The Transcriptional Cycle Is Suited to Daytime N2 Fixation in the Unicellular Cyanobacterium "Candidatus Atelocyanobacterium thalassa" (UCYN-A)

Symbiosis between a marine alga and a N-2-fixing cyanobacterium (Cyanobacterium UCYN-A) is geographically widespread in the oceans and is important in the marine N cycle. UCYN-A is uncultivated and is an unusual unicellular cyanobacterium because it lacks many metabolic functions, including oxygenic photosynthesis and carbon fixation, which are typical in cyanobacteria. It is now presumed to be an obligate symbiont of haptophytes closely related to Braarudosphaera bigelowii. N-2-fixing cyanobacteria use different strategies to avoid inhibition of N-2 fixation by the oxygen evolved in photosynthesis. Most unicellular cyanobacteria temporally separate the two incompatible activities by fixing N-2 only at night, but, surprisingly, UCYN-A appears to fix N-2 during the day. The goal of this study was to determine how the unicellular UCYN-A strain coordinates N-2 fixation and general metabolism compared to other marine cyanobacteria. We found that UCYN-A has distinct daily cycles of many genes despite the fact that it lacks two of the three circadian clock genes found in most cyanobacteria. We also found that the transcription patterns in UCYN-A are more similar to those in marine cyanobacteria that are capable of aerobic N-2 fixation in the light, such as Trichodesmium and heterocyst-forming cyanobacteria, than to those in Crocosphaera or Cyanothece species, which are more closely related to unicellular marine cyanobacteria evolutionarily. Our findings suggest that the symbiotic interaction has resulted in a shift of transcriptional regulation to coordinate UCYN-A metabolism with that of the phototrophic eukaryotic host, thus allowing efficient coupling of N-2 fixation (by the cyanobacterium) to the energy obtained from photosynthesis (by the eukaryotic unicellular alga) in the light. IMPORTANCE The symbiotic N-2-fixing cyanobacterium UCYN-A, which is closely related to Braarudosphaera bigelowii, and its eukaryotic algal host have been shown to be globally distributed and important in open-ocean N-2 fixation. These unique cyanobacteria have reduced metabolic capabilities, even lacking genes for oxygenic photosynthesis and carbon fixation. Cyanobacteria generally use energy from photosynthesis for nitrogen fixation but require mechanisms for avoiding inactivation of the oxygen-sensitive nitrogenase enzyme by ambient oxygen (O-2) or the O-2 evolved through photosynthesis. This study showed that symbiosis between the N-2-fixing cyanobacterium UCYN-A and its eukaryotic algal host has led to adaptation of its daily gene expression pattern in order to enable daytime aerobic N-2 fixation, which is likely more energetically efficient than fixing N-2 at night, as found in other unicellular marine cyanobacteria.