Phyllosphere community assembly and response to drought stress on common tropical and temperate forage grasses

Abstract

Grasslands represent a critical ecosystem important for global food production, soil carbon storage, and water regulation. Current intensification and expansion practices add to the degradation of grasslands and dramatically increase greenhouse gas emissions and pollution. Thus, new ways to sustain and improve their productivity are needed. Research efforts focus on the plant-leaf microbiome, or phyllosphere, because its microbial members impact ecosystem function by influencing pathogen resistance, plant hormone production, and nutrient availability through processes including nitrogen fixation. However, little is known about grassland phyllospheres and their response to environmental stress. In this study, globally dominant temperate and tropical forage grass species were grown in a greenhouse under current climate conditions and drought conditions that mimic future climate predictions to understand if (i) plant host taxa influence microbial community assembly, (ii) microbial communities respond to drought stress, and (iii) phyllosphere community changes correlate to changes in plant host traits and stress-response strategies. Community analysis using high resolution sequencing revealed Gammaproteobacteria as the dominant bacterial class, which increased under severe drought stress on both temperate and tropical grasses while overall bacterial community diversity declined. Bacterial community diversity, structure, and response to drought were significantly different between grass species. This community dependence on plant host species correlated with differences in grass species traits, which became more defined under drought stress conditions, suggesting symbiotic evolutionary relationships between plant hosts and their associated microbial community. Further understanding these strategies and the functions microbes provide to plants will help us utilize microbes to promote agricultural and ecosystem productivity in the future. IMPORTANCEGlobally important grassland ecosystems are at risk of degradation due to poor management practices compounded by predicted increases in severity and duration of drought over the next century. Finding new ways to support grassland productivity is critical to maintaining their ecological and agricultural benefits. Discerning how grassland microbial communities change in response to climate stress will help us understand how plant-microbe relationships may be useful to sustainably support grasslands in the future. In this study, phyllosphere community diversity and composition was significantly altered under drought conditions. The significance of our research is demonstrating how severe climate stress reduces bacterial community diversity, which previously was directly associated with decreased plant productivity. These findings guide future questions about functional plant-microbe interactions under stress conditions, greatly enhancing our understanding of how bacteria can increase food security by promoting grassland growth and resilience.