Cyanobacterial Heterocysts

Abstract

Cyanobacteria are phototrophic bacteria carrying out oxygen‐producing photosynthesis. Besides showing the capability of building their cellular carbon from carbon dioxide (CO2), available in the atmosphere, several strains of cyanobacteria have also acquired the ability to fix molecular dinitrogen (N2), a ubiquitous source of nitrogen. As the enzyme responsible for nitrogen fixation (nitrogenase) is highly sensitive to oxygen, nitrogen fixation and oxygenic photosynthesis cannot take place simultaneously in cyanobacterial cells. To solve this problem, some filamentous strains are able to restrict N2 fixation to a specialised cell type, the heterocyst. Heterocysts are morphologically distinct, terminally differentiated cells that develop, in the absence of alternative sources of combined nitrogen, mostly in a semiregular pattern along the filaments. Thus, a filament containing heterocysts provides division of labour between vegetative cells (photosynthetic CO2 fixation) and heterocysts (anaerobic N2 fixation). These cyanobacteria represent true multicellular organisms with profound morphological cell differentiation and sophisticated intercellular communication systems, ultimately orchestrated by complex gene expression patterns.

Key Concepts

  • Although bacteria, some filamentous cyanobacteria are true multicellular organisms, showing different cell types performing specialised tasks.
  • When lacking a source of combined nitrogen, these cyanobacteria start a program of cell differentiation resulting in a pattern of semiregularly spaced heterocysts along the filament.
  • Heterocysts differentiate from vegetative cells, which carry out oxygenic photosynthesis, and provide a microoxic environment for the activity of oxygen‐labile nitrogenase.
  • Nitrogenase is the enzyme responsible for N2 fixation and allows the organism to live from sunlight, air (CO2 and N2) and some minerals.
  • The two cell types rely on each other and exchange metabolites and signalling molecules, via septal junctions mediating cell‐to‐cell contact.
  • Two transcription factors, HetR and NtcA, regulate the changes in gene expression during heterocyst differentiation.
  • The pattern of spaced heterocysts is regulated by inhibitor gradients that promote the decay of HetR, confirming mathematical models of two‐dimensional pattern formation in heterocystous cyanobacteria.

Keywords: cyanobacteria; differentiation; nitrogen fixation; pattern formation; cell–cell communication

Figure 1. Patterned differentiation of heterocysts in diazotrophic filaments of Nostoc sp. PCC 7120. (a) Filaments growing on top of combined nitrogen‐free media. Courtesy of Elvira Olmedo‐Verd, CSIC and Universidad de Sevilla, Spain. (b) Structures of a vegetative cell (left) and a terminal heterocyst (right) visualised by transmission electron microscopy. Specific features of heterocysts, such as polar granule, heterocyst glycolipids (HGL) and heterocyst polysaccharides (HEP) are indicated. (c) Schematic representation of differentiation of a mature heterocyst from a vegetative cell. (d) Schematic representation of membrane systems and envelopes characteristic of a vegetative cell (left) and a heterocyst (right).
Figure 2. Molecular exchange occurs through nanopores in the septal peptidoglycan, which harbour septal junction complexes. (a) Scheme of a filament showing molecular exchange between vegetative cells and heterocysts. Fixed carbon is transferred in the form of glutamate and sucrose, whereas fixed nitrogen is transferred as glutamine and β‐aspartyl‐arginine. (b) Electron micrograph of isolated septal murein with central nanopore array consisting of dozens of nanopores with diameters of 20 nm. (c) Electron cryo tomogram of a septum between two vegetative cells. Arrows point to septal junctions (courtesy of Martin Pilhofer and Gregor Weiss, ETH Zürich, Switzerland). (d) Scheme of putative septal junctions (shown in orange) between vegetative cells.
Figure 3. Heterocyst‐specific gene expression analysed by promoter fusion to the gfp gene encoding green fluorescent protein. Expression of small RNA NsiR8 (Brenes‐Álvarez et al., ) is shown both in immature heterocysts (still showing red autofluorescence, marked with asterisks) and in mature heterocysts (showing diminished red autofluorescence, marked with triangles). Confocal fluorescence images correspond to bright field (a), red autofluorescence (b) and merged red (autofluorescence) plus green (GFP) fluorescence (c).
Figure 4. Simplified scheme of the relevant steps involved in the differentiation of mature, functional heterocysts. An approximate time scale is shown for heterocyst differentiation in the model cyanobacterium Nostoc sp. PCC 7120 under laboratory conditions.
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Further Reading

Flores E and Herrero A (2010) Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nature Reviews. Microbiology 8: 39–50.

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Zhao J and Wolk CP (2008) Developmental biology of heterocysts, 2006. In: Whitworth DE (ed.) Myxobacteria: Multicellularity and Differentiation, pp 397–418. ASM Press: Washington, D.C.

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Muro‐Pastor, Alicia M, and Maldener, Iris(Nov 2019) Cyanobacterial Heterocysts. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000306.pub3]