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Lipid acquisition and transport are fundamental processes in all organisms, but many of the key players remain unidentified. Here, we elucidate the lipid-cycling mechanism of the Mycoplasma pneumoniae membrane protein P116. We show that P116 not only extracts lipids from its environment but also self-sufficiently deposits them into both bacterial and eukaryotic cell membranes as well as liposomes. Our structures and molecular dynamics simulation show that the N-terminal region of P116, which resembles an SMP domain, is responsible for perturbing the membrane, while a hydrophobic pocket exploits the chemical gradient to collect the lipids and the protein’s dorsal side acts as a mediator of membrane directionality. Furthermore, ligand binding and growth curve assays suggest the potential for designing small molecule inhibitors targeting this essential and immunodominant protein. We show that P116 is a versatile lipid acquisition and delivery machinery that shortcuts the multi-protein pathways used by more complex organisms. Thus, our work advances the understanding of common lipid transport strategies, which may aid research into the mechanisms of more complex lipid-handling machineries.