The TerC family metal chaperone MeeY enables surfactin export in <i>Bacillus subtilis</i>

TerC family proteins are widely conserved integral membrane proteins with functions related to metal transport. In <i>Bacillus subtilis</i>, the TerC proteins MeeF and MeeY play overlapping roles in the metalation of manganese-requiring membrane and extracellular enzymes. TerC proteins interact with the secretion translocon SecYEG and metalate proteins either during or after protein translocation. Here, we demonstrate that swarming motility is dependent on MeeY. This swarming defect can be complemented extracellularly and is correlated with a loss of surfactin. Surfactin export is mediated by SwrC, an RND family efflux pump previously shown to interact with MeeY in co-immunoprecipitation studies. The amendment of the growth medium with manganese has long been known to enhance surfactin production. We suggest a model in which surfactin export is enhanced by the MeeY-dependent metalation of the surfactin lipopeptide during export.IMPORTANCE<i>Bacillus subtilis</i> produces surfactin, a powerful detergent-like compound that functions in intercellular communication, surface motility, and as a broad-spectrum antimicrobial agent. Production of surfactin, a cyclic lipopeptide, depends on a non-ribosomal peptide synthase followed by export by SwrC, a member of the resistance-nodulation-cell division (RND) family of export proteins. Here, we demonstrate that surfactin production additionally requires MeeY, a TerC family membrane protein that exports manganese ions to support the function of secreted and membrane metalloenzymes. We propose that MeeY interacts with SwrC to facilitate metal binding to the surfactin lipopeptide during export from the cell. These results may explain the long-appreciated role that divalent metal ions play in surfactin production during industrial fermentation.