A bacterium isolated from soil as an alginate lyase producer shows characteristic morphological and taxonomical properties consistent with being classified in the genus Sphingomonas. The bacterium utilizes high molecular weight (HMW)-alginate for growth by depolymerization of the polymer with intracellular alginate lyases, which are generated from a common precursor protein through autoregulated post-translational modifications. Electron microscopic observations of the cell surface and of thin sections of cells grown on HMW-alginate revealed dynamic changes in both cell surface and membrane structures. The most remarkable change is recognized in the formation of mouth-like pits which open and close depending on the presence or absence of HMW-alginate. Enzymatic and genetic analyses of HMW-alginate incorporation processes confirmed the presence of a pit-dependent and macromolecule-specific ABC transporter system in cells of Sphingomonas species A1. This is the first description of a bacterium with a pit on the cell surface and a pit-dependent endocytosic uptake system for macromolecules.