Skip to main content
SpringerLink
Log in
Book cover

Inclusions in Prokaryotes pp 167–193Cite as

Cyanophycin—an Ideal Bacterial Nitrogen Storage Material with Unique Chemical Properties

  • Chapter

Part of the book series: Microbiology Monographs ((MICROMONO,volume 1))

Abstract

Cyanophycin (CGP) is a nitrogen-rich, polypeptide-like storage material of cyanobacteria and heterotrophic bacteria. CGP inclusions were discovered more than 100 years ago and from that time on have attracted the interest of many researchers with both basic and applied research interests. The discovery of CGP goes along with the development of the light microscope and the electron microscope, respectively, as well as application of differential staining techniques and refined analysis methods that were employed to determine its chemical structure. CGP has different physiological functions depending on the cell type and organism in which it occurs, but can be considered as a widespread intracellular nitrogen reserve. Its biosynthesis is mediated by the activity of a single enzyme, the cyanophycin synthetase, that possesses two putative active sites responsible for the alternating incorporation of the amino acids arginine and aspartic acid. Heterologous expression of CGP synthetase genes (cphA) and the activity of the enzyme during in vitro studies led to the formation of CGP with altered monomer composition. By employment of recombinant bacterial strains that accumulate large amounts of CGP, strategies were developed to produce CGP in semitechnical amounts in comparably cost effective and time saving biotechnological processes. CGP inclusion body formation in transgenic plant lines demonstrated the potential of eukaryotic organisms to serve as hosts for heterologous expression of cphA and as potential future CGP production organisms.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Aboulmagd E, Oppermann-Sanio FB, Steinbüchel A (2000) Molecular characterization of the cyanophycin synthetase from Synechocystis sp. strain PCC6308. Arch Microbiol 174:297–306

    Article  PubMed  CAS  Google Scholar 

  • Aboulmagd E, Oppermann-Sanio FB, Steinbüchel A (2001a) Purification of Synechocystis sp. strain PCC6308 cyanophycin synthetase and its characterization with respect to substrate and primer specificity. Appl Environ Microbiol 67:2176–2182

    Article  PubMed  CAS  Google Scholar 

  • Aboulmagd E, Voss I, Oppermann-Sanio FB, Steinbüchel A (2001b) Heterologous expression of cyanophycin synthetase and cyanophycin synthesis in the industrial relevant bacteria Corynebacterium glutamicum and Ralstonia eutropha and in Pseudomonas putida. Biomacromolecules 2:1338–1342

    Article  PubMed  CAS  Google Scholar 

  • Allen MM (1984) Cyanobacterial cell inclusions. Annu Rev Microbiol 38:1–25

    Article  PubMed  CAS  Google Scholar 

  • Allen MM (1988) Inclusions: cyanophycin. Methods Enzymol 167:207–213

    CAS  Google Scholar 

  • Allen MM, Hawley MA (1983) Protein degradation and synthesis of cyanophycin granule polypeptide in Aphanocapsa sp. J Bacteriol 154:1480–1484

    PubMed  CAS  Google Scholar 

  • Allen MM, Hutchinson F, Weathers PJ (1980) Cyanophycin granule polypeptide formation and degradation in the cyanobacterium Aphanocapsa 6308. J Bacteriol 141:687–693

    PubMed  CAS  Google Scholar 

  • Allen MM, Morris R, Zimmermann W (1984) Cyanophycin granule polypeptide protease in a unicellular cyanobacterium. Arch Microbiol 138:119–123

    Article  CAS  Google Scholar 

  • Allen MM, Courtney Y, Medeiros L, Zizlsperger N, Farooq M, Kolodny NH (2005) Effects of light and chloramphenicol stress on incorporation of nitrogen into cyanophycin in Synechocystis sp. strain PCC 6308. Biochim Biophys Acta 1725:141–146

    Google Scholar 

  • Allen MM, Weathers PP (1980) Structure and composition of cyanophycin granules in the cyanobacterium Aphanocapsa 6308. J Bacteriol 141:959–962

