Organ-specific filtering by abiotic and biotic environmental factors shapes distinct yet overlapping microbial communities across Lotus corniculatus roots, shoots, flowers, and seeds

Plant microbiome assembly is modulated via filtering by the host plant and local environment as well as stochastic processes like microbial dispersal. Lotus corniculatus in natural populations that are continuously exposed to natural perturbations and microbial sources is an ideal plant model system to study the ecological processes that structure the distinct yet overlapping microbial communities in plant organs. We observed spatial and temporal variation in microbiomes associated with L. corniculatus roots, shoots, flowers, and seeds across seven grassland sites for four years. In this study we examined how abiotic and biotic factors in the local environment throughout multiple years contribute to the structure of microbiomes associated with L. corniculatus populations. We show that plant microbiomes are shaped by a set of environmental factors that are distinct to each plant compartment. These environmental factors either directly influence the plant microbiomes or by indirectly affecting them via other biotic factors. The environmental factors soil temperature seasonality, soil microbiome composition, air temperature seasonality, plant community richness, and grazing are found to influence the structure and microbial interactions in the plant organs, and are different in relationships with microbiomes with each compartment, possibly influencing dispersal decisions of microorganisms and consequently contribute in shaping distinct yet overlapping microbiomes across plant organs. Burkholderia and Sulfuritalea, plant-associated microbes that are highly correlated with environmental variables across all plant organs, respond to environmental variables differently depending on their organ microhabitat. This organ-dependent environmental perception is also observed in biomarker microbes in roots, shoots, and flowers, such as the rhizobial symbiont Mesorhizobium, leaf pathogen Setosphaeria, and necrotroph Botryotinia, respectively. Our knowledge about the organ-specific response of plant microbiomes to abiotic and biotic perturbations will equip us with a framework to understand and engineer plant microbiomes in the context of global climate change. The observed patterns on dispersal decisions or habitat choice based on organ-dependent environmental cues and microbial interactions in plant microbiomes also advance our insights on how beneficial microbes or pathogens survive and persist on specific plant microhabitat and environmental conditions.