Symbiosis has been key to evolution on Earth. The success of eukaryotes was possible due to the establishment of endosymbiotic relationships between unicellular microorganisms that gave rise to specialized organelles (chloroplasts and mitochondria), yet the mechanisms underpinning such biological innovations are still unresolved. An unusual marine nitrogen-fixing symbiosis involving a cyanobacterium called UCYN-A and a single-celled haptophyte algae (Braarudosphaera bigelowii) was recently found to have undergone genome rearrangements analogous to organelle evolution. Since no eukaryotes fix nitrogen (N2), an essential nutrient for life, knowledge on this peculiar symbiosis may serve as a unique opportunity for understanding the acquisition of new organelle-derived functions in eukaryotes. The UCYNELLE project is designed to provide new insights on organelle evolution through the multidisciplinary study of the UCYN-A symbiosis from an ecological, evolutionary and metabolic perspective: First, experimental manipulations with the UCYN-A culture and field surveys will be conducted to identify the molecular basis regulating the metabolic coupling between symbiotic partners and the associated microbiome. Second, the organelle genomes of the haptophyte host will be compared to those of the different UCYN-A lineages via comparative genomics to explore any parallelisms in their mode of evolution. Finally, the natural variation in cell size shown by UCYN-A and its host across different UCYN-A symbioses will allow investigating the metabolic scaling (metabolic rates vs cell size) of the N2 fixation process compared to that of typical organelle-driven metabolisms (photosynthesis and respiration) through the study of the volumetric relationships between chloroplasts, mitochondria, UCYN-A and its host. Elucidating the mechanism underlying the UCYN-A symbiosis will help to understand the early evolutionary steps leading to the acquisition of plastids in eukaryotes.
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