Eco-evolutionary interaction between microbiome presence and rapid biofilm evolution determines plant host fitness

Microbiomes are important to the survival and reproduction of their hosts. Although ecological and evolutionary processes can happen simultaneously in microbiomes, little is known about how microbiome eco-evolutionary dynamics determine host fitness. Here we show, using experimental evolution, that fitness of the aquatic plant Lemna minor is modified by interactions between the microbiome and the evolution of one member, Pseudomonas fluorescens. Microbiome presence promotes P. fluorescens' rapid evolution to form biofilm, which reciprocally alters the microbiome's species composition. These eco-evolutionary dynamics modify the host's multigenerational fitness. The microbiome and non-evolving P. fluorescens together promote host fitness, whereas the microbiome with P. fluorescens that evolves biofilm reduces the beneficial impact on host fitness. Additional experiments suggest that the microbial effect on host fitness may occur through changes in microbiome production of auxin, a plant growth hormone. Our study, therefore, experimentally demonstrates the importance of the eco-evolutionary dynamics in microbiomes for host-microbiome interactions.