Phyllosphere fungal diversity generates pervasive non-additive effects on plant performance

Abstract

All plants naturally harbor diverse microbiomes that can dramatically impact their health and productivity. However, it remains unclear how microbiome diversity, especially in the phyllosphere, impacts intermicrobial interactions and consequent non-additive effects on plant productivity. Combining manipulative experiments, field collections, culturing, microbiome sequencing, and synthetic consortia, we experimentally tested for the first time how foliar fungal community diversity impacts plant productivity. We inoculated morning glories with 32 synthetic phyllosphere communities of either low or high diversity or with single fungal taxa, and measured effects on plant productivity and allocation. We found 1) non-additive effects were pervasive with 56% of microbial communities interacting synergistically or antagonistically to impact plant productivity, including some consortia capable of generating acute synergism (e.g., >1000% increase in productivity above the additive expectation), 2) interactions among commensal fungi were responsible for this non-additivity in diverse communities, 3) synergistic interactions were ~4 times stronger than antagonistic effects, 4) fungal diversity affected the magnitude but not frequency or direction of non-additivity, and 5) diversity affected plant performance nonlinearly with highest performance in low microbial diversity treatments. These findings highlight the importance of interpreting plant-microbial interactions under a framework that incorporates intermicrobial interactions and non-additive outcomes to understand natural complexity.