Accumulation of ambient phosphate into the periplasm of marine bacteria is proton motive force dependent

Bacteria acquire phosphate (Pi) by maintaining a periplasmic concentration below environmental levels. We recently described an extracellular Pi buffer which appears to counteract the gradient required for Pi diffusion. Here, we demonstrate that various treatments to outer membrane (OM) constituents do not affect the buffered Pi because bacteria accumulate Pi in the periplasm, from which it can be removed hypo-osmotically. The periplasmic Pi can be gradually imported into the cytoplasm by ATP-powered transport, however, the proton motive force (PMF) is not required to keep Pi in the periplasm. In contrast, the accumulation of Pi into the periplasm across the OM is PMF-dependent and can be enhanced by light energy. Because the conventional mechanism of Pi-specific transport cannot explain Pi accumulation in the periplasm we propose that periplasmic Pi anions pair with chemiosmotic cations of the PMF and millions of accumulated Pi pairs could influence the periplasmic osmolarity of marine bacteria. The ubiquitous oceanic bacteria harbour an external phosphate buffer for modulating phosphate (Pi) uptake. Here, using both oceanic SAR11, Prochlorococcus and Synechococcus strains as a model, the authors show that the Pi buffer accumulation in the periplasm is proton motive force-dependent and can be enhanced by light energy.