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

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