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Heterocyst Differentiation and Nitrogen Fixation in Cyanobacteria

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Associative and Endophytic Nitrogen-fixing Bacteria and Cyanobacterial Associations

Part of the book series: Nitrogen Fixation: Origins, Applications, and Research Progress ((NITR,volume 5))

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References

  • Bauer, C., Scappino, L., and Haselkorn R. (1993). Growth of the cyanobacterium Anabaena on molecular nitrogen: NifJ is required when iron is limited. Proc. Natl. Acad. Sci. USA, 90, 8812-8816.

    Article  PubMed  CAS  Google Scholar 

  • Bauer, C. C., Ramaswamy, K. S., Endley, S., Scappino, L. A., Golden, J. W., and Haselkorn, R. (1997). Suppression of heterocyst differentiation in Anabaena PCC 7120 by a cosmid carrying wild-type genes encoding enzymes for fatty acid synthesis. FEMS Microbiol. Lett., 151, 23-30.

    Article  PubMed  CAS  Google Scholar 

  • Berg, H., Ziegler, K., Piotukh, K., Baier, K., Lockau, W., and 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

    Article  PubMed  CAS  Google Scholar 

  • Berman-Frank, I., Lundgren, P., Chen, Y.-B., Kolber, Z., Bergman, B., and Fakolwski, P. (2001). Segregation of nitrogen fixation and oxygeneic photosynthesis in the marine cyanobacterium Trichodesmium. Science, 294, 1534-1537.

    Article  PubMed  CAS  Google Scholar 

  • Black, K., Buikema, W. J., and Haselkorn R. (1995). The hglK gene is required for localization of heterocyst-specific glycolipids in the cyanobacterium Anabaena PCC 7120. J. Bacteriol., 177, 6440-6448.

    PubMed  CAS  Google Scholar 

  • Black, T. A., and Wolk C. P. (1994). Analysis of a Het– mutation in Anabaena sp. strain PCC 7120 implicates a secondary metabolite in the regulation of heterocyst spacing. J. Bacteriol., 176, 2282-2292.

    PubMed  CAS  Google Scholar 

  • Böhme, H. (1998). Regulation of nitrogen fixation in heterocyst-forming cyanobacteria. Trends Plant Sci., 9, 346-351.

    Article  Google Scholar 

  • Brahamsha, B., and Haselkorn R. (1992). Identification of multiple RNA polymerase sigma factors homologs in the cyanobacterium Anabaena strain 7120: Cloning, expression and inactivation of sigB and sigC genes. J. Bacteriol., 174, 7273-7282.

    PubMed  CAS  Google Scholar 

  • Buikema, W. J., and Haselkorn R. (1991a). Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena 7120. Genes Dev., 5, 321-330.

    CAS  Google Scholar 

  • Buikema, W. J., and Haselkorn R. (1991b). Isolation and complementation of nitrogen fixation mutants of the cyanobacterium Anabaena sp. strain PCC 7120. J. Bacteriol., 173, 1879-1885.

    CAS  Google Scholar 

  • Buikema, W. J., and Haselkorn R. (1993). Molecular genetics of cyanobacterial development. Ann. Rev. Plant Physiol., 44, 33-52.

    Article  CAS  Google Scholar 

  • Buikema, W. J., and Haselkorn R. (2001). Expression of the Anabaena hetR gene from a copper-regulated promoter leads to heterocyst differentiation under repressing conditions. Proc. Natl. Acad. Sci. USA, 98, 2729-2734.

    Article  PubMed  CAS  Google Scholar 

  • Callahan, S. M., and Buikema W. J. (2001). The role of HetN in maintenance of the heterocyst pattern in Anabaena sp. PCC 7120. Mol. Microbiol., 40, 941-950.

    Article  PubMed  CAS  Google Scholar 

  • Cardemil, L., and Wolk C. P. (1979). The polysaccharides from heterocyst and spore envelopes of a blue-green alga: Structure of the basic repeating unit. J. Biol. Chem., 254, 736-741.