    PubMed  CAS  Google Scholar 

  • Ariño X, Ortega-Calvo JJ, Hernandez-Marine M, Saiz-Jimenez C (1995) Effect of sulfur starvation on the morphology and ultrastructure of the cyanobacterium Gloeothece sp. PCC 6909. Arch Microbiol 163:447–453

    Google Scholar 

  • Baumgärtel O (1920) Das Problem der Cyanophyceenzelle. Arch Protistenk 41:50–148

    Google Scholar 

  • Berg H, Ziegler K, Piotukh H, Baier K, Lockau W (2000) Biosynthesis of the cyanobacterial reserve polymer multi-l-arginyl-poly-l-aspartic acid (cyanophycin). Mechanism of the cyanophycin synthetase reaction studied with synthetic primers. Eur J Biochem 267:5561–5570

    Article  PubMed  CAS  Google Scholar 

  • Borzi A (1887) Le communicazione intracellulari delle Nostochinee. Malpighia 1:74–203

    Google Scholar 

  • Byrom D (1992) Production of poly-β-hydroxy-butyrate-poly-β-hydroxyvalerate copolymers. FEMS Microbiol Rev 103:247–250

    CAS  Google Scholar 

  • Caiola MM (1975) A light electron microscopic study of blue-green algae growing in the coralloid-roots of Encephalartos altensteinii and in culture. Phycologia 14:25–33

    Google Scholar 

  • Carr NG (1988) Nitrogen reserve and dynamic reservoirs in cyanobacteria. In: Rogers LJ, Gallon JR (eds) Biochemistry of algae and cyanobacteria. Clarendon, Oxford, pp 13–21

    Google Scholar 

  • Chiu WL, Peters GA, Levieille G, Still PC, Cousins S, Osborne B, Elhai J (2005) Nitrogen deprivation stimulates symbiotic gland development in Gunnera manicata. Plant Physiol 139:224–230

    Article  PubMed  CAS  Google Scholar 

  • Dembinska ME, Allen MM (1988) Cyanophycin granule size variation in Aphanocapasa. J Gen Microbiol 143:295–298

    Google Scholar 

  • Drawert H (1949) Zellmorphologische und Zellphysiologische Studien an Cyanophyceen. Planta 37:161–209

    Article  CAS  Google Scholar 

  • Drews G, Niklowitz W (1957) Beiträge zur Cytologie der Blaualgen. 3. Untersuchungen über die granulären Einschlüsse der Hormogonales. Arch Mikrobiol 25:33–351

    Article  Google Scholar 

  • Eggerling L, Sahm H (1999) l-glutamate and l-lysine: traditional products with impetuous developments. Appl Microbiol Biotechnol 52:146–153

    Article  Google Scholar 

  • Elbahloul Y, Krehenbrink M, Reichelt R, Steinbüchel A (2005a) Physiological conditions conducive to high content in biomass of Acinetobacter calcoaceticus strain ADP1. Appl Environ Microbiol 71:858–866

    Article  PubMed  CAS  Google Scholar 

  • Elbahloul Y, Frey K, Sanders J, Steinbüchel A (2005b) Protamylasse, a residual compound of industrial starch production provides a suitable medium for large scale cyanophycin production Appl Environ Microbiol 71:7759–7767

    Article  PubMed  CAS  Google Scholar 

  • Erickson NA, Kolodny NH, Allen MM (2001) A rapid and sensitive method for the analysis of cyanophycin. Biochim Biophys Acta 1526:5–9

    PubMed  CAS  Google Scholar 

  • Fogg GE (1951) Growth and heterocyst production in Anabaena cylindrica Lemm. III The cytology of heterocysts. Ann Bot 15:23–35

    Google Scholar 

  • Frey KM, Oppermann-Sanio FB, Schmidt H, Steinbüchel A (2002) Technical-scale production of cyanophycin with recombinant strains of Escherichia coli. Appl Environ Microbiol 68:3377–3384

