Outer membrane ‘PusCD’ complexes coordinate phospho(inositol)lipid utilisation in plant Bacteroidota

Gram-negative bacteria belonging to the phylum Bacteroidota are prominent and ecologically important members of host-associated microbiomes. A feature of Bacteroidota species is the presence of diverse outer membrane TonB-dependent transporter and cognate surface-exposed lipoprotein (TBDT-SLP) complexes. Many ’SusCD-like‘ TBDT-SLPs coordinate complex carbohydrate capture from the environment. Here, we show the model soil Bacteroidota species Flavobacterium johnsoniae synthesises two TBDT-SLP complexes (named PusCD1 and PusCD2) that are essential for growth on phosphatidylinositol, a member of an abundant lipid class within plant plasma membranes, as a phosphorus source. Structural characterisation of ligand-bound PusCD1 complex from F. johnsoniae membranes reveals a new binding mechanism for organophosphorus and broadens the known functional repertoire of this class of transporters. Diverse PusCD-like complexes are widespread among plant-associated Bacteroidota, pointing to a major, previously unrecognised route for the recycling of organophosphorus compounds in the rhizosphere, with potential implications for engineering microbial-mediated phosphorus recovery from organic waste streams.