Cyanophycin
Part 7. Polyamides and Complex Proteinaceous Materials
Dr. Fred Bernd Oppermann-Sanio,
Prof. Dr. Alexander Steinbüchel,
Dr. Fred Bernd Oppermann-Sanio
- [email protected]
- ++49-251-8339823 | Fax: ++49-251-8338388
Institut für Mikrobiologie der Westfälischen Wilhelms-Universität, Corrensstraße 3, Münster, Germany, 48149
Search for more papers by this authorProf. Dr. Alexander Steinbüchel
- [email protected]
- ++49-251-8339821 | Fax: ++49-251-8338388
Institut für Mikrobiologie der Westfälischen Wilhelms-Universität, Corrensstraße 3, Münster, Germany, 48149
Search for more papers by this authorDr. Fred Bernd Oppermann-Sanio,
Prof. Dr. Alexander Steinbüchel,
Dr. Fred Bernd Oppermann-Sanio
- [email protected]
- ++49-251-8339823 | Fax: ++49-251-8338388
Institut für Mikrobiologie der Westfälischen Wilhelms-Universität, Corrensstraße 3, Münster, Germany, 48149
Search for more papers by this authorProf. Dr. Alexander Steinbüchel
- [email protected]
- ++49-251-8339821 | Fax: ++49-251-8338388
Institut für Mikrobiologie der Westfälischen Wilhelms-Universität, Corrensstraße 3, Münster, Germany, 48149
Search for more papers by this authorAbstract
- Introduction
- Historical Outline
- Chemical Structure
- Chemical Analysis and Detection
- Solubility Properties of CGP and Isolation
- Molecular Weight and Structure of CGP
- Quantification of CGP
- Variations in Composition and CGP-like Polymers
- Occurrence
- Occurrence in Cyanobacteria
- Occurrence in Chemotrophic Bacteria
- Functions
- Physiology
- Biochemistry
- Primary Structures and Motifs Occurring in CGP Synthetases
- Assay of CGP Synthetase Activity and Substrate Specificity
- Mechanism of Catalysis
- Molecular Genetics
- Biodegradation
- Intracellular Mobilization
- Extracellular Breakdown
- Biotechnological Production of CGP
- Fermentative Production after Heterologous Expression of cphA in E. coli
- Isolation of CGP
- Fermentative Production after Heterologous Expression of cphA in other Bacteria
- In-Vitro Biosynthesis of CGP
- Outlook and Perspectives
- Patents
References
- Aboulmagd, E., Oppermann-Sanio, F. B., Steinbüchel, A. (2000) Molecular characterization of the cyanophycin synthetase from Synechocystis sp. strain PCC 6308, Arch. Microbiol. 174, 297–306.
- Aboulmagd, E., Oppermann-Sanio, F. B., Steinbüchel, A. (2001a) Purification of Synechocystis sp. strain PCC 6308 cyanophycin synthetase and its characterization with respect to substrate and primer specificity, Appl. Environ. Microbiol. 67, 2176–2182.
- Aboulmagd, E., Voss, I., Oppermann-Sanio, F. B., 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.
- Allen, M. M. (1984) Cyanobacterial cell inclusions, Annu. Rev. Microbiol. 38, 1–25.
- Allen, M. M. (1988) Inclusions: cyanophycin, Methods Enzymol. 167, 207–213.
- Allen, M. M., Hawley, M. A. (1983) Protein degradation and synthesis of cyanophycin granule polypeptide in Aphanocapsa sp., J. Bacteriol. 154, 1480–1484.
- Allen, M. M., Weathers, P. J. (1980) Structure and composition of cyanophycin granules in the cyanobacterium Aphanocapsa 6308, J. Bacteriol. 141, 959–962.
- Allen, M. M., Hutchison, F., Weathers, P. J. (1980) Cyanophycin granule polypeptide formation and degradation in the cyanobacterium Aphanocapsa 6308, J. Bacteriol. 141, 687–693.
- Allen, M. M., Morris, R., Zimmerman, W. (1984) Cyanophycin granule polypeptide protease in a unicellular cyanobacterium, Arch. Microbiol. 138, 119–123.
- Ariño, X., Ortega-Calvo, J. J., 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.
- Ashiuchi, M., Misono, H. (2002) Poly-γ-glutamic acid, in: Biopolymers ( A. Steinbüchel, Ed.), Weinheim, Germany: Wiley-VCH, pp. 123–173, Vol. 7.
- Berg, H., Ziegler, K., Piotukh, K., Baier, K., Lockau, W., Volkmer-Engert, R. (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.
- Bertrand, J. A., Auger, G., Martin, L., Fanchon, E., Blanot, D., Le Beller, D., van Heijenoort, J., Dideberg, O. (1999) Determination of the MurD mechanism through crystallographic analysis of enzyme complexes, J. Mol. Biol. 289, 579–590.