    Article  PubMed  CAS  Google Scholar 

  • Fritsch FE (1945) The structure and reproduction of the algae, vol II. Cambridge University Press, Cambridge

    Google Scholar 

  • Füchtenbusch B, Wullbrandt D, Steinbüchel A (2000) Production of polyhydroxyalkanoic acids by Ralstonia eutropha and Pseudomonas oleovorans from an oil remaining from biotechnological rhamnose production. Appl Microbiol Biotechnol 53:167–172

    Article  PubMed  Google Scholar 

  • Fuhs GW (1958) Untersuchungen an Ultradünnschnitten von Oscillatoria amoena. Protoplasma 49:523–540

    Article  Google Scholar 

  • Füser G, Steinbüchel A (2005) Investigations on the solubility behavior of cyanohycin in solutions of simple inorganic salts. Biomacromolecules 6:1367–1374

    Article  PubMed  CAS  Google Scholar 

  • Geitler L (1932) Cyanophyceae. In: Kolkwitz R (ed) Dr. L. Rabenhorst’s Kryptogamen-Flora, vol 14. Rabenhorst, Leipzig, pp 7–8

    Google Scholar 

  • Golecki JR, Heinrich UR (1991) Ultrastructural and electron spectroscopic analyses of cyanobacteria and bacteria. J Microsc 162:147–154

    PubMed  CAS  Google Scholar 

  • Gorelova OA, Kleimenov SI (2003) The accumulation and degradation dynamics of cyanophycin in cyanobacteria grown in symbiotic associations with plant tissues and cells. Mikrobiologiia 72:361–369

    PubMed  CAS  Google Scholar 

  • Gupta M, Carr NG (1981) Enzyme activities related to cyanophycin metabolism in heterocysts and vegetative cells of Anabaena sp. J Gen Microbiol 125:7–13

    Google Scholar 

  • Hai T, Oppermann-Sanio FB, Steinbüchel A (1999) Purification and characterization of cyanophycin and cyanophycin synthetase from the thermophilic Synechococcus sp. MA19. FEMS Microbiol Lett 181:229–236

    Article  PubMed  CAS  Google Scholar 

  • Hai T, Ahlers H, Gorenflo V, Steinbüchel A (2000) Axenic cultivation of anoxygenic phototrophic bacteria, cyanobacteria and microalgae in a new closed tubular photobioreactor. Appl Microbiol Biotechnol 53:383–389

    Article  PubMed  CAS  Google Scholar 

  • Hai T, Oppermann-Sanio FB, Steinbüchel A (2002) Molecular characterization of a thermostable cyanophycin synthetase from the thermophilic cyanobacterium Synechococcus sp. strain MA19 and in vitro synthesis of cyanophycin and related polyamides. Appl Environ Microbiol 68:93–101

    Article  PubMed  CAS  Google Scholar 

  • Hegler R (1901) Untersuchungen über die Organisation der Phycochromaceenzelle. Jahrb Wiss Bot 36:229–354

    Google Scholar 

  • Hejazi M, Piotukh K, Mattow J, Deutzmann R, Volkmer-Engert R, Lockau W (2002) Isoaspartyl dipeptidase activity of plant-type asparaginases. Biochem J 364:129–136

    PubMed  CAS  Google Scholar 

  • Hiraishi T, Kajiyama M, Tabata K, Abe H, Yamato I, Doi Y (2003a) Biochemical and molecular characterization of poly(aspartic acid) hydrolase-2 from Sphingomonas sp. KT-1. Biomacromolecules 4:1285–1292

    Article  PubMed  CAS  Google Scholar 

  • Hiraishi T, Kajiyama M, Tabata K, Yamato I, Doi Y (2003b) Genetic analysis and characterization of poly(aspartic acid) hydrolase-1 from Sphingomonas sp. KT-1. Biomacromolecules 4:80–86

    Article  PubMed  CAS  Google Scholar 

  • Howarth RW, Cole JJ (1985) Molybdenum availability, nitrogen limitation, and phytoplankton growth in natural waters. Science 229:653–655

