Deep-sea hydrothermal vents emit intense infrared (IR) radiation that profoundly shapes microbial ecology and promotes bacterial growth. To investigate the mechanisms underlying IR responsiveness, we isolated Rhodotorula mucilaginosa strain F-J1, a deep-sea yeast. We found that both elevated temperature and near-infrared (NIR, 810–1050 nm) irradiation stimulated F-J1 growth. Whereas dark-grown cultures were highly temperature-sensitive, NIR irradiation—particularly at 880 nm—not only enhanced growth but also substantially lowered the Arrhenius activation energy, indicating a wavelength-dependent, temperature-insensitive stimulation mechanism. At the atomic level, substituting hydrogen with deuterium (via heavy water) suppressed F-J1 growth. This inhibition was partially alleviated by wavelength-dependent NIR irradiation, implicating water’s overtone vibrations. However, deuterium completely abolished the stimulatory effect of 880 nm NIR, revealing a distinct, wavelength-specific mechanism. Inhibition of mitochondrial ribosome function and oxidative phosphorylation impaired NIR-stimulated growth, underscoring the critical role of mitochondrial metabolism. Electron microscopy further showed NIR-induced mitochondrial morphological changes consistent with heightened metabolic activity. Proteomic analysis identified upregulation of mitochondrial ribosomal protein S18, suggesting enhanced mitochondrial protein biosynthesis under optimal NIR conditions. Together, these findings uncover a mitochondria-centered, non-thermal IR-sensing mechanism that parallels known photobiomodulation processes in mammalian cells. This work provides new insights into the ecological role of IR radiation in deep-sea hydrothermal ecosystems and highlights its potential biomedical and biotechnological applications.