    PubMed  CAS  Google Scholar 

  • Chastain, C. J., Brusca, J. S., Ramasubramanian, T. S., Wei, T. F., and Golden, J. W. (1990). A sequence specific DNA-binding factor (VF1) from Anabaena sp. strain PCC 712 vegetative cells binds to three adjacent sites in the xisA upstream region. J. Bacteriol., 172, 5044-5051.

    PubMed  CAS  Google Scholar 

  • Curatti, L., Flores, E., and Salerno G. (2002). Sucrose is involved in the diazotrophic metabolism of the heterocyst-forming cyanobacterium Anabaena sp. FEBS Lett., 513, 175-178.

    Article  PubMed  CAS  Google Scholar 

  • Curatti, L., Porchia, A. C., Herrera-Estrella, L., and Salerno G. L. (2000). A prokaryotic sucrose synthase gene (susA) isolated from a filamentous nitrogen-fixing cyanobacterium encodes a protein similar to those of plants. Planta, 211, 729-735.

    Article  PubMed  CAS  Google Scholar 

  • Dong, Y., Huang, X., Wu, X. Y., and Zhao J. (2000). Identification of the active site of HetR protease and its requirement for heterocyst differentiation in the cyanobacterium Anabaena sp. strain PCC 7120. J. Bacteriol., 182, 1575-1579.

    Article  PubMed  CAS  Google Scholar 

  • Ehira, S., Ohmori, M., and Sato N. (2003). Genome wide expression analysis of the response to nitrogen deprivation in the heterocyst-forming cyanobacterium Anabaena sp. Strain 7120. DNA Res., 30, 97-113.

    Article  Google Scholar 

  • El-Shehawy, R., Lugomela, C., Ernst, A., and Bergman B. (2003). Diurnal expression of hetR and diazocyte development in the filamentous non-heterocystous cyanobacterium Trichodesmium erythraeum. Microbiology, 149, 1139-1146.

    Article  PubMed  CAS  Google Scholar 

  • Elhai, J., and Wolk C. P. (1988). Conjugal transfer of DNA to cyanobacteria. Methods Enzymol., 167, 747-754.

    Article  PubMed  CAS  Google Scholar 

  • Fay, P., Stewart, W. D. P., Walsby, A. E., and Fogg G. E. (1968). Is the heterocyst the site of nitrogen fixation in blue-green algae? Nature, 220, 810-812.

    Article  PubMed  CAS  Google Scholar 

  • Fleming, H., and Haselkorn R. (1973). Differentiation in Nostoc muscorum: Nitrogenase is synthesized in heterocysts. Proc. Natl. Acad. Sci. USA, 70, 2727-2731.

    Article  PubMed  CAS  Google Scholar 

  • Fleming, H., and Haselkorn R. (1974). The program of protein synthesis during heterocyst differentiation in nitrogen-fixing blue-green algae. Cell, 3, 159-170.

    Article  CAS  Google Scholar 

  • Forchhammer, K, and Tandeau de Marsac, N. (1994). The PII protein in the cyanobacterium Synechococcus sp. strain PPC 7942 is modified by serine phosphorylation and signals the cellular N status. J. Bacteriol., 176, 84-91.

    PubMed  CAS  Google Scholar 

  • Frìas, J. E., Flores, E., and Herrero A. (1994). Requirement of the regulatory protein NtcA for the expression of nitrogen assimilation and heterocyst development genes in the cyanobacterium Anabaenasp. PCC 7120. Mol. Microbiol., 14, 823-832.

    Article  PubMed  Google Scholar 

  • Frìas, J. E., Merida,, A., Herrero, A., Martin-Nieto, J., and Flores E. (1993). General distribution of the nitrogen control gene ntcA in cyanobacteria. J. Bacteriol., 175, 5710-5713.