    CAS  PubMed  Google Scholar 

  • Joentgen W, Groth T, Steinbüchel A, Hai T, Oppermann FB (1998) Poly-aspartic acid homopolymers and copolymers, biotechnical production and use thereof. Int Patent Appl WO 98/39090

    Google Scholar 

  • Joentgen W, Müller N, Mitschker A, Schmidt H (2003) Polyaspartic acids. In: Fahnestock SR, Steinbüchel A (eds) Biopolymers, vol 7. Wiley, Weinheim, pp 175–199

    Google Scholar 

  • Krehenbrink M, Steinbüchel A (2004) Partial purification and characterization of a non-cyanobacterial cyanophycin synthetase from Acinetobacter calcoaceticus strain ADP1 with regard to substrate specificity, substrate affinity and binding to cyanophycin. Microbiology 150:2599–2608

    Article  PubMed  CAS  Google Scholar 

  • Krehenbrink M, Oppermann-Sanio FB, Steinbüchel A (2002) Evaluation of non-cyanobacterial genome sequences for occurrence of genes encoding proteins homologous to cyanophycin synthetase and cloning of active cyanophycin synthetase from Acinetobacter sp. strain DSM 587. Arch Microbiol 177:371–380

    Article  PubMed  CAS  Google Scholar 

  • Lang NJ (1968) The fine structure of blue-green algae. Annu Rev Microbiol 22:15–46

    Article  PubMed  CAS  Google Scholar 

  • Lang NJ, Fisher A (1969) Variation in the fixation image of structured granules in Anabaena. Arch Mikrobiol 67:173–181

    Article  PubMed  CAS  Google Scholar 

  • Lang NJ, Simon RD, Wolk P (1972) Correspondence of cyanophycin granules with structured granules in Anabaena cylindrica. Arch Microbiol 83:313–320

    Google Scholar 

  • Laurent S, Forchhammer K, Gonzalez L, Heulin T, Zhang CC, Bedu S (2004) Cell-type specific modification of PII is involved in the regulation of nitrogen metabolism in the cyanobacterium Anabaena PCC 7120. FEBS Lett 576:261–265

    Article  PubMed  CAS  Google Scholar 

  • Lawry NH, Simon RD (1982) The normal and induced occurrence of cyanophycin inclusion bodies in several blue-green algae. J Phycol 18:391–399

    Article  CAS  Google Scholar 

  • Leganés F, Fernández-Piñas, Wolk CP (1998) A transposition-induced mutant of Nostoc elipsosporum implicates an arginine-biosynthetic gene in the formation of cyanophycin granules and of functional heterocysts and akinetes. Microbiology 144:1799–1805

    PubMed  Google Scholar 

  • Li H, Sherman DM, Bao S, Sherman LA (2001) Pattern of cyanophycin acumulation in non-nitrogen-fixing cyanobacteria. Arch Microbiol 176:9–18

    Article  PubMed  CAS  Google Scholar 

  • Liotenberg S, Campbell D, Rippka R, Hourmard J, de Marsac NT (1996) Effect of the nitrogen source on phycobiliprotein synthesis and cell reserves in a chromatically adapting filamentous cyanobacterium. Microbiology 142:611–622

    Article  PubMed  CAS  Google Scholar 

  • Mackerras AH, De Chazal NM, Smith GD (1990) Transient accumulation of cyanophycin in Anabaena cylindrica and Synechocystis 6308. J Gen Microbiol 136:2057–2065

    CAS  Google Scholar 

  • Maugini E (1966) Contributo alla conoscenza citologica di nostoc comune vaucher con particolare riguardo allultrastruttura. Caryologia 19:267–298

    Google Scholar 

  • Merrit MV, Sid SS, Mesh L, Allen MM (1994) Variations in the amino acid composition of cyanophycin in the cyanobacterium Synechocystis sp PCC 6308 as a function of growth conditions. Arch Microbiol 162:158–166

