According to the proton-electrostatics localization hypothesis presented in this work, protons injected into a thylakoid may be electrostatically localized at the water-membrane interface along the lumenal surface. This hypothesis provides a natural frame work to explain a wide range of experimental observations in the bioenergetics of chloroplast and other biological systems conducted since the 1960s, including the longstanding well-characterized energetic problems of alkalophilic bacteria such as Bacillus firmus. It can also help reconcile the elegant scientific observations of both the Dilley experiment and the Junge neutral-red thylakoid proton detection. Our analysis indicates that the Mitchellian view of delocalized proton coupling to ATP synthase could only be true under special circumstances; namely, when the membrane electrical potential difference is near zero and the bulk phase-to-bulk phase pH difference becomes the dominant factor. The proton coupling under most physiological conditions of photosynthesis is likely to occur in a mixed state of proton electrostatic localization of excess charge at the membrane surface and delocalization in the bulk media. The proton-electrostatics localization hypothesis leads to a new bioenergetics equation for the proton motive force which may provide a unified framework for understanding the energetics of many biological systems.