Gram-negative bacteria resist many approved antibiotics because they have an impermeable outer membrane1. The high-priority pathogen Pseudomonas aeruginosa is infamous for acquiring multidrug resistance and is particularly dangerous for individuals with pre-existing immune deficiencies, such as cystic fibrosis2.
In this study, we show that potent protein antibiotics, called L-type pyocins3, exploit a critical vulnerability in the outer membrane by inhibiting the essential β-barrel assembly machinery (BAM) complex4. We obtained three high-resolution cryo-electron microscopy structures of P. aeruginosa apo-BAM and in two distinct complexes with L-type pyocins, revealing an elaborate multi-step mechanism of action. L-type pyocins first interact with a surface-exposed region of BamA and subsequently deploy a C-terminal peptide that competitively binds β-strand 1, blocking the initiation site of outer-membrane β-barrel protein assembly5. This action occurs at the bacterial cell surface, making L-type pyocins intrinsically insensitive to efflux pumps and periplasmic immunity systems.
To chart the cellular consequences of BAM inhibition, we combined genetic and multi-omics profiling. Within minutes of treatment, P. aeruginosa responds by upregulating microbial competition programs, such as the type VI secretion system, and downregulating translation. Longer term responses include drastic changes in the abundance of outer-membrane proteins, consistent with stress from arrested β-barrel assembly. To investigate how intoxicated cells die, we performed cryo-electron tomography with L-type pyocin-treated P. aeruginosa and observed catastrophic outer membrane disruption, which is lethal for Gram-negative bacteria. Functionally, exposure to L-type pyocins renders P. aeruginosa susceptible to the antibiotic vancomycin, demonstrating immediate potential for combination therapy with approved, but normally ineffective drugs.
In summary, we determined the L-type pyocin cytotoxic mechanism and the cellular consequences of BAM inhibition, from atom to cell4. We validate the BAM complex as a high-value therapeutic target for antibiotics that function without cell entry and define an engineerable system for further development of L-type pyocins as next-generation antibiotics against multidrug-resistant P. aeruginosa.