Under light conditions, Mn(II) facilitates the photoautotrophic growth of Georhizobium sp. MAB10, a strain derived from deep-sea ferromanganese nodules, along with the generation of dark Mn oxides (β-MnO2). This study investigated the genetic basis of Mn(II) oxidation-coupled anoxygenic photoautotrophy using genome sequencing and biochemical assays of strain MAB10. Preliminary results indicated the presence of genes encoding a functional pheophytin-quinone-type photosynthetic reaction center and a putative key enzyme for Mn(II) oxidation, namely FtsP/CotA-like multicopper oxidase GE001273. Under light conditions, Mn(II) significantly reduced the respiration rate and elevated the intracellular NADH/NADtotal ratio. This suggested that Mn(II)-derived electrons entered the cyclic photophosphorylation, partially replacing the oxidative phosphorylation for ATP production and enhancing the electron flow to complex I for NADH generation. In vitro enzymatic studies confirmed that GE001273 was a catalyst for Mn(II) oxidation in the outer membrane. Comprehensive genomic analyses of respiration and carbon and nitrogen metabolism revealed the high ecophysiological flexibility of strain MAB10 during Mn(II) oxidation-coupled anoxygenic photoautotrophy in deep-sea habitats. These analyses provided insights into bacterial Mn(II) oxidation-coupled anoxygenic photoautotrophy during microorganism-mediated deep-sea ferromanganese nodule formation.