Electroactive membrane exchange facilitates photosynthetic electron harvesting in biophotovoltaics

Biophotovoltaics (BPV) offers a sustainable solution for solar energy conversion by harnessing the capability of photosynthetic microorganisms. However, inefficient extraction of photosynthetic electrons across the non-conductive cell membrane of cyanobacteria severely hampers BPV performance. Here, we report an electroactive membrane exchange strategy to implant functional electron transfer components from Shewanella into cyanobacteria to create a conductive outer membrane. By genetically removing the surface layer of Synechocystis sp. PCC 6803, we enabled membrane exchange with Shewanella -derived outer membrane vesicles (OMVs) bearing multi-heme cytochromes. Fluorescent and lipidomic characterizations confirm the stable integration of these OMVs-borne cytochromes into the outer membrane of cyanobacteria. The resulting conductive outer membrane achieves a ten-fold increase in photocurrent generation of cyanobacteria. Inhibitor studies verify that the harvested electrons originate from photosynthetic water-splitting, while control experiments with artificial liposomes and heat-inactivated OMVs demonstrate that both membrane exchange and cytochrome functionality are essential. Remarkably, the OMVs-integrated cyanobacteria exhibit enhanced tolerance to oxidative stress by reducing reactive oxygen species and increasing efflux of toxic metabolites. This OMVs-mediated functionalization provides a versatile, genetic-modification-free platform for endowing non-exoelectrogenic microorganisms with enhanced interfacial electron transfer, with potential applications for bioenergy, biosensing and biotechnology. • A OMVs-induced membrane exchange technology is developed in cyanobacteria. • Membrane exchange enables cytochromes-based electron conduit implanted into outer membrane. • Conductive outer membrane achieves a ten-fold increase in photocurrent generation. • This increase is specifically attributed to membrane anchoring of heterogenous cytochromes. • OMVs-integrated cyanobacteria exhibit enhanced tolerance to oxidative stress.