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Cyanobacterial Advanced article Heterocysts Article Contents . Introduction Iris Maldener, Institute of Microbiology/Organismic Interactions; University of Tu¨bingen, . Structure of Mature Heterocysts . Heterocyst Function Tu¨bingen, Germany . Heterocyst Development Alicia M Muro-Pastor, Instituto de Bioquı´mica Vegetal y Fotosı´ntesis, CSIC-Universidad . Acknowledgements de Sevilla, Sevilla, Spain Online posting date: 18th October 2010 Based in part on the previous version of this Encyclopedia of Life Sciences (ELS) article, Cyanobacterial Heterocysts by Annelies Ernst and Iris Maldener. Cyanobacteria are phototrophic bacteria carrying out Introduction oxygen-producing photosynthesis. Indeed, cyanobacteria were the inventors of oxygenic photosynthesis carried out Diazotrophic cyanobacteria, which fix molecular nitrogen, by eukaryotic algae and plants. Besides showing the cap- are photosynthetic microorganisms that gain their energy ability of building their cellular carbon from carbon di- from sunlight and their carbon and nitrogen from air and oxide, available in the atmosphere, several strains of water. Being able to utilise carbon dioxide, nitrogen and cyanobacteria have also acquired the ability to fix water as macronutrients, these organisms can occupy molecular dinitrogen (N ). As the enzyme responsible niches not accessible to other microorganisms that require 2 reduced carbon compounds and chemically less inert, for nitrogen fixation (nitrogenase) is highly sensitive bound, nitrogen species for growth. Fixation of nitrogen towards oxygen, nitrogen fixation and oxygenic photo- is a highly energy-demanding process catalysed by an synthesis cannot take place simultaneously in cyano- extremely oxygen-labile enzyme, nitrogenase. Organisms bacterial cells. To solve this problem, some filamentous that fix nitrogen have evolved a variety of strategies to strains are able to restrict N2 fixation to a special cell maintain an active nitrogenase in the presence of oxygen, type, the heterocyst. Heterocysts are specialised, mor- and cyanobacteria are even able to reconcile photo- phologically distinct, terminally differentiated cells that synthetic oxygen production with nitrogen fixation (Fay, develop, in the absence of alternative sources of combined 1992; Gallon, 1992). Some cyanobacteria bypass the oxy- nitrogen, mostly in a semiregular pattern along the fila- gen problem by making their nitrogenases only in the dark ment. Thus, a filament containing heterocysts provides when photosynthesis is inactive and the intracellular par- division of labour between photosynthetic carbon dioxide tial pressure of oxygen (PO2) is lowered by respiration. In this case the two processes are temporally separated. Sev- fixation (in vegetative cells) and anaerobic N fixation (in 2 eral strains of multicellular cyanobacteria can modify a heterocysts). These cyanobacteria represent true multi- small percentage of their cells for the task of nitrogen fix- cellular organisms with profound morphological cell ation, thereby generating a spatial separation of the pro- differentiation and sophisticated intercellular communi- cesses. In some genera the functional specialisation of cation systems. nitrogen-fixing cells is accompanied by a morphological differentiation of about every tenth cell of a filament into heterocysts, producing a semiregular pattern of morpho- logically and metabolically different cell types. Prospective heterocysts form a special envelope that limits the entrance of oxygen. Additionally they enhance their respiratory activity and switch-off the oxygen-releasing activity of ELS subject area: Microbiology photosystem II. This allows the mature heterocyst to gen- erate a microoxic environment suitable for the functioning How to cite: of nitrogenase. Because developing heterocysts lose the Maldener, Iris; and Muro-Pastor, Alicia M (October 2010) ability to fix carbon dioxide, adjacent vegetative cells have Cyanobacterial Heterocysts. In: Encyclopedia of Life Sciences (ELS). to provide reduced compounds for the generation of John Wiley & Sons, Ltd: Chichester. reductants for respiration and nitrogen fixation. In turn, DOI: 10.1002/9780470015902.a0000306.pub2 heterocysts supply vegetative cells with the needed fixed ENCYCLOPEDIA OF LIFE SCIENCES & 2010, John Wiley & Sons, Ltd. www.els.net 1 Cyanobacterial Heterocysts nitrogen, probably in the form of amino acids. Having Heterocyst two different cell types (photosynthetic vegetative cells and specialised nitrogen-fixing heterocysts) these cyano- bacteria can be considered as true multicellular organisms. Hep-layer Both cell types of the trichome depend on each other and must communicate with respect to exchange of metabolites N2 NH3 as well as signalling molecules. This communication could