Coupling of excitation energy to photochemistry in natural marine phytoplankton communities under iron stress

Abstract

Oxygenic photosynthesis requires excitation energy transfer from light-harvesting complexes (LHCs) to reaction centers (RCs) to drive photochemical redox chemistry. The effective absorption cross section of RCs dynamically responds to the light environment on time scales of seconds to days, allowing rapid acclimations to changes in spectral irradiance and photoprotection under high light, thereby optimizing light absorption for photochemistry. Although energy coupling between LHC–RCs has been studied for decades in laboratory cultures, it remains poorly understood in real-world conditions, where it is potentially influenced by nutrients. In the oceans, one of the most critical micronutrients for photosynthesis is iron (Fe). To investigate the effects of Fe stress on the energetic coupling between LHC–RCs in natural phytoplankton assemblages in the Southern Atlantic Ocean, we assessed photophysiological responses using a pair of custom-built fluorometers measuring chlorophyll-a variable fluorescence and picosecond fluorescence lifetimes. Detailed analysis based on the functional absorption cross section of the oxygen-evolving complex, quantum yield of photochemistry, energetic connectivity of RCs, and the average lifetime of in vivo chlorophyll fluorescence suggested that between 10 and 25% of LHCs remain uncoupled from RCs and do not effectively contribute to photochemical charge separation. Addition of Fe to samples under trace metal-clean on-board incubations indicates relatively rapid recoupling (< 24 h) of antennae to photochemistry, followed by biophysical stabilization of recoupled complexes. Our findings highlight the crucial role of micronutrients in controlling the excitation energy transfer from LHCs to RCs in marine phytoplankton and the overall primary productivity in the real-world oceans.