    PubMed  Google Scholar 

  • Gambacorta, A., Soriente, A., Trincone, A., and Sodano G. (1995). Biosynthesis of the heterocyst glycolipids in the cyanobacterium Anabaena cylindrica. Phytochem. (Oxford), 39, 771-774.

    Article  CAS  Google Scholar 

  • Golden, J. W., and Yoon H. S. (1998). Heterocyst formation in Anabaena. Curr. Opin. Microbiol., 1, 623-629.

    Article  PubMed  CAS  Google Scholar 

  • Golden, J. W., Milligan, M. E., and Haselkorn R. (1987). Different recombination site specificity of two developmentally regulated genome rearrangements. Nature, 327, 526-529.

    Article  PubMed  CAS  Google Scholar 

  • Golden, J. W., Robinson, S. J., and Haselkorn R. (1985). Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena. Nature, 314, 419-423.

    Article  PubMed  CAS  Google Scholar 

  • Hai, T., Oppermann-Sanio, F. B., and Steinbuchel 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 

  • Hanson, T. E. K., Forchhammer, K., Tandeau de Marsac, N., and Meeks J. C. (1998). Characterization of the glnB gene product of Nostoc punctiforme strain ATCC 29133: glnB or the PII protein may be essential. Microbiology, 144, 1537-1547.

    Article  PubMed  CAS  Google Scholar 

  • Haselkorn, R., and Buikema W. J. (1992). Nitrogen fixation in cyanobacteria. In G. Stacey, R. H. Burris and H. J. Evans (Eds.), Biological nitrogen fixation (pp. 166-190). New York, NY: Chapman and Hall.

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Herrero, A., Muro-Pastor, A. M., and Flores E. (2001). Nitrogen control in cyanobacteria. J. Bacteriol., 183, 411-425.

    Article  PubMed  CAS  Google Scholar 

  • Jones, K. M., and Haselkorn R. (2002). Newly identified cytochrome c oxidase operon in the nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120 specifically induced in heterocysts. J. Bacteriol., 184, 2491-2499.

    Article  PubMed  CAS  Google Scholar 

  • Kaneko, T., Nakamura, Y., Wolk, C. P., Kuritz, T., Sasamoto, S., Watanabe, A., et al. (2001). Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res., 8, 205-253.

    Article  PubMed  CAS  Google Scholar 

  • Khudyakov, I., and Wolk C. P. (1997). hetC, a gene coding for a protein similar to bacterial ABC protein exporters, is involved in early regulation of heterocyst differentiation in Anabaena sp. strain PCC7120. J. Bacteriol., 179, 6071-6978.

    Google Scholar 

  • Lambein, F., and Wolk C. P. (1973). Structural studies on the glycolipids from the envelope of the heterocyst of Anabaena cylindrica. Biochemistry, 12, 791-798.

    Article  PubMed  CAS  Google Scholar 

  • Lammers, P. J., Golden, J. W., and Haselkorn R. (1986). Identification and sequence of a gene required for a developmentally regulated DNA excision in Anabaena. Cell, 44, 905-911.

    Article  PubMed  CAS  Google Scholar 

  • Liang, J., Scappino, L., and Haselkorn R. (1992). The patA gene product, which contains a region similar to CheY of Escherichia coli, controls heterocyst pattern formation in the cyanobacterium Anabaena 7120. Proc. Natl. Acad. Sci. USA, 89, 5655-5659.

    Article  PubMed  CAS  Google Scholar 

  • Liang, J., Scappino, L., and Haselkorn R. (1993). The patB gene product, required for growth of the cyanobacterium Anabaena sp. strain PCC 7120 under nitrogen-limiting conditions, contains ferredoxin and helix-turn-helix domains. J. Bacteriol., 175, 1697-1704.

    PubMed  CAS  Google Scholar 

  • Liu, D., and Golden J. W. (2002). hetL overexpression stimulates heterocyst formation in Anabaena sp. strain PCC 7120. J. Bacteriol., 184, 6873-6881.

