Pierre Dupuy, Yves‐Marie Boudehen, Marion Faucher, John A. Buglino, Allison Fay, Sylvain Cantaloube, Yasmina Grimoire, Julien Marcoux, F. Levet, Laetitia Bettarel, Bertille Voisin, J. Rech, Jean‐Yves Bouet, Olivier Saurel, Jean‐Baptiste Sibarita, Michael S. Glickman, Claude Gutierrez, Olivier Neyrolles
Bacterial pathogens must withstand metal-induced stress during infection, yet the mechanisms by which they sense and respond to toxic metal ions remain incompletely understood. Here, we uncover a previously unrecognized mechanism in Mycobacterium tuberculosis, the causative agent of tuberculosis, which assembles dynamic, membrane-associated platforms organized by PacL proteins to mediate resistance to multiple metals. The small membrane-associated proteins PacL1, PacL2, and PacL3 coordinate the clustering of P-type ATPase pumps, namely CtpC, CtpG, and CtpV, into functional complexes that we term effluxosomes. Using single-particle tracking, we reveal distinct dynamic populations, with highly mobile PacL proteins integrating into more slowly mobile effluxosomes. PacL proteins stabilize CtpC and CtpG within these assemblies, promoting cross-resistance to zinc and cadmium, with PacL1 acting as a multi-substrate metallochaperone that binds zinc, cadmium, and copper via a conserved C-terminal motif. Single-molecule-based super-resolution microscopy shows that conserved residues within the PacL transmembrane domain are essential for effluxosome assembly. Strikingly, proximity labeling reveals a broad PacL1 interaction network, suggesting that effluxosomes contribute to a wider stress adaptation program. These findings establish effluxosomes as dynamic membrane machineries that orchestrate coordinated multi-metal resistance in M. tuberculosis, opening new avenues for antimicrobial targeting.