Ultradian metabolic rhythm in the diazotrophic cyanobacterium Cyanothece sp. ATCC 51142

Abstract

The unicellular cyanobacterium Cyanothece sp. American Type Culture Collection (ATCC) 51142 is capable of performing oxygenic photosynthesis during the day and microoxic nitrogen fixation at night. These mutually exclusive processes are possible only by temporal separation by circadian clock or another cellular program. We report identification of a temperature-dependent ultradian metabolic rhythm that controls the alternating oxygenic and microoxic processes of Cyanothece sp. ATCC 51142 under continuous high irradiance and in high CO 2 concentration. During the oxygenic photosynthesis phase, nitrate deficiency limited protein synthesis and CO 2 assimilation was directed toward glycogen synthesis. The carbohydrate accumulation reduced overexcitation of the photosynthetic reactions until a respiration burst initiated a transition to microoxic N 2 fixation. In contrast to the circadian clock, this ultradian period is strongly temperature-dependent: 17 h at 27°C, which continuously decreased to 10 h at 39°C. The cycle was expressed by an oscillatory modulation of net O 2 evolution, CO 2 uptake, pH, fluorescence emission, glycogen content, cell division, and culture optical density. The corresponding ultradian modulation was also observed in the transcription of nitrogenaserelated nifB and nifH genes and in nitrogenase activities. We propose that the control by the newly identified metabolic cycle adds another rhythmic component to the circadian clock that reflects the true metabolic state depending on the actual temperature, irradiance, and CO 2 availability.

Cellular trade-offs and optimal resource allocation during cyanobacterial diurnal growth

“…We envision a stoichiometric whole-cell model, with a focus on energetic constraints, that allows us to assess the optimality of metabolic strategies in diverse environments. Of particular interest are the energetic implications of carbon cycling (43), light damage and its repair, and the coupling of metabolic processes to the cell cycle, as well as the temporal segregation of incompatible metabolic processes, such as nitrogen fixation in certain cyanobacteria (44). We conjecture that global resource allocation models, together with the methodology described here, will allow us to assess the condition-dependent cost and benefit of individual genes (45) in the context of a growing cell, and thereby facilitate the study of metabolic adaptations and metabolic diversity of cyanobacteria (46) with the ultimate aim of understanding the limits of phototrophic growth in complex environments.…”

Daily Rhythms in the Cyanobacterium Synechococcus elongatus Probed by High-resolution Mass Spectrometry–based Proteomics Reveals a Small Defined Set of Cyclic Proteins

“…They demonstrated that 12-h genes have alternating peak heights, which is consistent with our observation at the protein level of pilin polypeptide PilA-like (signal transduction), carbonate dehydratase (nitrogen metabolism), 2-hydroxy-6-oxohepta-24-dienoate hydrolase (no specific function), and a putative uncharacterized protein. Recent reports describe rhythms shorter than 24 h, called ultradian rhythms, which have also been reported to occur in related cyanobacteria such as Cyanothece (48,49) and Prochlorococcus (50).…”

Nitrogen Fixation Outside and Inside Plant Tissues

“…As a result, cyanobacteria are nutritionally independent to a large degree (Meeks, 1988) and occupy diverse habitats, ranging from freshwater and oceanic ecosystems, temperate soils to extreme environments such as hot springs and deserts (Herrero et al, 2001). To counter the adverse effects of oxygen evolution from photosynthesis on BNF, diazotrophic cyanobacteria have developed strategies such as temporal separation of oxygenic photosynthesis and micro-oxic NF (Cerveny et al, 2013) and formation of thick-walled, non-photosynthetic heterocysts with microaerobic interiors that are conducive for NF (Wolk et al, 1994).…”