Plewka-Mandelkow, J. F.; Thomas, A. S.; Vorholt, J. A.; Kraemer, U.

Diversity and composition of plant-associated microbiota are attributed to host and microbial genotype as well as the environment, yet our understanding of the causal factors driving these patterns remains incomplete. Elevated concentrations of the micronutrients zinc (Zn), manganese (Mn) and copper (Cu), and exposure to non-essential trace elements including cadmium (Cd) and arsenic (As), can be toxic. Here we explored whether differences in metal(loid) homeostasis between plants and bacteria shape microbial community composition in the phyllosphere. Among the biologically relevant metal(loid)s Cd, Cu, Mn, Zn, and As, we identified CdII as the most toxic, and AsV (arsenate) as the most harmless, by screening 224 representative Arabidopsis thaliana phyllosphere bacterial strains on metal(loid) concentration series in synthetic media. Comparing bacteriotoxicity profiles with our measurements of the leaf apoplastic fluid ionome indicated that Zn2+ and Cd2+ concentrations are the most likely to arrest growth of metal-sensitive strains in planta. Soil bacterial strains were several-fold more sensitive to both these metals than leaf strains, consistent with selection for increased bacterial Zn and Cd tolerance in the phyllosphere. Keystone strains, known to govern bacterial community structure, were highly metal-sensitive, with only few between-metal interactions and no between-strain interactions modulating single-metal(loid) toxicities. Overall, bacterial genus explained 63% of the variance in metal(loid)-related gene content and 42% of the metal(loid) tolerance phenotypic variance. Cd tolerance correlated with the presence and copy number of known Cd-related genes. In summary, our results support the hypothesis that plant metal homeostasis contributes to structuring bacterial communities in the leaf endosphere.