- Borzi, A. (1887) Le comunicazioni intracellulari delle Nostochinee, Malpighia 1, 74–203.
- Byrom, D. (1992) Production of poly-β-hydroxybutyrate–poly-β-hydroxyvalerate copolymers, FEMS Microbiol. Rev. 103, 247–250.
- Carr, N. G. (1988) Nitrogen reserves and dynamic reservoirs in cyanobacteria, in: Biochemistry of the Algae and Cyanobacteria ( L. J. Rogers, J. R. Gallon, Eds.), Oxford: Clarendon Press, 13–21.
- Cunin, R., Glansdorff, N., Piérard, A., Stalon, V. (1986) Biosynthesis and metabolism of arginine in bacteria, Microbiol. Rev. 50, 314–352.
- Dembinska, M. E., Allen, M. M. (1988) Cyanophycin granule size variation in Aphanocapsa, J. Gen. Microbiol. 143, 295–298.
- Dementin, S., Bouhss, A., Auger, G., Parquet, C., Mengin-Lecreulx, D., Dideberg, O., van Heijenoort, J., Blanot, D. (2001) Evidence of a functional requirement for a carbamoylated lysine residue in MurD, MurE and MurF synthetases as established by chemical rescue experiments, Eur. J. Biochem. 268, 5800–5807.
- Eggeling, L., Sahm, H. (1999) L-Glutamate and L-lysine: traditional products with impetuous developments, Appl. Microbiol. Biotechnol. 52, 146–153.
- Erickson, N. A., Kolodny, N. H., Allen, M. M. (2001) A rapid and sensitive method for the analysis of cyanophycin, Biochim. Biophys. Acta 1526, 5–9.
- Eveland, S. S., Pompliano, D. L., Anderson, M. S. (1997) Conditionally lethal Escherichia coli murein mutants contain point defects that map to regions conserved among murein and folyl poly-γ-glutamate ligases: identification of a ligase superfamily, Biochemistry 36, 6223–6229.
- Fogg, G. E. (1951) Growth and heterocyst production in Anabaena cylindrica Lemm. III. The cytology of heterocysts, Ann. Bot. 15, 23–35.
- Frey, K. M., Oppermann-Sanio, F. B., Steinbüchel, A. (2002) Technical scale production of cyanophycin with recombinant strains of Escherichia coli, Appl. Environ. Microbiol. 68, 3377–3384.
- 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.
- Galperin, M. Y., Koonin, E. V. (1997) A diverse superfamily of enzymes with ATP-dependent carboxylate-amine/thiol ligase activity, Protein Sci. 6, 2639–2643.
- Geitler, L. (1932) Cyanophyceae von Europa unter Berücksichtigung der anderen Kontinente, in: Dr. L. Rabenhorst's Kryptogamen-Flora von Deutschland, Östereich und der Schweiz ( R. Kolkwitz, Ed.), Leipzig: Akademische Verlagsgesellschaft, Vol. 14.
- Golecki, J. R., Heinrich, U. R. (1991) Ultrastructural and electron spectroscopic analyses of cyanobacteria and bacteria, J. Microsc. 162, 147–154.
- Gupta, M., Carr, N. G. (1981) Enzyme activities related to cyanophycin metabolism in heterocysts and vegetative cells of Anabaena sp., J. Gen. Microbiol. 125, 17–23.
- Hai, T., Oppermann-Sanio, F. B., Steinbüchel, A. (1999) Purification and characterization of cyanophycin and cyanophycin synthetase from the thermophilic Synechococcus sp. MA19, FEMS Microbiol. Lett. 181, 229–236.
- Hai, T., Ahlers, H., Gorenflo, V., Steinbüchel, A. (2000) Axenic cultivation of anoxygenic phototrophic bacteria, cyanobacteria, and microalgae in a new closed tubular glass photobioreactor, Appl. Microbiol. Biotechnol. 53, 383–389.
- Hai, T., Oppermann-Sanio, F. B., 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.
- Hegler, R. (1901) Untersuchungen über die Organisation der Phycochromaceenzelle, Jahrbücher für wissenschaftliche Botanik 36, 229–354.
- Hejazi, M., Piothukh, K., Mattow, J., Deutzmann, R., Volkmer-Engerts, R., Lockau, W. (2002) Isoaspartyl dipeptidase activity of plant-type asparaginases, Biochem. J. 364, 129–136.
- Howarth, R. W., Cole, J. J. (1985) Molybdenum availability, nitrogen limitation, and phytoplankton growth in natural waters, Science 229, 653–655.
