Microbial communities living inside plant leaves or on the leaf surface are differently shaped by environmental cues

Abstract

Leaf-associated microbial communities can promote plant health and resistance to biotic and abiotic stresses. However, the importance of environmental cues in the assembly of the leaf endo- and epi-microbiota remains elusive. Here we aimed to investigate the impact of seasonal environmental variations, on the establishment of the leaf microbiome, focusing on long-term changes (five years) in bacterial, fungal, and non-fungal eukaryotic communities colonizing the surface and endosphere of six wild Arabidopsis thaliana populations. While leaf-microbial communities were found to be highly stochastic, the leaf niche had a predominant importance with endophytic microbial communities consistently exhibiting a lower diversity and variability. Furthermore, our analyses revealed that among environmental factors, radiation and humidity-related factors are the most important drivers of diversity paderns in the leaf, albeit with stronger effects on epiphytic communities. Using linear models, we further identified 30 important genera whose relative abundance in leaf compartments could be modeled from environmental variables, suggesting specific niche preferences for these taxa. With the hypothesis that these environmental factors could impact interactions within microbial communities, we analyzed the seasonal paderns of microbial interaction networks across leaf compartments. We showed that epiphytic networks are more complex than endophytic, and that the complexity and connectivity of these networks are partially correlated with the mentioned environmental cues. Our results indicate that humidity and solar radiation function as major environmental cues shaping the phyllosphere microbiome at the micro-scale (leaf compartment) and macro-scale (site). These findings could have practical implications for selecting and developing field-adapted microbes in the face of, and for predicting microbial invasions in response to global change.