Iron as a principal mediator of dysbiosis prevention in the phyllosphere

Abstract

Multicellular organisms require a correct microbiota composition for optimal health and fitness. Dysbiosis could lead to serious health consequences in humans and plants, and is pervasive during pathogen infections across systems. A recent study shows that carbon source availability plays a role in bacterial community assembly in Arabidopsis leaves [1]. However, whether carbon sources or other molecules are critical for leaf microbiota homeostasis remains unknown. Here, an unbiased in planta metatranscriptomic analysis of endophytic microbiota in leaves of wild-type and dysbiotic min7 fls2 efr cerk1 (mfec) mutant, which is defective in pattern-recognition receptor (PRR) signaling and MIN7-dependent vesicle trafficking, revealed that bacteria inside Arabidopsis leaves exhibit taxa-specific transcriptional responses. Most notably, iron starvation response was detected in Stenotrophomonas strains, a group of endophytic bacteria that cause dysbiotic symptoms. Elevated expression of canonical iron starvation genes confirmed low iron availability in mfec plants. This low iron environment was associated with a reduced level of the plasma membrane H-ATPase AHA2, resulting in a higher apoplastic pH that favors less-bioavailable ferric iron over soluble ferrous iron. Supplementing iron in mfec plants was sufficient to restore microbiota homeostasis and alleviate dysbiosis phenotypes. The role of iron in dysbiosis extends to Pseudomonas syringae foliar infection, which drives leaf dysbiosis through two iron-dependent mechanisms. Iron thus emerges as a surprising, key switch between healthy and dysbiotic microbiota in the endophytic spaces of plants.