- Joentgen, W., Groth, T., Steinbüchel, A., Hai, T., Oppermann, F. B. (1998) Polyaspartic acid homopolymers and copolymers, biotechnical production and use thereof, International patent application WO 98/39090.
- Krehenbrink, M., Oppermann-Sanio, F.-B., Steinbüchel, A. (2002) Evaluation of non-cyanobacterial genome sequences for occurrence of genes encoding proteins homologous to cyanophycin synthetase and cloning of an active cyanophycin synthetase from Acinetobacter sp. strain DSM 587, Arch. Microbiol. 177, 371–380.
- Lang, N. J. (1968) The fine structure of blue-green algae, Annu. Rev. Microbiol. 22, 15–46.
- Lang, N. J., Simon, R. D., Wolk, C. P. (1972) Correspondence of cyanophycin granules with structured granules in Anabaena cylindrica, Arch. Mikrobiol. 83, 313–320.
- Lawry, N. H., Simon, R. D. (1982) The normal and induced occurrence of cyanophycin inclusion bodies in several blue-green algae, J. Phycol. 18, 391–399.
- Leganés, F., Fernández-Piñas, F., Wolk, C. P. (1998) A transposition-induced mutant of Nostoc ellipsosporum implicates an arginine-biosynthetic gene in the formation of cyanophycin granules and of functional heterocysts and akinetes, Microbiology 144, 1799–1805.
- Li, H., Sherman, D. M., Bao, S., Sherman, L. A. (2001) Pattern of cyanophycin accumulation in nitrogen-fixing and non-nitrogen-fixing cyanobacteria, Arch. Microbiol. 176, 9–18.
- Liotenberg, S., Campbell, D., Rippka, R., Hourmard, J., Tandeau de Marsac, N. (1996) Effect of the nitrogen source on phycobiliprotein synthesis and cell reserves in a chromatically adapting filamentous cyanobacterium, Microbiology 142, 611–622.
- Mackerras, A. H., de Chazal, N. M., Smith, G. D. (1990) Transient accumulation of cyanophycin in Anabaena cylindrica and Synechocystis 6308, J. Gen. Microbiol. 136, 2057–2065.
- Makino, S. I., Uchida, I., Terakado, N., Sasakawa, C., Yoshikawa, M. (1989) Molecular characterization and protein analysis of the cap region, which is essential for encapsulation in Bacillus anthracis, J. Bacteriol. 171, 722–730.
- Merritt, M. V., Sid, S. S., Mesh, L., Allen, M. M. (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.
- Messineo, L. (1966) Modification of the Sakaguchi reaction: spectrophotometric determination of arginine in proteins without previous hydrolysis, Arch. Biochem. Biophys. 117, 534–540.
- Miller, M. M., Lang, N. J. (1968) The fine structure of akinete formation and germination in Cylindrospermum, Arch. Mikrobiol. 60, 303–313.
- Obst, M., Oppermann-Sanio, F. B., 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.
- Oppermann-Sanio, F. B., Hai, T., Aboulmagd, E., Hezayen, F. F., Jossek, S., Steinbüchel, A. (1999) Biochemistry of microbial polyamide metabolism, in: Biochemical Principles and Mechanisms of Biosynthesis and Biodegradation of Polymers ( A. Steinbüchel, Ed.), Weinheim, Germany: Wiley-VCH, 185–193.
- Oppermann-Sanio, F. B., Steinbüchel, A. (2002) Occurrence, functions and biosynthesis of polyamides in microorganisms and biotechnological production, Naturwissenschaften 89, 11–22.
- Page-Sharp, M., Behm, C. A., Smith, G. D. (1998) Cyanophycin and glycogen synthesis in a cyanobacterial Scytonema species in response to salt stress, FEMS Microbiol. Lett. 160, 11–15.
- Pandey, R. K., Talpasayi, E. R. S. (1982) Spore differentiation in relation to certain antibiotics in the blue-green alga Nodularia spumigena Mertens, Z. Allg. Mikrobiol. 22, 191–196.
- Parnas, H., Cohen, D. (1976) The optimal strategy for the metabolism of reserve materials in micro-organisms, J. Theor. Biol. 56, 19–55.
- Quintero, M. J., Muro-Pastor, A. M., Herrero, A., Flores, E. (2000) Arginine catabolism in the cyanobacterium Synechocystis sp. strain PCC 6803 involves the urea cycle and arginase pathway, J. Bacteriol. 182, 1008–1015.
- 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.
- Rippka, R., Stanier, R. Y. (1978) The effects of anaerobiosis on nitrogenase synthesis and heterocyst development by nostocean cyanobacteria, J. Gen. Microbiol. 105, 83–94.
- Rodriguez-Lopez, M., Muñoz Calvo, M. L., Gomez-Acebo, J. (1971) The effect of rifamycins in the ultrastructure of Anacystis montana, J. Ultrastruct. Res. 36, 595–602.