    Article  PubMed  CAS  Google Scholar 

  • Luque, I., Flores, E., and Herrero A. (1994). Molecular mechanism for the operation of nitrogen control in cyanobacteria. EMBO J., 13, 2862-2869.

    PubMed  CAS  Google Scholar 

  • Martin-Figueroa, E., Navarro, F., and Florencio F. J. (2000). The GS-GOGAT pathway is not operative in the heterocysts. Cloning and expression of glsF gene from the cyanobacterium Anabaena sp. PCC 7120. FEBS Lett., 476, 282-286.

    Article  PubMed  CAS  Google Scholar 

  • Mazur, B. J., Rice, D., and Haselkorn R. (1980). Identification of blue-green algal nitrogen fixation genes by using heterologous DNA hybridization probes. Proc. Natl. Acad. Sci. USA, 77, 186-190.

    Article  PubMed  CAS  Google Scholar 

  • Meeks, J. C., and Elhai J. (2002). Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol. Mol. Biol. Rev., 66, 94-121.

    Article  PubMed  CAS  Google Scholar 

  • Meeks, J. C., Wolk, C. P., Thomas, J., Lockau, W., Shaffer, P. W., Austin, S. M., Chien, W.-S., and Galonski A. (1977). The pathways of assimilation of 13NH4 + by the cyanobacterium, Anabaena cylindrica. J. Biol. Chem., 252, 7894-7900.

    PubMed  CAS  Google Scholar 

  • Nagaraja, R., and Haselkorn R. (1984). Protein HU from the cyanobacterium Anabaena. Biochimie, 76, 1082-1089.

    Article  Google Scholar 

  • Orcutt, K., Rassmussen, U., Webb, E., Waterbury, J. B., Gundersen, K, and Bergman, B. (2002). Characterization of Trichodesmium spp. by genetic techniques. Appl. Environ. Microbiol., 68, 2236-2245.

    Article  PubMed  CAS  Google Scholar 

  • Orr, J., and Haselkorn R. (1982). Regulation of glutamine synthetase activity and synthesis in free-living Anabaena and in symbiotic association. J. Bacteriol., 152, 626-635.

    PubMed  CAS  Google Scholar 

  • Orr, J., Keefer, L. M., Keim, P., Nguyen, T. D., Wellems, T., Heinrikson, R. L., and Haselkorn R. (1981). Purification, physical characterization, and NH2-terminal sequence of glutamine synthetase from the cyanobacterium Anabaena 7120. J. Biol. Chem., 256, 13091-13098.

    PubMed  CAS  Google Scholar 

  • Peschek, G. A., Villagraten, K., and Wastyn M. (1991). Respiratory protection of the nitrogenase in dinitrogen-fixing cyanobacteria. Plant Soil, 137, 17-24.

    Article  CAS  Google Scholar 

  • Rice, D., Mazur, B. J., and Haselkorn R. (1982). Isolation and physical mapping of nitrogen fixation genes from the cyanobacterium Anabaena 7120. J. Biol. Chem., 257, 13157-13163.

    PubMed  CAS  Google Scholar 

  • Richter, R., Hejazi, M., Kraft, R., Ziegler, K., and 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 

  • Schmetterer, G., Valladares, A., Pils, D., Steinbach, S., Pacher, M., Muro-Pastor, A. M., et al. (2001). The coxBAC operon encodes a cytochrome c oxidase required for heterotrophic growth in the cyanobacterium Anabaena variabilis strain ATCC 29413. J. Bacteriol., 183, 6429-6434.

    Article  PubMed  CAS  Google Scholar 

  • Thiel, T. (1993). Characterization of genes for an alternative nitrogenase in the cyanobacterium Anabaena variabilis. J. Bacteriol., 175, 6276-6286.

    PubMed  CAS  Google Scholar 

  • Thiel, T., Lyons, E. M., Erker, J. C., and Ernst A. (1995). A second nitrogenase in vegetative cells of a heterocyst-forming cyanobacterium. Proc. Natl. Acad. Sci. USA, 92, 9358-9362.