operate via the continuous periplasm or via cell-to-cell connections. HM Heterocysts undergo a terminal differentiation and Fixed nitrogen become unable to reproduce by cell division. In diazo- Fixed carbon Hgl-layer trophically growing filaments the semiregular pattern of heterocysts is maintained by differentiation of new het- erocysts at approximately equal distances between two pre- Polar granule existing ones. The possibility to grow filaments without CO2 Glucose heterocysts by supplying them with combined nitrogen has CM facilitated the isolation and characterisation of mutants TM specifically affected in heterocyst development and func- OM tion. The phenotype of mutants range from absence of Vegetative cells heterocysts to the presence of aberrant or supernumerary Carboxysome heterocysts (MCH). Through the use of mutants, such complex processes as sensing and responding to environ- mental signals, control of differentiation, intercellular communication and biological pattern formation became Figure 1 Ultrastructure of Anabaena strain PCC 7120. The structures of a amenable to analysis. See also: Cyanobacteria; Nitrogen terminal heterocyst and two vegetative cells visualised by transmission Fixation; Nitrogenase Complex; Photosynthesis; Photo- electron microscopy. synthesis and Respiration in Cyanobacteria; Photo- synthesis: Light Reactions; Photosynthesis: The Calvin Cycle extracellular deposition of Hep and Hgl exhibit a highly oxygen-sensitive nitrogenase that is synthesised only under microaerobic growth conditions (reviewed in Awai et al., Structure of Mature Heterocysts 2009; Nicolaisen et al., 2009). See also: Polysaccharides Membranes The differences in ultrastructure of vegetative cells and heterocysts (Figure 1) reflect the strategy of heterocyst- In heterocysts, four types of lipid bilayers are observed that forming cyanobacteria to reconcile two incompatible differ in composition and function. processes: oxygenic photosynthesis and oxygen-sensitive i. Intracellular thylakoids contain photosynthetic pig- nitrogen fixation. ments and components of the photosynthetic and Heterocyst envelope respiratory electron transport chain. However, they differ structurally and functionally from those in vege- To limit the entrance of oxygen, mature heterocysts have a tative cells (Figure 1). They lack photosystem II activity special envelope that consists of a laminated layer con- and the amount of phycobiliproteins, the major light taining heterocyst glycolipids (Hgl) and a protective harvesting pigments of photosystem II, is reduced. homogeneous layer of heterocyst envelope polysaccharides The remaining pigments serve as antennae of photo- (Hep) (Figure 1). Hgl is composed of a hydrophilic sugar system I. The primary function of heterocyst thylakoids moiety (glucose, galactose and mannose) linked via a appears to be the provision of extra ATP (adenosine glycosidic bond to a C26 or C28 polyhydroxy or ketohy- triphosphate) for nitrogenase by means of cyclic pho- droxy hydrocarbon chain; polyhydroxy and ketohydroxy tophosphorylation. See also: Photosystem I; Photosys- Hgl are products of distinct biosynthetic pathways. Inter- tem II actions of the hydrophobic chains result in the formation of ii. Photomicrographs show a paucity of absorption of lipid monolayers of 4 nm width with low permeability for chlorophyll towards the poles of heterocysts, in the gases and solutes. Heterocyst envelope polysaccharides region of the ‘honeycomb’ membrane, named after consist of concatamers of an oligosaccharide that has a its distinct regular structure. In the dark, the product of tetrasaccharide backbone (25% mannose, 75% glucose) oxidation of diaminobenzidine, which reacts with hae- and side-chains comprising strain-specific combinations of moproteins, is accumulated preferentially in this region. mannose, glucose, galactose, xylose and arabinose as This was taken as evidence for enhanced respiratory terminal residues. Mutants defective in the synthesis or activity in this membrane region. 2 ENCYCLOPEDIA OF LIFE SCIENCES & 2010, John Wiley & Sons, Ltd. www.els.net Cyanobacterial Heterocysts iii. The cytosol is surrounded by the cytoplasmic membrane. mechanisms are involved in intracellular exchange. A This membrane lacks photosynthetic pigments. Mem- continuous periplasmic space represents a good possible brane energisation is provided by hydrogen ion-trans- extracellular candidate route for substances that have to locating respiratory electron transport chains and, in move along the filament from one cell to another. Since the some strains, by hydrogen ion-translocating ATP outer membrane is continuous along the filament, the hydrolases. The cytoplasmic membrane contains periplasmic space should also be continuous, thus sur- numerous
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