Photosynthesis emerged at least 3.5 billion years ago as the unique biological process able to convert Solar energy into chemical energy. It first appeared in anoxygenic bacteria and then in oxygen-producing organisms, leading to the evolution of complex life forms with an oxygen-based metabolism (such as humans). Oxygenic photosynthesis produces ATP and NADPH, and the right balance between these energy-rich molecules allows the assimilation of CO2 into organic matter. Although the mechanisms of ATP/NADPH synthesis are well understood, less is known about how CO2 assimilation was optimised. This process was essential for the successful phototrophic colonisation of land (by Plantae) and oceans (by phytoplankton). Plants and phytoplankton are known to adopt different acclimation strategies to ensure high efficiency of photosynthesis under a wide range of environmental conditions. These different strategies are probably the result of the different evolutionary origins of plastids, the specialized organelles where photosynthetic light reactions take place. The emergence of photosynthetic cells by primary or secondary endosymbiosis involved not only the transfer of DNA from the symbiont to the host genome, but also the establishment of metabolic interactions between the symbiont and the host. This was a major challenge, as it involved the integration of a 'solar panel' (the future plastid) into a host cell that already had a 'petrol’ powered engine (the mitochondrion). The presence of the two engines posed a ‘plumbing’ problem for the host: how to connect the two devices. In the primary chloroplasts, present in Plantae, the connection was made at the level of metabolites. Genomic analysis of the first emerging primary endosymbionts suggests that pathogens (Chlamydia-like bacteria) donated genes to the host to facilitate the export of photosynthetic products from the chloroplast to the cytosol, where they are transformed into polysaccharides to fuel mitochondrial respiration. This solution allowed the energy autonomy of both organelles to be maintained. A different solution seems to have been adopted by the secondary endosymbiotic micro-organisms that colonised the oceans (the so-called phytoplankton). In diatoms, ecologically efficient oceanic organisms, the chloroplast is directly connected to the mitochondria, promoting chloroplast-mitochondria exchanges, which optimise the distribution of ATP and NADPH to cellular functions during the day (when both engines are working) and at night (when only the mitochondria are functional).
Is this second mechanism a paradigm for the optimisation of photosynthesis in the ocean? This is the main question ChloroMito is answering addressing the following objectives through a combination of genetics, cell tomography and single-cell spectroscopy approaches:
- What molecular mechanism(s) allow energy exchange between the two organelles?
- Are these mechanisms widely conserved in other oceanic taxa?
- Is this the solution adapted by phytoplankton to optimise their growth?
- Does it modulate the dynamic responses of phytoplankton to different integrated growth environments?
Overall, ChloroMito has changed our understanding of oceanic photosynthesis, challenging concepts that are often deduced from plant-based concepts. This project has also generated new technologies suitable for the study of paradigm questions in photosynthesis beyond ChloroMito itself
