Farnelid, Hanna

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.

Summary The symbiotic unicellular cyanobacterium Candidatus Atelocyanobacterium thalassa (UCYN‐A) is one of the most abundant and widespread nitrogen (N 2 )‐fixing cyanobacteria in the ocean. Although it remains uncultivated, multiple sublineages have been detected based on partial nitrogenase ( nifH ) gene sequences, including the four most commonly detected sublineages UCYN‐A1, UCYN‐A2, UCYN‐A3 and UCYN‐A4. However, very little is known about UCYN‐A3 beyond the nifH sequences from nifH gene diversity surveys. In this study, single cell sorting, DNA sequencing, qPCR and CARD‐FISH assays revealed discrepancies involving the identification of sublineages, which led to new information on the diversity of the UCYN‐A symbiosis. 16S rRNA and nifH gene sequencing on single sorted cells allowed us to identify the 16S rRNA gene of the uncharacterized UCYN‐A3 sublineage. We designed new CARD‐FISH probes that allowed us to distinguish and observe UCYN‐A2 in a coastal location (SIO Pier; San Diego) and UCYN‐A3 in an open ocean location (Station ALOHA; Hawaii). Moreover, we reconstructed about 13% of the UCYN‐A3 genome from Tara Oceans metagenomic data. Finally, our findings unveil the UCYN‐A3 symbiosis in open ocean waters suggesting that the different UCYN‐A sublineages are distributed along different size fractions of the plankton defined by the cell‐size ranges of their prymnesiophyte hosts.

AbstractThe symbiosis between a marine alga and a N2-fixing 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. N2-fìxing cyanobacteria use different strategies to avoid inhibition of N2 fixation by the oxygen evolved in photosynthesis. Most unicellular cyanobacteria temporally separate the two incompatible activities by fixing N2 only at night, but surprisingly UCYN-A appears to fix N2 during the day. The goal of this study was to determine how the unicellular UCYN-A coordinates N2 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 transcription patterns in UCYN-A are most similar to marine cyanobacteria that are capable of aerobic N2 fixation in the light such as Trichodesmium and heterocyst-forming cyanobacteria, rather than 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 the phototrophic eukaryotic host, thus allowing efficient coupling of N2 fixation (by the cyanobacterium) to the energy obtained from photosynthesis (by the eukaryotic unicellular alga) in the light.ImportanceThe symbiotic N2-fixing cyanobacterium UCYN-A and its eukaryotic algal host, which is closely related to Braarudosphaera bigelowii, have been shown to be globally distributed and important in open ocean N2 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 (O2) or the O2 evolved through photosynthesis. This study shows that the symbiosis between the N2-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 N2 fixation, which is likely more energetically efficient than fixing N2 at night, as in other unicellular marine cyanobacteria.