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. Importance: Microorganisms are believed to participate in the biotic process of deep-sea ferromanganese nodule formation [Mn(II) oxidation]. Despite the multitude of studies and reviews focusing on the details of Mn(II) oxidation catalyzed by diverse heterotrophs, the mechanistic roles of manganese chemolithotrophs from ferromanganese nodules remain unclear. We demonstrate that strain Georhizobium sp. MAB10 can utilize Mn(II)-derived electrons for photoautotrophic growth, with concomitant generation of dark β-MnO2 type Mn oxides under near-infrared light condition. This study uses genomic and biochemical assays to explore the genetic basis of Mn(II) oxidation-coupled anoxygenic photoautotrophy. The comprehensive analyses of respiration and carbon and nitrogen metabolism further elucidated the high ecophysiological flexibility of strain MAB10 in deep-sea habits. These findings expand our understanding of the role of chemolithotrophs in deep-sea ferromanganese nodule formation and justify further investigations into the molecular basis for Mn(II) oxidation-coupled anoxygenic photoautotrophy.