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Chapter 4 : Heterocyst Formation in Anabaena

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Abstract:

Heterocysts are differentiated cyanobacterial cells whose principal known function is the fixation of dinitrogen (N), an oxygen (O)-sensitive process, under aerobic conditions. Cyclic AMP, which plays a role in signal transduction in prokaryotes as well as eukaryotes, is present in sp., is responsive to nitrogen deprivation, and can disrupt the normal pattern of heterocyst formation. In sp., nitrate assimilation responds rapidly to nitrogen deprivation. The contiguous genes nirA, encoding nitrite reductase; nrtA, -B, - C, and -D, encoding nitrate transport proteins; and narB, encoding nitrate reductase, are rapidly and strongly induced in response to nitrogen stepdown. The fatty acyl portion of such lipids might be expected to be generated by a fatty acid or polyketide synthase. Indeed, it was found that mutations in closely positioned genes denoted hetN and hgIB (hetM), hgIC, and hgID that encode proteins that show a potential functional relationship to such synthases resulted in a lack of heterocyst envelope glycolipids. By means of a diversity of genetic approaches, including transposon mutagenesis, complementation of mutations induced by UV light and chemicals, response to added cosmids, and site-specific mutagenesis, numerous other genes that participate in differentiation of sp. have been identified. There may be independent regulation of the formation of the glycolipid and polysaccharide portions of the heterocyst envelope and of the (as yet little studied) maturation of the interior of the heterocyst.

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4
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Figures

Image of FIGURE 1
FIGURE 1

Light micrograph of filaments of Anabaena sp. strain PCC 7120. (A to C) Wild-type cells; those in panel C contain constitutively promoted extra copies of the patS gene on a pDU1-based shuttle vector. (D) patS mutant. The cells were grown with (A) and without (B to D) fixed nitrogen. Heterocysts (arrowheads) are absent from the nitrate-grown wild type, are present at semiregular intervals along the filaments of the wild type deprived of fixed nitrogen, are repressed by PatS, and are present in clusters and at abnormally close intervals in the nitrogen-deprived patS mutant. (An electron micrograph of a heterocyst of wild-type Anabaena sp. strain PCC 7120 may be seen in Fig. 6D .) (Reprinted from Yoon and Golden, 1998.)

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4
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Image of FIGURE 2
FIGURE 2

Working model of certain genetic dependency relationships expressed in response to nitrogen stepdown. The thick arrows indicate a likelihood that that which follows the arrow depends upon that which precedes the arrow. For example, ntcA, but not hanA, is required for uptake and reduction of nitrate, which are catalyzed by products of the nirrA-nrtABCD-narB sequence. Both are required for heterocyst formation. Because the hanA gene is preceded by an NtcA-binding site, its transcription may depend upon activity of NtcA. There is suggestive evidence that HanA participates, direcdy or indirectly, in the transcriptional regulation of hetR and that nlcA acts also later in heterocyst differentiation. A hetR mutation prevents both heterocyst formation and (in N. ellipsosporum) akinete formation. The similar phenotypes of hetC and hetP mutants (the two genes map close together) are suggestive of a blockage in a very early step in the differentiation of cells that have been chosen to become heterocysts but, in N. ellipsosponum, no blockage in the formation of akinetes. Beyond the hetC-hetP step, formation of the two layers of the heterocyst envelope and development of the protoplast of the heterocyst appear to proceed independently, except that a combination of completion of the glycolipid layer and enhanced respiration may lead to microaerobic conditions in the protoplast, and microaerobiosis is required for such late biochemical changes as the appearance of nitrogenase activity, hep genes may also be active during formation of the akinete envelope (Leganés, 1994; Wolk et al, 1994). Where patS falls in this scheme is unclear. Thin curved arrows marked a to d refer to regulation that is probable (a), demonstrated (b), and possible (c and d). Temporal relationships, e.g., that in any particular region of the heterocyst envelope, glycolipid deposition follows polysaccharide deposition and that nitrogenase activity follows excisase activity, are not direcdy illustrated (for references, see the text). An earlier version of this model has appeared (Wolk et al., 1999).

