The reactive species of oxygen (ROS) and chlorine (RCS) damage cellular components, potentially leading to cell death. In proteins, the sulfur-containing amino acid methionine (Met) is converted to methionine sulfoxide (Met-O), which can cause a loss of biological activity. Here, we report the identification of an enzymatic system repairing proteins with oxidatively-damaged Met residues in the bacterial cell envelope, a compartment particularly exposed to the ROS and RCS generated by the host defense mechanisms. This system is made of the molybdenum-containing enzyme MsrP and the heme-binding membrane protein MsrQ. Both proteins, whose synthesis is induced by hypochlorous acid (HOCl), a powerful antimicrobial released by neutrophils, are widely conserved throughout Gram-negative bacteria, including major human pathogens. MsrPQ is essential for extracytosolic protein quality control and the maintenance of envelope integrity under bleach stress, rescuing Met residues from oxidation in a wide series of structurally unrelated periplasmic proteins. For this activity, MsrPQ uses electrons from the respiratory chain, which represents a novel mechanism to import reducing equivalents into the bacterial cell envelope. A remarkable feature of MsrPQ is its capacity to reduce both R- and S- diastereoisomers of Met-O, making this oxidoreductase complex functionally different from conventional methionine sulfoxide reductases (Msr). The surprising observation that the bacterial periplasm contains a single enzymatic complex able to fully protect Met residues from oxidative damage suggests that potentially similar systems exist in the endoplasmic reticulum (ER) and other subcellular oxidizing compartments