Thriving across seawater depths: How blue light shapes a large PSI supercomplex and specific photosynthetic traits in the seagrass Posidonia oceanica

Seagrasses are marine flowering plants that perform oxygenic photosynthesis both under high, white sunlight and under low, blue-green light, conditions fundamentally different from those experienced by land plants. Thus far, the adaptation of seagrass photosynthetic machinery to this underwater light gradient remains poorly understood. Here, we investigate the Mediterranean seagrass Posidonia oceanica, an ecosystem engineer thriving from the surface down to 40 m depth, to uncover how it maintains efficient photosynthesis across this gradient. Combining spectroscopy with pigment and blue native-PAGE analysis, we show that P. oceanica maintains a high but stable photosystem I (PSI)/PSII ratio and constant antenna size at all depths, in conjunction with a high abundance of light-harvesting complex II (LHCII). Electron microscopy observation indicated that adjustment of photosynthetic efficiency along the depth gradient is primarily achieved through structural remodeling of thylakoid architecture, rather than major changes in photosystem composition. We also identify a previously undescribed large PSI supercomplex (L-PSI-LHCII) that binds an additional Lhca1-Lhca4 dimer and a phosphorylated LHCII trimer. This complex, expressed at all tested depths, is enriched in chlorophyll b, lacks the far-red-absorbing chlorophylls (red forms) typical of land plants, and exhibits distinct energy-transfer dynamics optimized for blue-light harvesting. The presence of similar PSI supercomplex in other marine seagrasses, such as Zostera marina, suggests a conserved strategy among deep-growing species. Collectively, these results reveal how seagrasses combine structural adaptation at the level of PSI with thylakoid architecture reorganization to sustain efficient photosynthesis and long-term carbon fixation under blue-dominated marine light.