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4
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Image of FIGURE 3
FIGURE 3

Localization of expression of helR, visualized as hetR:: luxAB transcriptional fusions in the presence (A to D) and absence (E and F) of intact helR after 0 (A and E), 3.5 (B), 6, (C), and 24 (D and F) h of deprivation of fixed nitrogen in Anabaena sp. strain PCC 7120. In panel D, the arrows indicate mature heterocysts that appear nonluminescent due, at least in part, to a decrease in the concentration of O. a substrate of luciferase, within the heterocyst ( ). In each panel, the upper image is a bright-field micrograph with an instrumentally generated honeycomb background and the lower image represents luminescence integrated for 20 min. Bar. 10 µm. (Reproduced from , with permission.)

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4
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Image of FIGURE 4
FIGURE 4

Heterocyst envelope glycolipids of Anabaena sp. strain PCC 7120.

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4
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Image of FIGURE 5
FIGURE 5

Composite structure of the probable repeating element of heterocyst envelope polysaccharides from A. cylindrica (a), A. variabilis (b), and Cylindrospermum sp. (c). The anomeric configurations of the linkages and the locations of particular side branches have been determined only for A. cylindrica. The dashes correspond to linkages that are present in only some of the positions indicated.

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4
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Image of FIGURE 6
FIGURE 6

Electron micrographs of the wild type (A and B) and hep A mutant DR1069 (C and D) of Anabaena sp. strain PCC 7120. (A and B) In a heterocyst (H) of wild-type Anabaena sp. strain PCC 7120, the laminated layer of glycolipids (GL) is enveloped by a layer of polysaccharide (PS). In contrast, the only envelope layer seen in heterocysts of the hepA mutant (C) is the laminated layer of glycolipids. (D) Enlargement of box in panel C. V, vegetative cell. (Panels A and B are reproduced from Zhu et al., 1998, with permission.)

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4
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References

