Enterobacter sp. SA187 is a root endophytic bacterium that maintains growth and yield of plants under abiotic stress conditions. In this work, we compared the metabolic wirings of Arabidopsis and SA187 in the free-living and endophytic interaction states. The interaction of SA187 with Arabidopsis induced massive changes in bacterial gene expression for chemotaxis, flagellar biosynthesis, quorum sensing, and biofilm formation. Besides modification of the bacterial carbon and energy metabolism, various nutrient and metabolite transporters and the entire sulfur pathway were up-regulated. Under salt stress, Arabidopsis resembled plants under sulfate starvation but not when colonized by SA187, which reprogramed the sulfur regulon of Arabidopsis. In accordance, salt hypersensitivity of multiple Arabidopsis sulfur metabolism mutants was partially or completely rescued by SA187 as much as by the addition of sulfate, L-cysteine, or L-methionine. Many components of the sulfur metabolism that are localized in the chloroplast were partially rescued by SA187. Finally, salt-induced accumulation of reactive oxygen species as well as the hypersensitivity of LSU mutants were suppressed by SA187. LSUs encode a central regulator linking sulfur metabolism to chloroplast superoxide dismutase activity. The coordinated regulation of the sulfur metabolic pathways in both the beneficial microorganism and the host plant is required for salt stress tolerance in Arabidopsis and might be a common mechanism utilized by different beneficial microbes to mitigate the harmful effects of different abiotic stresses on plants.