Cyanobacterial Heterocysts

Iris Maldener, University of Tübingen, Tübingen, Germany
Alicia M Muro‐Pastor, CSIC‐Universidad de Sevilla, Sevilla, Spain

Published online: October 2010

DOI: 10.1002/9780470015902.a0000306.pub2

Cyanobacteria are phototrophic bacteria carrying out oxygen-producing photosynthesis. Indeed, cyanobacteria were the inventors of oxygenic photosynthesis carried out by eukaryotic algae and plants. Besides showing the capability of building their cellular carbon from carbon dioxide, available in the atmosphere, several strains of cyanobacteria have also acquired the ability to fix molecular dinitrogen (N2). As the enzyme responsible for nitrogen fixation (nitrogenase) is highly sensitive towards 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 special cell type, the heterocyst. Heterocysts are specialised, morphologically distinct, terminally differentiated cells that develop, in the absence of alternative sources of combined nitrogen, mostly in a semiregular pattern along the filament. Thus, a filament containing heterocysts provides division of labour between photosynthetic carbon dioxide fixation (in vegetative cells) and anaerobic N2 fixation (in heterocysts). These cyanobacteria represent true multicellular organisms with profound morphological cell differentiation and sophisticated intercellular communication systems.

Key Concepts:

  • Although bacteria, some filamentous cyanobacteria are true multicellular organisms, showing different cell types for specialised tasks.
  • When starved for a source of combined nitrogen these cyanobacteria start a programme of cell differentiation resulting in a pattern of semiregularly spaced heterocysts along the filament.
  • Heterocysts develop from vegetative cells, the sites for oxygenic photosynthesis, and provide a microoxic environment for the oxygen-labile nitrogenase.
  • Nitrogenase is the enzyme responsible for N2 fixation and allows the organism to live from sunlight, air (carbon dioxide and N2) and some minerals.
  • Under nitrogen fixing conditions the two cell types rely on each other and exchange metabolites and signalling molecules, presumably via protein-complex-mediated cell-to-cell contact or the continuous periplasmic space that surrounds all cells of the multicellular filament.
  • Global nitrogen control factor NtcA controls activation of many genes involved in heterocyst differentiation and function.
  • HetR, the activator of heterocyst differentiation, is regulated by NtcA, known inhibitors of heterocyst differentiation PatS and HetN, as well as by proteins HetF and PatA controlling HetR turnover.
  • 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 communication

Figure 1. Ultrastructure of Anabaena strain PCC 7120. The structures of a terminal heterocyst and two vegetative cells visualised by transmission electron microscopy.
Figure 2. Intracellular solute exchange could occur via a periplasmic route or with the aid of cell-to-cell connections in a filament of Anabaena. (a) Electron micrograph of the septum between two vegetative cells of an Anabaena filament. Purple arrows point to electron dense material traversing the septum through the periplasmic space that could present putative cell-to-cell bridges. (b) Filament of Anabaena sp. PCC 7120 (strain CSAM137; Flores et al., 2007) expressing an SepJ-GFP fusion protein. GFP is found in the middle of the septum between two cells. Courtesy of Vicente Mariscal, CSIC and Universidad de Sevilla, Spain. (c) Scheme of intracellular and periplasmatic routes of solutes between the cells of a heterocystous filament: Barrels represent exporter, as putative sugar transporters of vegetative cells, tetrads represent importers of solutes, as amino acids imported by heterocysts. Protein complexes are localised in the septum, putatively composed of SepJ and Fra proteins that allow the transport of small solutes (small yellow dots) between adjacent cells of the filaments. Half circles and half squares represent binding proteins and dots represent solutes that diffuse through the periplasmic space. Artwork of (c) by Ingeborg Schleip is gratefully acknowledged.
Figure 3. Fluxes of carbon, nitrogen and reductant in heterocysts. Heterocysts act as a sink for carbohydrates (sucrose?) from vegetative cells and as a source of fixed nitrogen (glutamine, NH4+, aspartate?) to vegetative cells. Solid lines represent fluxes of carbon and nitrogen; dashed lines refer to fluxes of reducing equivalents; question marks indicate uncertainties. Enzymes, enzyme complexes and components of the electron transport chains are circled; storage compounds are in italic; metabolites are depicted in regular letters. Abbreviations: AcCoA, acetyl-coenzyme A; arg, arginine; asp, aspartate; b6/f, cytochrome b6/f complex; cit, citrate; fruc, fructose; F6P, fructose 6-phosphate; Fdx, vegetative cell-type ferredoxin; FdxH, heterocyst-specific ferredoxin; FNR, ferredoxin: NADP+ oxidoreductase; G6P, glucose 6-phosphate; 6PG, 6-phosphogluconate; gln, glutamine; glu, glutamate; gluc, glucose; H2ase, uptake hydrogenase; isocit, isocitrate; KG, -ketoglutarate; NDH, NAD(P)H dehydrogenase; oaa, oxaloacetate; ox. PPC, oxidative pentose phosphate cycle; P, inorganic phosphate; PEP, phosphoenolpyruvate; PGA, 3-phosphoglycerate; PSI, photosystem I; pyr, pyruvate; R5P, ribulose 5-phosphate; RET, respiratory electron transport; trioseP, triose phosphate. Not all intermediates are depicted. Modified from Wolk et al. (1994, Figure 4). Copyright © Kluwer Academic Publishers 1994, with kind permission.
Figure 4. Increased expression of GFP from the ntcA promoter in (pro)heterocysts 8 h after nitrogen step-down. The micrograph is an overlay of red (autofluorescence) and green (GFP fluorescence) channels (see also Olmedo-Verd et al., 2006).
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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.
    Kumar K, Mella-Herrera RA and Golden JW (2010) Cyanobacterial Heterocysts. Cold Spring Harbor Perspectives in Biology 2009 2: a000315, originally published online February 24, 2010, pp. 1–19.
    book Xu X, Elhai J and Wolk CP (2008) "Transcriptional and developmental responses by Anabaena to deprivation of fixed nitrogen". In: Herrero A and Flores E (eds) The Cyanobacteria. Molecular Biology, Genomics and Evolution. Norfolk, UK: Caister Academic Press.
    Zhang C-C, Laurent S, Sakr S, Peng L and Bédu S (2006) Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Molecular Microbiology 59: 367–375.
    book Zhao J and Wolk CP (2008) "Developmental biology of heterocysts, 2006". In: Whitworth DE (ed.) Myxobacteria: Multicellularity and Differentiation, pp. 397–418. Washington, DC: ASM Press.

Related Sub-Topics:

Multicellularity | Bacteria | Microbial Photosynthesis | Microbial Interactions and Communities
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Article Title: Cyanobacterial Heterocysts
 
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Maldener, Iris, and Muro‐Pastor, Alicia M(Oct 2010) Cyanobacterial Heterocysts. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000306.pub2]