Metabolic tradeoffs constrain the cell size ratio in a nitrogen-fixing organelle-like symbiosis

Abstract

Biological nitrogen fixation is a key metabolic process exclusively performed by prokaryotes, some of which are in symbiosis with eukaryotes. Symbiotic interactions led to the evolution of organelles for photosynthesis and respiration but a true nitrogen-fixing organelle has never been reported. We found that the size ratio between the marine symbiotic nitrogen-fixing cyanobacteria UCYN-A and their algal hosts is strikingly conserved across different lineages, and consistent with size relationships of organelles in this symbiosis and other species. Metabolic modeling showed that this size relationship maximizes the coordinated growth rate based on tradeoffs between nutrient acquisition and exchange. This study suggests that size relationships of endosymbionts and organelles in unicellular organisms are constrained by predictable metabolic underpinnings, and that UCYN-A is functioning as a nitrogen-fixing organelle, or ‘nitroplast’. Keywords: Microbial symbiosis, nitrogen fixation, organellogenesis, UCYN-A