Increasing drought events coupled with dwindling water reserves threaten global food production and security. This issue is exacerbated by the use of crops that overconsume water, undermining yield. We show here that microorganisms naturally associated with plant roots can undermine efficient water use, whereas modified bacteria can enhance it. We demonstrate that microbe-encoded genes shape drought tolerance, likely by modulating plant hormonal balance. Specifically, we built a minimal holobiont out of Arabidopsis thaliana and either the bacterium Pseudomonas putida UW4 or its isogenic AcdS mutant, lacking the enzyme ACC deaminase. This enzyme breaks down the precursor of ethylene, a key regulator in plant response to drought. This single mutation profoundly affected plant physiology and shifted the plant from a 'water-spender' (with more growth under well-watered conditions) to a 'water-spender' phenotype. Under drought, plants associated with wild-type bacteria consumed soil water faster, leading to a shorter period of growth followed by death. In contrast, plants associated with the AcdS mutant managed to maintain growth by reducing water consumption via stomatal closure, thus conserving soil water. This allowed plants to survive severe water deficiency. We conclude that plant-associated bacteria can modulate plant water use strategies, opening possibilities to engineer water-savvy crop-production systems.