/content/book/10.1128/9781555818166.chap4
1. Adams, D. G.,, and N. G. Carr. 1981. Heterocyst differentiation and cell division in the cyanobacter-ium Anabaena cylindrical effect of high light intensity./ Cell Set. 49:341352.
2. Altschul, S. F.,, T. L. Madden,, A. A. Schafler,, J. Zhang,, Z. Zhang,, W. Miller,, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:33893402.
3. Bateman, A.,, A. G. Murzin,, and S. A. Tcich-tnann. 1998. Stracture and distribution of penta-peptide repeats in bacteria. Protein Sci. 7: 14771480.
4. Bauer, C. C.,, W. J. Buikema,, K. Black,, and R. Haselkorn. 1995. A shon-filament mutant of Anabaena sp. strain PCC 7120 that fragments in nitrogen-deficient medium. J. Bacterial. 177:15201526.
5. Bauer, C. C.,, K. S. Ramaswamy,, S. Endley,, L. A. Scappino,, J. W. Golden,, and R. Haselkorn. 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. 151:2330.
6. Black, K.,, W. Buikema,, and R. Haselkorn. 1995. The hglK gene is required for localization of hetero-cyst-specific glycolipids in the cyanobacterium Anabaena sp. strain PCC 7120. J. Bacterid. 177: 64406448.
7. Black, T. A.,, and C. P. Wolk. 1994. Analysis of a Het- mutation in Anabaena sp. strain PCC 7120 implicates a secondary metabolite in the regulation of heterocyst spacing J. Bacteriol 176:22822292.
8. Black, T. A.,, Y. Cai,, and C. P. Wolk. 1993. Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena. Mol. Microbiol. 9:7784.
9. Böhme, H. 1998. Regulation of nitrogen fixation in heterocyst-forming cyanobacteria. Trends Plant Sci. 3:346351.
10. Bradley, S.,, and N. G. Carr. 1977. Heterocyst development in Anabaena cylindrica: the necessity for light as an initial trigger and sequential stages of commitment. J. Cen. Microbiol. 101:291297.
11. Brahamsha, B.,, and R. Haselkorn. 1991. Isolation and characterization of the gene encoding the principal sigma factor of the vegetative cell RNA polymerase from the cyanobacterium Anabaena sp. strain PCC 7120J. Bacterid. 173:24422450.
12. Brahamsha, B.,, and R. Haselkorn. 1992. Identification of multiple RNA polymerase sigma factor homologs in the cyanobacterium Anabaena sp. strain PCC 7120: cloning, expression, and inactiva-tion of the sigB and sigC genes. J. Bacteriol. 174: 72737282.
13. Buikema, W.J.,, and R. Haselkorn. 1991. Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena 7120. Genes Dev. 5:321330.
14. Buikema, W. J.,, and R. Haselkorn. 1993. Molecular genetics of cyanobacterial development. Anmi. Rev. Plant Physiol. Plant Mol. Biol. 44:3352.
15. Cai, Y.,, and C. P. Wolk. 1997a. Nitrogen deprivation of Anabaena sp. strain PCC 7120 elicits rapid activation of a gene cluster that is essential for uptake and utilization of nitrate. J. Bacterial. 179: 258266.
16. Cai, Y.,, and C. P. Wolk. 1997b. Anabaena sp. strain PCC 7120 responds to nitrogen deprivation with a cascade-like sequence of transcriptional activations. J. Bacterial. 179:267271.
17. Campbell, D.,, J. Houmard,, and N. Tandeau de Marsac. 1993. Electron transport regulates cellular differentiation in the filamentous cyanobacterium Calothrix. Plant Cell 5:451463.
18. Campbell, E. L.,, K. D. Hagen,, M. F. Cohen,, M. L. Summers,, and J. C. Meeks. 1996. The devR gene product is characteristic of receivers of two-component regulatory systems and is essential for heterocyst development in the filamentous cyanobacterium Nostoc sp. strain ATCC 29133. J. Bacteriol. 178:20372043.
19. Campbell, E. L.,, M. F. Cohen,, and J. C. Meeks. 1997. A polyketide-synthase-like gene is involved in the synthesis of heterocyst glycolipids in Nostoc punctiforme strain ATCC 29133. Arch. Microbiol. 167:251258.
20. Cardemil, L.,, and C. P. Wolk. 1979. The polysaccharides from heterocyst and spore envelopes of a blue-green alga. Structure of the basic repeating unit. J. Biol. Chan. 254:736741.
