added nutrients are converted into plant population growth. Whether phyllosphere microbiomes mediate this resource-productivity relationship remains unclear. Here we show that phyllosphere microbiomes decoupled nutrient enrichment from productivity in a duckweed polyploid complex. In microbe-free microcosm ecosystems, nutrient enrichment increased productivity, whereas with microbes, enrichment failed to increase productivity despite abundant residual nutrients. This decoupling was not explained by direct microbial competition for nutrients or predicted microbial functions associated with pathogenicity, oxygen depletion, or acidification. Instead, nutrient enrichment stimulated biofilm formation, potentially restricting plant access to nutrients. Predicted microbial phosphorus immobilization and transformation also increased, but neither explained the decline in ecosystem phosphorus removal. This decline instead reflected lower plant productivity associated with biofilm formation, leaving much of the phosphorus unused. These patterns were consistent across ploidy levels, with the productivity advantage of polyploids associated with greater nutrient-use efficiency rather than greater tolerance of microbial effects. Our results reveal that phyllosphere microbiomes mediate how nutrient enrichment translates into ecosystem functioning.