    Google Scholar 

  • Messineo L (1966) Modification of the Sakaguchi reaction: Spectrophotometric determination of arginine in poteins without previous hydrolysis. Arch Biochem Biophys 117:534–540

    Article  CAS  Google Scholar 

  • Miller MM, Lang NJ (1968) The fine structure of akinete formation and germination in Cylindrospermum. Arch Mikrobiol 60:303–313

    Article  Google Scholar 

  • Neumann K, Stephan DP, Ziegler K, Hühns M, Broer I, Lockau W, Pistorius EK (2005) Production of cyanophycin, a suitable source for the biodegradable polymer polyaspartate, in transgenic plants. Plant Biotechnol 3:249–258

    Article  CAS  Google Scholar 

  • Nilsson M, Rasmussen U, Bergman B (2005) Competition among symbiotic cyanobacterial Nostoc strains forming artificial associations with rice (Oryza sativa). FEMS Microbiol Lett 245:139–144

    Article  PubMed  CAS  Google Scholar 

  • Obst M, Steinbüchel A (2004) Microbial degradation of poly(amino acid)s. Biomacromolecules 5:1166–1176

    Article  PubMed  CAS  Google Scholar 

  • Obst M, Oppermann-Sanio FB, Luftmann H, Steinbüchel A (2002) Isolation of cyanophycin degrading bacteria, cloning and characterization of an extracellular cyanophycinase gene (cphE) from Pseudomonas anguilliseptica strain BI. J Biol Chem 277:25096–25105

    Article  PubMed  CAS  Google Scholar 

  • Obst M, Sallam A, Luftmann H, Steinbüchel A (2004) Isolation and characterization of Gram-positive cyanophycin degrading bacteria-kinetic studies on cyanophycin depolymerase activity in aerobic bacteria. Biomacromolecules 5:153–161

    Article  PubMed  CAS  Google Scholar 

  • Obst M, Krug A, Luftmann H, Steinbüchel A (2005) Degradation of cyanophycin by Sedimentibacter hongkongensis strain KI and Citrobacter amalonaticus strain G isolated from an anaerobic bacterial consortium. Appl Environ Microbiol 71:3642–3652

    Article  PubMed  CAS  Google Scholar 

  • Oppermann-Sanio FB, Steinbüchel A (2002) Occurrence, functions and biosynthesis of polyamides in microorganisms and biotechnological production. Naturwissenschaften 89:11–22

    Article  PubMed  CAS  Google Scholar 

  • Oppermann-Sanio FB, Steinbüchel A (2003) Cyanophycin. In: Fahnestock SR, Steinbüchel A (eds) Biopolymers, vol 7. Wiley, Weinheim, pp 83–106

    Google Scholar 

  • Oppermann-Sanio FB, Aboulmagd E, Hai T, Hezayen FF, Jossek S, Steinbüchel A (1999) Biochemisty of microbial polyamide metabolism. In: Steinbüchel A (ed) Proceedings of the international symposium on biochemical principles and mechanisms of biosynthesis and biodegradation of polymers, Münster, Germany. Wiley, Weinheim, pp 368–375

    Google Scholar 

  • Page-Sharp M, Behm CA, Sith GD (1998) Cyanophycin and glycogen synthesis in a cyanobacterial Scytonema species in response to salt stress. FEMS Microbiol Lett 160:11–15

    Article  CAS  Google Scholar 

  • Pandey RK, Talpasayi ERS (1982) Spore differention in relation to certain antibiotics in the blue-green alga Nodularia spumigea Mertens. Z Allg Mikrobiol 22:191–196

    PubMed  CAS  Google Scholar 

  • Pankratz HS, Bowen CC (1963) Cytology of blue-green algae. 1. Cells of symploca muscorum. Am J Bot 50:387–399

