Leaf traits and temperature shape the elevational patterns of phyllosphere microbiome

Aim: The phyllosphere microbiome is central to plant health, distribution, and ecosystem function, yet, we lack a clear understanding of the drivers shaping their diversity in mountain ranges. Here, we examined how the endo- and epiphytic phyllosphere microbiomes of mountains simultaneously respond to climate and leaf functional traits. Location: Temperate forests of Changbai Mountain Natural Reserve, China. Methods: We collected the leaves of dominant tree species along seven elevations from 800 to 1950. We investigated changes in species richness and Shannon diversity of endo- and epiphytic phyllosphere fungal and bacterial communities (using next-generation sequencing of ITS2 and 16S) along an 1150 m elevational gradient. We also examined the direct and indirect effects of climate (mean annual temperature; MAT) and 13 leaf morphological and chemical traits on the microbiome of the phyllosphere. Results: Phyllosphere microbiome declined monotonically with increasing elevation, contrasting with the hump-shaped biodiversity patterns that are commonly reported. We observed a steeper decline in epiphytic bacterial diversity than in endophytic bacteria, whereas conversely endophytic fungi diversity declined more dramatically with increasing elevation than epiphytic fungi. Host plant traits – those involved in resource uptake and leaf surface temperature – predominantly shaped the elevational patterns of endophytic phyllosphere microbiome, whereas MAT mostly increased the richness and Shannon diversity of epiphytic organisms. We also observed weak, but significant indirect effects suggesting that host plant traits are important biotic drivers mediating climate effects on endophytic phyllosphere microbiome. Also, no covariation between bacteria and fungi was observed (neither for endophytic nor for epiphytic organisms), supporting neutral associations between bacterial and fungal communities, irrespective of the elevation. Main Conclusions: Both direct and mediating effects of plant traits should be considered to better understand the drivers shaping the richness and Shannon diversity of endo- and epiphytic phyllosphere microbiomes, and more generally the plant–microbe associations. Our study also offers a trait-based attempt to disentangle the effects of biotic and abiotic filters in shaping endo- and epiphytic phyllosphere microbiome along an elevational gradient.