21. Cardemil, L.,, and C. P. Wolk. 1981a. The polysaccharides from the envelopes of heterocysts and spores of the blue-green algae Anabaena variabilis and Cylindrospennnm liclienifonne. J. Pitycol. 17: 234240.
22. Cardemil, L.,, and C. P. Wolk. 1981b. Isolated heterocysts of Anabaena variabilis synthesize envelope polysaccharide. Biocliim. Biophys. Acta 674: 265276.
23. Carrasco, C. D.,, and J. W. Golden. 1995. Two heterocyst-specific DNA rearrangements of nif operons in Anabaena cylindrica and Nostoc sp. strain Mac. Microbiology 141:24792487.
24. Carrasco, C. D.,, J. A. Buettner,, and J. W. Golden. 1995. Programed DNA rearrangement of a cyanobacterial hupL gene in heterocysts. Proc. Natl. Acad. Sci. USA 92:791795.
25. Chastain, C. J.,, J. S. Brusca,, T. S. Ramasubramanian,, T.-F. Wei,, and J. W. Golden. 1990. A sequence-specific DNA-binding factor (VF1) from Anabaena sp. strain PCC 7120 vegetative cells binds to three adjacent sites in the xisA upstream region. J. Bacterid. 172:50445051.
26. Davey, M. W.,, and F. Lambein. 1992a. Semiprepararive isolation of individual cyanobacterial heterocyst-type glycolipids by reverse-phase high-performance liquid chromatography. Anal. Biochem. 206:226230.
27. Davey, M. W.,, and F. Lambein. 1992b. Quantitative derivatization and high-performance liquid chromatographic analysis of cyanobacterial heterocyst-type glycolipids. Anal. Biochem. 206:323327.
28. Doherty, H. M.,, and D. G. Adams. 1995. Cloning and sequence of ftsZ and flanking regions from the cyanobacterium Anabaena PCC 7120. Gene 163: 9396.
29. Elhai, J.,, and C. P. Wolk. 1990. Developmental regulation and spatial pattern of expression of the structural genes for nitrogenase in the cyanobacterium Anabaena. EMBO J. 9:33793388.
30. Elhai, J.,, and C. P. Wolk. 1991. Hierarchical control by oxygen in heterocysts of Anabaena, abstr. 114B. In Abstracts of the 7th International Symposium on Photosynthetic Prokaryotes..
31. Elhai, J.,, A. V. Matveyev,, and C. S. Nielsen. 1998. Two-stage model of patterned heterocyst differentiation in Anabaena, abstr. 157. In Abstracts of the 6th Cyanobacterid Workshop..
32. Ernst, A.,, and C. P. Wolk. Unpublished observations.
33. Ernst, A.,, T. Black,, Y. Cai,, J.-M. Panoff,, D. N. Tiwari,, and C. P. Wolk. 1992. Synthesis of nitrogenase in mutants of the cyanobacterium Anabaena sp. strain PCC 7120 affected in heterocyst development or metabolism. J. Bacteriol. 174:60256032.
34. Fay, P. 1969. Metabolic activities of isolated spores of Anabaena cylindrica. J. Exp. Bot. 20:100109.
35. Fay, P.,, W. D. P. Stewart,, A. E. Walsby,, and G. E. Fogg. 1968. Is the heterocyst the site of nitrogen fixation in blue-green algae? Nature (London) 220: 810812.
36. Fernández-Pifias, F.,, and C. P. Wolk. 1994. Expression of luxCD-E in Anabaena sp. can replace the use of exogenous aldehyde for in vivo localization of transcription by luxAB. Gene 150:169174.
37. Fernández-Piñas, F.,, F. Leganés,, and C. P. Wolk. 1994. A third genetic locus required for the formation of heterocysts in Anabaena sp. strain PCC 7120. J. Bacterial. 176:52775283.
38. Fiedler, G.,, M. Arnold,, S. Hannus,, and I. Malde-ner. 1998. The DevliCA exporter is essential for envelope formation in heterocysts of the cyano-bacterium Anabaena sp. strain PCC 7120. Mol. Microbiol. 27:11931202.
39. Florencio, F. J.,, M. Garcia-Dominguez,, E. Mar-tin-Figueroa, andj. L. Crespo. 1998. The GS-GOGAT pathway in cyanobacteria. Regulation and complexity of a central metabolic route, abstr. A16. In Abstracts of the 6th Cyanobacterial Workshop..
40. Fogg, G. E. 1949. Growth and heterocyst production in Anabaena cylindrica Lemm. II. In relation to carbon and nitrogen metabolism. Ann. Bot. N. Ser. 13:241259.