    Article  Google Scholar 

  • Picossi S, Valladares A, Flores E, Herrero A (2004) Nitrogen-regulated genes for the metabolism of cyanophycin, a bacterial nitrogen reserve polymer: expression and mutational analysis of two cyanophycin synthetase and cyanophycinase gene clusters in heterocyst-forming cyanobacterium Anabaena sp. PCC 7120. J Biol Chem 279:11582–11592

    Article  PubMed  CAS  Google Scholar 

  • Pötter M, Steinbüchel A (2005) Poly(3-hydroxybutyrate) granule-associated proteins: impacts on poly(3-hydroxybutyrate) synthesis and degradation. Biomacromolecules 6:552–560

    Article  PubMed  CAS  Google Scholar 

  • Qiu YL, Yu J (2003) Azolla—a model organism for plant genomic studies. Genomics Proteomics Bioinformatics 1:15–25

    PubMed  CAS  Google Scholar 

  • Richter R, Hejazi M, Kraft R, Ziegler K, Lockau W (1999) Cyanophycinase, a peptidase degrading the cyanobacterial reserve material multi-l-arginyl-poly-l-aspartic acid (cyanophycin): molecular cloning of the gene of Synechocystis sp. PCC 6803, expression in Escherichia coli, and biochemical characterization of the purified enzyme. Eur J Biochem 263:163–169

    Article  PubMed  CAS  Google Scholar 

  • Rippka R, Stanier RY (1978) The effects of anaerobiosis on nitrogenase synthesis and heterocyst developement by nostocean cyanobacteria. J Gen Microbiol 105:83–94

    CAS  Google Scholar 

  • Ris H, Singh RN (1961) Electron microscope studies on blue-green algae. J Biophys Biochem Cytol 9:63–80

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Lopez M, Muñoz Calvo ML, Gomez-Acebo J (1971) The effect of rifamycins in ultrastructure of Anacystis montana. J Ultrastruct Res 36:595–602

    Article  PubMed  CAS  Google Scholar 

  • Sarma TA, Khattar JIS (1986) Accumulation of cyanophycin and glycogen during sporulation in the blue-green alga Anabaena torulosa. Biochem Physiol Pflanz 181:155–164

    CAS  Google Scholar 

  • Sarma TA, Ahuja G, Khattar JI (2004) Nutrient stress causes akinete differentiation in cyanobacterium Anabaena torulosa with concomitant increase in nitrogen reserve substances. Folia Microbiol (Praha) 49:557–561

    Article  CAS  Google Scholar 

  • Schmidt EW, Nelson JT, Rasko DA, Sudek S, Eisen JA, Haygood MG, Ravel J (2005) Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc Natl Acad Sci USA 102:7315–7320

    Article  PubMed  CAS  Google Scholar 

  • Schwamborn M (1998) Chemical synthesis of polyaspartate: a biodegradable alternative currently used polycarboxylate homo-and copolymers. Polym Degrad Stab 59:39–45

    Article  CAS  Google Scholar 

  • Sherman DM, Tucker D, Sherman LA (2000) Heterocyst development and localization of cyanophycin in N2-fixing cultures of Anabaena sp. PCC7120 (Cyanobacteria). J Phycol 36:932–941

    Article  CAS  Google Scholar 

  • Simon RD (1971) Cyanophycin granules from the Blue-Green alga Anabaena cylindrica: A reserve materal consisting of copolymers of aspartic acid and arginine. Proc Natl Acad Sci USA 68:265–267

    Article  PubMed  CAS  Google Scholar 

  • Simon RD (1973a) Measurement of the cyanophycin granule polypeptide contained in the blue-green alga Anabaena cylindrica. J Bacteriol 114:1213–1216

    PubMed  CAS  Google Scholar 

  • Simon RD (1973b) The effect of chloramphenicol on the production of cyanophycin granule polypeptide in the blue-green alga Anabaena cylindrica. Arch Mikrobiol 92:115–122

    Article  PubMed  CAS  Google Scholar 

  • Simon RD (1976) The biosynthesis of multi-l-arginyl-poly(l-aspartic acid) in the filamentous cyanobacterium Anabaena cylindrica. Biochim Biophys Acta 422:407–418