- Sarma, T. A., Khattar, J. I. S. (1986) Accumulation of cyanophycin and glycogen during sporulation in the blue-green alga Anabaena torulosa, Biochem. Physiol. Pflanz. 181, 155–164.
- Schlegel, H. G. (1993) General Microbiology, Cambridge: Cambridge University Press.
- Schwamborn, M. (1998) Chemical synthesis of polyaspartates: a biodegradable alternative to currently used polycarboxylate homo- and copolymers, Polym. Degrad. Stab. 59, 39–45.
- Sherman, D. M., Tucker, D., Sherman, L. A. (2000) Heterocyst development and localization of cyanophycin in N2-fixing cultures of Anabaena sp. PCC 7120 (Cyanobacteria), J. Phycol. 36, 932–941.
- Simon, R. D. (1971) Cyanophycin granules from the blue-green alga Anabaena cylindrica: a reserve material consisting of copolymers of aspartic acid and arginine, Proc. Natl. Acad. Sci. USA 68, 265–267.
- Simon, R. D. (1973a) Measurement of the cyanophycin granule polypeptide contained in the blue-green alga Anabaena cylindrica, J. Bacteriol. 114, 1213–1216.
- Simon, R. D. (1973b) The effect of chloramphenicol on the production of cyanophycin granule polypeptide in the blue-green alga Anabaena cylindrica, Arch Mikrobiol. 92, 115–122.
- Simon, R. D. (1976) The biosynthesis of multi-L-arginyl-poly(L-aspartic acid) in the filamentous cyanobacterium Anabaena cylindrica, Biochim. Biophys. Acta 422, 407–418.
- Simon, R. D. (1987) Inclusion bodies in the cyanobacteria: cyanophycin, polyphosphate, polyhedral bodies, in: The Cyanobacteria ( P. Fay, C. van Baalen, Eds.), Amsterdam: Elsevier, 199–225.
- Simon, R. D., Weathers, P. J. (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.
- Simon, R. D., Lawry, N. H., McLendon, G. L. (1980) Structural characterization of the cyanophycin granule polypeptide of Anabaena cylindrica by circular dichroism and Raman spectroscopy, Biochim. Biophys. Acta 626, 277–281.
- Stephan, D. P., Ruppel, H. G., Pistorius, E. K. (2000) Interrelation between cyanophycin synthesis, L-arginine catabolism and photosynthesis in the cyanobacterium Synechocystis sp. strain PCC 6803, Z. Naturforsch. 55c, 927–942.
- Suarez, C., Kohler, S. J., Allen, M. M., Kolodny, N. H. (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.
- Thoden, J. B., Kappock, T. J., Stubbe, J., Holden, H. M. (1999) Three-dimensional structure of N5-carboxyaminoimidazole ribonucleotide synthetase: a member of the ATP grasp protein superfamily, Biochemistry 38, 15480–15492.
- Tomaselli Feroci, L., Margheri, M. C., Pelosi, E. (1976) Ultrastructure of Spirulina in comparison with Oscillatoria, Zentralbl. Bakteriol. Abt. II 131, 592–601.
- Van Eykelenburg, C. (1980) Ecophysiological studies on Spirulina platensis. Effect of temperature, light intensity and nitrate concentration on growth and ultrastructure, Antonie Van Leeuwenhoek 46, 113–127.
- Von Döhren, H. (2002) Non-ribosomal biosynthesis of linear and cyclic oligopeptides, in: Biopolymers ( A. Steinbüchel, Ed.), Weinheim, Germany: Wiley-VCH, pp. 51–81, Vol. 7.
- Weathers, P. J., Allen, M. M. (1978) Variations in short term products of inorganic carbon fixation in exponential and stationary phase cultures of Aphanocapsa 6308, Arch. Microbiol. 116, 231–234.
- Wingard, L. L., Miller, S. R., Sellker, J. M. L., Stenn, E., Allen, M. M., Wood, A. M. (2002) Cyanophycin production in a phycoerythrin-containing marine Synechococcus strain of unusual phylogenetic affinity, Appl. Environ. Microbiol. 68, 1772–1777.
- Yoshida, T., Hiraki, J., Nagasawa, T. (2002) ɛ-Poly-l-lysine, in: Biopolymers ( A. Steinbüchel, Ed.), Weinheim, Germany: Wiley-VCH, pp. 107–121, Vol. 7.
- 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.
- Ziegler, K., Stephan, D. P., Pistorius, E. K., Ruppel, H. G., 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.
- 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.
Citing Literature
Biopolymers Online: Biology • Chemistry • Biotechnology • Applications
Browse other articles of this reference work:
