Solar-converting nanosystems using self-renewing biomaterial resources carry great potential for developing sustainable technologies to ameliorate climate change and minimize reliance on fossil fuels. By mimicking natural photosynthesis, diverse proof-of-concept biosolar systems have been used to produce green electricity, fuels and chemicals. Efforts so far have focused on optimizing light harvesting, biocatalyst loading and electron transfer (ET), however, the long-term performance of best-performing systems remains a major challenge due to the intensive use of diffusive, toxic mediators. To overcome this limitation, we developed a rationally designed nanosystem based on the entrapment of non-toxic mediator, ferrocene dimethanol (Fc), localized at the abiotic-biotic molecular interface that efficiently promoted ET between electrode surface and two photosynthetic proteins: cytochrome c and photosystem I. We demonstrate that space-confined Fc mediators (1 nM) are as effective in terms of ET kinetics as a 500 000-fold higher concentration of freely-diffusive Fc. The Fc-confined biophotocathodes showed a milestone photocurrent density of 14 μA cm-2 under oxic conditions compared to analogous planar (2D) biophotoelectrodes, with a photoconductive biolayer stable for over 5 months. The space-confined ET mediation reported in this work opens a new avenue for efficiently interfacing biomachineries, providing a benchmark design advancement in the quest for viable biohybrid technologies.