Nitrogen Fixation in Cyanobacteria

Abstract

Cyanobacteria are oxygenic photosynthetic bacteria that are widespread in marine, freshwater and terrestrial environments, and many of them are capable of fixing atmospheric nitrogen. However, ironically, nitrogenase, the enzyme that is responsible for the reduction of N2, is extremely sensitive to O2. Therefore, oxygenic photosynthesis and N2 fixation are not compatible. Hence, cyanobacteria had to evolve a variety of strategies circumventing this paradox, allowing them to grow at the expense of N2, a ubiquitous source of nitrogen. Some filamentous cyanobacteria differentiate heterocysts. These cells lack the oxygenic photosystem and possess a glycolipid cell wall that keeps the oxygen concentration sufficiently low for nitrogen fixation to take place. This strategy is known as spatial separation of oxygenic photosynthesis and nitrogen fixation. Nonheterocystous cyanobacteria may temporally separate these processes by fixing nitrogen during the night. Again others use a combination of these strategies.

Key Concepts

  • Cyanobacteria may fix the ubiquitously available CO2 and N2, and therefore cover the demand of the two most important elements.
  • The fixation of N2 comes at a high metabolic energy cost, but cyanobacteria are phototrophic organisms that use sunlight to cover their energy demand.
  • Nitrogenase, the enzyme complex responsible for the fixation of N2, is sensitive to oxygen and requires a near‐to‐anoxic environment.
  • Cyanobacteria are phototrophic organisms evolving oxygen and they developed various strategies to combine this with N2 fixation.
  • In order to fix N2, cyanobacteria separate the incompatible processes of oxygenic photosynthesis and N2 fixation spatially (in different cells) or temporally (during the night), or a combination of both.
  • N2 fixation in the ocean is restricted to the (sub)tropics and carried out by free‐living nonheterocystous filamentous and unicellular cyanobacteria and by symbiotic cyanobacteria living with microalgae.
  • Heterocystous cyanobacteria are found in freshwater, brackish water, terrestrial environments and symbiotic in plants and algae.
  • Cyanobacteria have a circadian clock that synchronises metabolic processes and allow for the fixation of N2.

Keywords: circadian rhythm; cyanobacteria; heterocyst; nitrogenase; nitrogen fixation

Figure 1. Examples of N2‐fixing cyanobacteria. Top: heterocystous cyanobacteria. From left to right: Calothrix, Fischerella and Nodularia. Centre: nonheterocystous filamentous cyanobacteria. From left to right: Trichodesmium, Symploca and Lyngbya. Bottom: unicellular cyanobacteria. From left to right: Crocosphaera, Cyanothece and Gloeothece.
Figure 2. Nitrogenase is an enzyme complex consisting of dinitrogenase reductase (Fe‐protein), composed of two identical subunits encoded by nifH, and dinitrogenase (MoFe‐protein), composed of four subunits, 2 by 2 identical and encoded by nifD and nifK. Dinitrogenase reductase reduces dinitrogenase after accepting electrons from ferredoxin, while hydrolysing ATP. Dinitrogenase subsequently reduces N2 to NH3 and H2.
Figure 3. Daily patterns of N2 fixation in various cyanobacteria. Top: heterocystous cyanobacteria. From left to right: Anabaena, Aphanizomenon and Nodularia. Centre: nonheterocystous filamentous cyanobacteria. From left to right: Trichodesmium, Symploca and Lyngbya. Bottom: unicellular cyanobacteria. From left to right: Gloeothece, Crocosphaera and Cyanothece.
Figure 4. A heterocyst neighboured by vegetative cells. This scheme illustrates the spatial separation of oxygenic photosynthesis (in the vegetative cell) and N2 fixation (in the heterocyst) and the relationships between them.
Figure 5. N2 fixation is monitored in an exponentially growing culture of Lyngbya aestuarii. Nitrogenase activity shows a cycle of approximately 24 h, indicative for a circadian rhythm. Reproduced with permission from Stal and Krumbein (1985) © Springer Science and Business Media.
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Further Reading

Bergman B, Gallon JR, Rai AN and Stal LJ (1997) N2 fixation by non‐heterocystous cyanobacteria. FEMS Microbiology Reviews 19: 139–185.

Berman‐Frank I, Lundgren P and Falkowski P (2003) Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Research in Microbiology 154: 157–164.

Bombar D, Heller P, Sanchez‐Baracaldo P, Carter PJ and Zehr JP (2014) Comparative genomics reveals surprising divergence of two closely related strains of uncultivated UCYN‐A cyanobacteria. The ISME Journal 8: 2530–2542.

Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiological Reviews 56: 340–373.

Gallon JR (1992) Reconciling the incompatible: N2 fixation and O2. New Phytologist 122: 571–609.

Sherman LA, Meunier P and Colón‐López MS (1998) Diurnal rhythms in metabolism: a day in the life of a unicellular, diazotrophic cyanobacterium. Photosynthesis Research 58: 25–42.

Stal LJ and Zehr JP (2008) Cyanobacterial nitrogen fixation in the ocean: diversity, regulation, and ecology. In: Flores E and Herrero A (eds) The Cyanobacteria: Molecular Biology, Genomics and Evolution, pp. 423–446. Norfolk, UK: Caister Academic Press.

Thompson AW and Zehr JP (2013) Cellular interactions: lessons from the nitrogen‐fixing cyanobacteria. Journal of Phycology 49: 1024–1035.

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Stal, Lucas J(Dec 2015) Nitrogen Fixation in Cyanobacteria. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021159.pub2]