A redefinition of the cyanobacterial lineage has been proposed based on phylogenomic analysis of distantly related nonphototrophic lineages. We define Cyanobacteria here as “Organisms in the domain bacteria able to carry out oxygenic photosynthesis with water as an electron donor and to reduce carbon dioxide as a source of carbon, or those secondarily evolved from such organisms.”
The symbiotic N
-fixing cyanobacterium UCYN-A, which is closely related to
, and its eukaryotic algal host have been shown to be globally distributed and important in open-ocean N
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
) or the O
evolved through photosynthesis. This study showed that symbiosis between the N
-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
fixation, which is likely more energetically efficient than fixing N
at night, as found in other unicellular marine cyanobacteria.
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.
Fixing on a Marine Partnership
Nitrogen fixation by microorganisms determines the productivity of the biosphere. Although plants photosynthesize by virtue of the ancient incorporation of cyanobacteria to form chloroplasts, no equivalent endosymbiotic event has occurred for nitrogen fixation. Nevertheless, in terrestrial environments, nitrogen-fixing symbioses between bacteria and plants, for example, are common.
) noticed that the ubiquitous marine cyanobacterium UCYN-A has an unusually streamlined genome lacking components of the photosynthetic machinery and central carbon metabolism—all suggestive of being an obligate symbiont. By using gentle filtration methods for raw seawater, a tiny eukaryote partner for UCYN-A of less than 3-µm in diameter was discovered. The bacterium sits on the cell wall of this calcifying picoeukaryote, donating fixed nitrogen and receiving fixed carbon in return.