Diazotrophy under continuous light in a marine unicellular diazotrophic cyanobacterium, Gloeothece sp. 68DGA

Abstract

Nitrogenase is extremely sensitive to molecular oxygen (O 2 ), and unicellular diazotrophic cyanobacteria separate nitrogen (N 2 )-fixation and photosynthesis to protect nitrogenase from O 2 produced by photosynthesis. When grown under 12 h light/12 h dark cycles (LD), the marine unicellular diazotrophic cyanobacterium Gloeothece sp. 68DGA expressed the nitrogenase protein and its activity (acetylene reduction activity) only during the dark phase. However, this strain was able to grow diazotrophically under continuous light (CL). To determine whether nitrogenase synthesis and N 2 -fixation are temporally separated from photosynthesis in the Gloeothece cells that have fully acclimated to CL, the proportion of cells containing nitrogenase (the Fe-protein of nitrogenase) in the culture was measured using an immunocytochemical technique. Cells were grown in a continuous-culture device to maintain constant cell density. Under LD, the cells showed diurnal oscillation of nitrogenase activity, photosynthesis, respiration and the expression and the abundance of the Fe-protein. The oscillation was gradually reduced after the transfer of the cells to CL, and was lost after 23-25 days of cultivation under CL. In CL-acclimated cultures, the Fe-protein was always detected in about 94 % of the cells, although the nitrogenase activity was about one-third of the maximum activity in LD-acclimated cultures. These results suggest that synthesis of nitrogenase proceeds without diurnal oscillation in the CL-acclimated cells of Gloeothece sp. 68DGA. As the respiration rate in CL-acclimated culture was as high as the maximum rate observed in LD-acclimated culture, O 2 -uptake mechanism(s) may have been upregulated to maintain low intracellular pO 2 .

Resolution of Conflicting Signals at the Single-Cell Level in the Regulation of Cyanobacterial Photosynthesis and Nitrogen Fixation

“…The development of specialized cells in filamentous cyanobacteria provides a spatial separation, with N 2 fixation occurring in the thick-walled heterocysts that lack the oxygenic photosystem (PS) II. Unicellular cyanobacteria separate N 2 fixation and photosynthesis temporally, with the former occurring during the dark and the latter in the light [3]–[6]. This segregation of N 2 fixation and photosynthetic activity is regulated by a circadian clock [4], [7]–[9].…”

“…However, both studies did not directly measure N 2 fixation and photosynthesis at the single-cell level leaving the question whether individual cells actually do perform both processes. There is evidence that some populations have the capacity to adjust their cellular metabolism in order to fix N 2 and CO 2 simultaneously after acclimation to continuous light [6]. So far, this observation appears to be restricted to the unicellular diazotrophic cyanobacteria Gloeothece sp.…”

“…So far, this observation appears to be restricted to the unicellular diazotrophic cyanobacteria Gloeothece sp. [6], [14] and Synechococcus sp. RF-1 [15].…”

Variations in the Rhythms of Respiration and Nitrogen Fixation in Members of the Unicellular Diazotrophic Cyanobacterial Genus Cyanothece

“…For instance, members of the genus Gloeothece fix nitrogen aerobically during the day, but at 0% dissolved oxygen concentration, nitrogen fixation is shifted entirely to the dark period (Ortega-Calvo and Stal, 1991;Taniuchi et al, 2008). In contrast, some Synechococcus spp.…”

Transcriptional regulators ChlR and CnfR are essential for diazotrophic growth in nonheterocystous cyanobacteria

“…by other factors such as fixed nitrogen amounts and environmental O 2 levels (11). Trichodesmium species are a group of major nitrogen fixers in the ocean.…”