Microbial autotrophy driven by extracellular electrons generated from mechanical forces via flexoelectricity

Mechanical force has recently emerged as a microbial energy source through direct mechanical-to-electrical energy conversion. However, the flexoelectric effect, a universal mechanoelectrical coupling phenomenon, remains underexplored as an energy source for microbial life. Here, we report a mechanically-driven microbial growth mechanism whereby mechanical energy is converted into electrical energy via the flexoelectric effect of a mineral. This process supports microbial growth in the absence of sunlight and chemical energy sources. Using flexoelectric manganese oxide and electroactive Rhodopseudomonas palustris as a model biohybrid, we demonstrate that mechanical force bends manganese oxide nanosheets to generate free electrical charge. R. palustris captures and utilizes this electrical energy for growth by coupling carbon fixation and denitrification in the absence of chemical electron donors under dark conditions. This pathway is accessible to various electroactive microorganisms and flexoelectric minerals. These findings reveal a noteworthy energy acquisition pathway for microbial survival in energy-limited settings, providing crucial evidence for the diversity of mechanical-to-metabolic coupling in biological processes.