    PubMed  CAS  Google Scholar 

  • Simon RD (1987) Inclusion bodies in the cyanobacteria: cyanophycin, polyphosphate, polyhedral bodies. In: Fay P, Van Baalen C (eds) The cyanobacteria. Elsevier, Amsterdam, pp 199–225

    Google Scholar 

  • Simon RD, Weathers P (1976) Determination of the structure of the novel polypeptide containing aspartic acid and arginine which is found in cyanobacteria. Biochim Biophys Acta 420:165–176

    PubMed  CAS  Google Scholar 

  • Simon RD, Lawry NH, MCLendon GL (1980) Structural characterization of the cyanophycin granule polypeptide of Anabaena cylindrica by circular dichroism and Raman spectroscopy. Biochim Biophys Acta 626:277–281

    PubMed  CAS  Google Scholar 

  • Steindler L, Huchon D, Avni A, Ilan M (2005) 16S rRNA phylogeny of sponge-associated cyanobacteria. Appl Environ Microbiol 71:4127–4130

    Article  PubMed  CAS  Google Scholar 

  • Stephan DP, Ruppel HG, Pistorius EK (2000) Interrelation between cyanophycin synthesis, l-arginine catabolism and photosynthesis in the cyanobacterium Synechocystis sp. strain PCC 6803. Z Naturforsch 55C:927–942

    Google Scholar 

  • Stewart WDP, Haystead A, Pearson HW (1969) Nitrogenase activity in heterocysts of filamentous blue-green algae. Nature 224:226–228

    Article  PubMed  CAS  Google Scholar 

  • Stubbe J, Tian J, He A, Sinskey AJ, Lawrence AG, Liu P (2005) Nontemplate-dependent polymerization processes: polyhydroxyalkanoate synthases as a paradigm. Annu Rev Biochem 74:433–480

    Article  PubMed  CAS  Google Scholar 

  • Suarez C, Kohler SJ, Allen MM, Kolodny NH (1999) NMR study of the metabolic 15N isotopic enrichment of cyanophycin synthesized by the cyanobacterium Synechocystis sp. strain PCC 6308. Biochim Biophys Acta 1426:429–438

    PubMed  CAS  Google Scholar 

  • Tabata K, Kajiyama M, Hiraishi T, Abe H, Doi Y (2001) Purification and characterization of poly(aspartic acid) hydrolase from Sphingomonas sp. KT-1. Biomacromolecules 2:1155–1160

    Article  PubMed  CAS  Google Scholar 

  • Tandeau de Marsac N, Houmard J (1993) Adatation of cyanobacteria to environmental stimuli: new steps towards molecular mechanisms. FEMS Microbiol Rev 104:119–190

    Article  CAS  Google Scholar 

  • Tischer I (1957) Untersuchungen über die granulären Einschlüsse und das Reduktions-Oxidations-Vermögen der Cyanophyceen. Arch Mikrobiol 27:400–428

    Article  PubMed  CAS  Google Scholar 

  • Van Eykelenburg C (1980) Ecophysiological studies on Spirulina platensis in comparison with Oscillatoria. Zentralbl Bakteriol Abt II 131:592–601

    Google Scholar 

  • Voss I, Diniz SC, Aboulmagd E, Steinbüchel A (2004) Identification of Anabaena sp. strain PCC7120 cyanophycin synthetase as a suitable enzyme for production of cyanophycin in Gram-negative bacteria like Pseudomonas putida and Ralstonia eutropha. Biomacromolecules 5:1588–1595

    Article  PubMed  CAS  Google Scholar 

  • Wältermann M, Steinbüchel A (2005) Neutral lipid bodies in prokaryotes: recent insights into structure, formation, and relationship to eukaryotic lipid depots. J Bacteriol 187:3607–3619

