Insights into the role of light and of the haptophyte host in gene expression and activity of the symbiotic, diazotrophic cyanobacterium UCYN-A.

The uncultivated unicellular cyanobacterium UCYN-A is widespread in the world ocean where it contributes significantly to nitrogen (N₂) fixation. This organism lives in symbiosis with a haptophyte, which provides fixed carbon in exchange for fixed nitrogen from UCYN-A. The UCYN-A genome is small and lacks many genes involved in biologically important pathways, including 2 of the 3 kai genes responsible for the maintenance of circadian rhythm in cyanobacteria. In spite of this, diel patterns in gene expression have been observed in UCYN-A, which suggests persisting controls of the timing of specific cell functions, possibly driven by the eukaryotic host for efficient coordination of cellular metabolism and growth. The mechanisms of interaction and metabolic regulation between UCYN-A and its haptophyte host are still virtually unknown. To investigate the role of light and of the host in UCYN-A’s activity, we incubated natural microbial populations sampled off the Californian coast (San Diego) under various light-dark conditions and used nanoscale secondary ion mass spectrometry to measure single cell N₂ fixation rates. Together with targeted nifH transcript quantification by digital droplet PCR, we found that N₂ fixation activity in UCYN-A cells persisted while maintained in the dark for a full day-night cycle, although at lower rates than cells maintained under a regular light-dark cycle. N₂ fixation rates were comparable between control cells and cells returned to normal light-dark cycle conditions after spending 24 hours in the dark. Our results suggest the existence of an internal clock controlling UCYN-A activity and that light and/or freshly fixed carbon from the host are necessary to fuel N₂ fixation. These findings, together with whole genome expression analyses, will help uncover mechanisms of coordinated metabolism, growth and cell division between UCYN-A and the host.