Metabolic trade-offs constrain the cell size ratio in a nitrogen-fixing symbiosis

Abstract

Biological dinitrogen (N₂) fixation is a key metabolic process exclusively performed by prokaryotes, some of which are symbiotic with eukaryotes. Species of the marine haptophyte algae Braarudosphaera bigelowii harbor the N₂-fixing endosymbiotic cyanobacteria UCYN-A, which might be evolving organelle-like characteristics. We found that the size ratio between UCYN-A and their hosts is strikingly conserved across sublineages/species, which is consistent with the size relationships of organelles in this symbiosis and other species. Metabolic modeling showed that this size relationship maximizes the coordinated growth rate based on trade-offs between resource acquisition and exchange. Our findings show that the size relationships of N₂-fixing endosymbionts and organelles in unicellular eukaryotes are constrained by predictable metabolic underpinnings and that UCYN-A is, in many regards, functioning like a hypothetical N₂-fixing organelle (or nitroplast).

Keywords: Braarudosphaera bigelowii; Candidatus Atelocyanobacterium thalassa; UCYN-A; cell size evolution; marine plankton ecology and evolution; metabolic modeling; microbial interactions; nitrogen-fixing symbiosis; nitroplast; organelle evolution.