    Article  PubMed  CAS  Google Scholar 

  • Wältermann M, Hinz A, Robenek H, Troyer D, Reichelt R, Malkus U, Galla HJ, Kalscheuer R, Stöveken T, von Landenberg P, Steinbüchel A (2005) Mechanism of lipidbody formation in prokaryotes: how bacteria fatten up. Mol Microbiol 55:750–763

    Article  PubMed  CAS  Google Scholar 

  • Weathers PJ, Allen MM (1978) Variations in short term products of inorganic carbon fixation in exponential and stationary phase cultures of Aphanocapsa 6308. Arch Microbiol 116:231–234

    Article  PubMed  CAS  Google Scholar 

  • Weber J (1989) Nematocysts (stinging capsules of Cnidaria) as Donnan-potentialdominated osmotic systems. Eur J Biochem 184:465–476

    Article  PubMed  CAS  Google Scholar 

  • Weber J (1990) Poly(ρ-glutamic acid)s are the major constituents of nematocysts in Hydra (Hydrozoa, Cnidaria). J Biol Chem 265:9664–9669

    PubMed  CAS  Google Scholar 

  • Wingard LL, Miller SR, Sellker JM, Stenn E, Allen MM, Wood AM (2002) Cyanophycin production in phycoerythrin-containing marine Synechococcus strain of unusual phylogenetic affinity. Appl Environ Microbiol 68:1772–1777

    Article  PubMed  CAS  Google Scholar 

  • Wolk CP, Wojciuch E (1971a) Photoreduction of acetylene by heterocysts. Planta 97:126–134

    Article  CAS  Google Scholar 

  • Wolk CP, Wojciuch E (1971b) Biphasic time course of solubilization of nitrogenase during cavitation of aerobically grown Anabaena cylindrica. J Phycol 8:339–344

    Article  Google Scholar 

  • Yuan X, Xiao S, Taylor TN (2005) Lichen-like symbiosis 600 million years ago. Science 308:1017–1020

    Article  PubMed  CAS  Google Scholar 

  • Ziegler K, Diener A, Herpin C, Richter R, Deutzmann R, Lockau W (1998) Molecular characterization of cyanophycin synthetase, the enzyme catalyzing the biosynthesis of the cyanobacterial reserve material multi-l-arginyl-poly-l-aspartate (cyanophycin). Eur J Biochem 254:154–159

    Article  PubMed  CAS  Google Scholar 

  • Ziegler K, Stephan DP, Pistorius EK, Ruppel HG, Lockau W (2001) A mutant of the cyanobacterium Anabaena variabilis ATCC 29413 lacking cyanophycin synthetase: growth properties and ultrastructural aspects. FEMS Microbiol Lett 196:13–18

    Article  PubMed  CAS  Google Scholar 

  • Ziegler K, Deutzmann R, Lockau W (2002) Cyanophycin synthetase like enzymes of non-cyanobacterial eubacteria: characterization of the polymer produced by a recombinant synthetase of Desulfitobacterium hafniense. Z Naturforsch Sect C 57:522–529

    CAS  Google Scholar 

  • Zuther E, Schubert H, Hagemann M (1998) Mutation of a gene encoding a putative glycoprotease leads to reduced salt tolerance, altered pigmentation, and cyanophycin accumulation in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 180:1715–1722

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Molekulare Mikrobiologie und Biotechnologie, Westfälische Wilhelms-Universität Münster, Corrensstrasse 3, 48149, Münster, Germany

    Martin Obst & Alexander Steinbüchel

Authors
  1. Martin Obst
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexander Steinbüchel
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Genetics and Biochemistry, Clemson University, Clemson, SC, 29634, USA

    Jessup M. Shively (Prof. Emeritus of Biochemistry) (Prof. Emeritus of Biochemistry)

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Obst, M., Steinbüchel, A. (2006). Cyanophycin—an Ideal Bacterial Nitrogen Storage Material with Unique Chemical Properties. In: Shively, J.M. (eds) Inclusions in Prokaryotes. Microbiology Monographs, vol 1. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-33774-1_7

Download citation

Publish with us

Policies and ethics

Search

Navigation