    Article  PubMed  CAS  Google Scholar 

  • Thomas, J., Meeks, J. C., Wolk, C. P., Shaffer, P. W., Austin, S. M., and Chen, W. S. (1977). Formation of glutamine from [13N]ammonia, [13N]dinitrogen, and [14C]glutamate by heterocysts isolated from Anabaena cylindrica. J. Bacteriol., 129, 1545-1555.

    PubMed  CAS  Google Scholar 

  • Tumer, N. E., Robinson, S. J., and Haselkorn R. (1983). Different promoters for the Anabaena glutamine synthetase gene during growth using molecular or fixed nitrogen. Nature, 306, 337-342.

    Article  CAS  Google Scholar 

  • Valladares, A., Herrero, A., Pils, D., Schmetterer, G., and Flores E. (2003). Cytochrome c oxidase genes required for nitrogenase activity and diazotrophic growth in Anabaena sp. PCC 7120. Mol. Microbiol., 47, 1239-1249.

    Article  PubMed  CAS  Google Scholar 

  • Vargas, W., Cumino, A., and Salerno G. L. (2003). Cyanobacterial alkaline/neutral invertases. Origin of sucrose hydrolysis in the plant cytosol? Planta, 216, 951-960.

    PubMed  CAS  Google Scholar 

  • Wei, T. F., Ramasubramanian, T. S., and Golden J. W. (1994). Anabaena sp. strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development. J. Bacteriol., 176, 4473-4482.

    PubMed  CAS  Google Scholar 

  • Wei, T. F., Ramasubramanian, T. S., Pu, F., and Golden J. W. (1993). Anabaena sp. strain 7120 bifA gene encoding sequence specific DNA-binding protein cloned by in vivo transcriptional interference selection. J. Bacteriol., 175, 4025-4035.

    PubMed  CAS  Google Scholar 

  • Wolk., C. P. (1991). Genetic analysis of cyanobacterial development. Curr. Opin. Genet. Dev., 1, 336-341.

    Article  PubMed  CAS  Google Scholar 

  • Wolk, C. P., Vonshak, A., Kehoe, P., and Elhai J. (1984). Construction of shuttle vectors capable of conjugative transfer from Escherichia coli to nitrogen-fixing filamentous cyanobacteria. Proc. Natl. Acad. Sci. USA, 81, 1561-1565.

    Article  PubMed  CAS  Google Scholar 

  • Yoon, H. S., and Golden J. W. (1998). Heterocyst pattern formation controlled by a diffusible peptide. Science, 282, 935-938.

    Article  PubMed  CAS  Google Scholar 

  • Yoon, H. S., and Golden J. W. (2001). PatS and products of nitrogen fixation control heterocyst pattern. J. Bacteriol., 183, 2605-2613.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, R., Cao, Z., and Zhao J. (1998). Characterization of HetR protein turnover in Anabaena sp. PCC 7120. Arch. Microbiol., 169, 417-423.

    Article  PubMed  CAS  Google Scholar 

  • Ziegler, K., Diener, A., Herpin, C., Richter, R., Deutzmann, R., and 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, D. P., Pistorius, E. K., Ruppel, H. G., and 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 

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  1. Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL 60637, USA

    R Haselkorn

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  1. Institut Pasteur, Paris, France

    Claudine Elmerich

  2. Department of Biochemistry, Virginia Polytechnic Institute and State University, Blacksburg, Virginia, U.S.A

    William E. Newton

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Haselkorn, R. (2007). Heterocyst Differentiation and Nitrogen Fixation in Cyanobacteria. In: Elmerich, C., Newton, W.E. (eds) Associative and Endophytic Nitrogen-fixing Bacteria and Cyanobacterial Associations. Nitrogen Fixation: Origins, Applications, and Research Progress, vol 5. Springer, Dordrecht. https://doi.org/10.1007/1-4020-3546-2_11

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