41. Frias, J. E.,, E. Flores,, and A. Herrero. 1994. Requirement of the regulatory protein NtcA for the expression of nitrogen assimilation and heterocyst development genes in the cyanobacterium Anabaena sp. PCC 7120. Mol. Microbiol. 14:823832.
42. Frias, J. E.,, E. Flores,, and A. Herrero. 1997. Nitrate assimilation gene cluster from the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. J. Bacteriol. 179:477486.
43. Gambacorta, A.,, I. Romano,, A. Trincone,, A. Soriente,, M. Giordano,, and G. Sodano. 1996. Heterocyst glycolipids from five nitrogen-fixing cyanobacteria. Gazz. Chim. Ital. 126:653656.
44. Gambacorta, A.,, E. Pagnotta,, I. Romano,, G. Sodano,, and A. Trincone. 1998. Heterocyst glycolipids from nitrogen-fixing cyanobacteria other than Nostocaceae. Phytochemistry 48:801805.
45. Geitler, L. 1932. Cyanophyceae, Aufl. 2. Akademische Verlagsgesellschaft, Leipzig, Germany.
46. Giddings, T. H.,, and L. A. Staehelin. 1981. Observation of microplasmodesmata in both heterocystforming and non-heterocyst forming filamentous cyanobacteria by freeze-fracture electron microscopy. Arch. Microbiol. 129:295298.
47. Golden, J., 1998. Programmed DNA rearrangements in cyanobacteria, p. 162173. In F. J. de Bruijn,, J. R. Lupski,, and G. M. Weinstock (ed.), Bacterial Genomes Physical Stntctiire and Analysis. Chapman and Hall, New York, N.Y..
48. Golden, J. W.,, S. J. Robinson,, and R. Haselkorn. 1985. Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena. Nature 314:419423.
49. Golden, J. W.,, C. D. Carrasco,, M. E. Mulligan,, G.J. Schneider,, and R. Haselkorn. 1988. Deletion of a 55-kilobase-pair DNA element from the chromosome during heterocyst differentiation of Anabaena sp. strain PCC 7120. J. Bacteriol. 170: 50345041.
50. Hager, K.-P.,, G. Dannebcrg,, and H. Bothe. 1983. The glutamate synthase in heterocysts of Nostoc muscorum. FEMS Microbiol. Lett. 17:179183.
51. Haselkorn, R. 1978. Heterocysts. Annu. Rev. Plant Physiol. 29:319344.
52. Haselkorn, R. 1992. Developmentally regulated gene rearrangements in prokaryotes. Annu. Rev. Genet. 26:111128.
53. Haselkorn, R., 1995. Molecular genetics of nitrogen fixation in photosynthetic prokaryotes, p. 2936. In I. A. Tikhonovich,, N. A. Provogov,, V. I. Romanov,, and W. E. Newton (ed.). Nitrogen Fixation: Fundamentals and Applications. Kluwer Academic Publishers, Dordrecht, The Netherlands.
54. Haselkorn, R.,, and W.J. Buikema,. 1992. Nitrogen fixation in cyanobacteria, p. 166190. In G. Stacey,, R. H. Uurris,, and H. J. Evans (ed.), Biological Nitrogen Fixation. Chapman and Hall, New York, N.Y..
55. Haselkorn, R.,, D. Rice,, S. E. Curtis,, and S. J. Robinson. 1983. Organization and transcription of genes important in Anabaena heterocyst differentiation. Ann. Microbiol. 134B:181193.
56. Helber, J. T.,, T. R. Johnson,, L. R. Yarbrough,, and R. Hirschberg. 1988. Regulation of nitrogenase gene expression in anaerobic cultures of Anabaena variabilis. J. Bacteriol. 170:552557.
57. Holland, D.,, and C. P. Wolk. 1990. Identification and characterization of hetA, a gene that acts early in the process of morphological differentiation of heterocysts. J. Bacteriol. 172:31313137.
58. Hopwood, D. A.,, C. Khosla,, D. H. Sherman,, M. J. Bibb,, S. Ebert-Khosla,, E.-S. Kim,, R. McDaniel,, W. P. Revill,, R. Torres,, and T. W. Yu,. 1993. Toward an understanding of the programming of aromatic polyketide synthases: a genetics-driven approach. In R. H. Daltz,, G. D. Hegeman,, and P. L. Skatrud (ed.). Industrial Microorganisms: Basic and Applied Molecular Genetics. American Society for Microbiology, Washington, D. C..
59. Janson, S.,, A. Matvayev,, and B. Bergman. 1998. The presence and expression of hetR in the non-heterocystous cyanobacterium Symploca PCC 8002. FEMS Microbiol. Lett. 168:173179.
60. Jiang, F.,, B. Mannervik,, and B. Bergman. 1997. Evidence for redox regulation of the transcription factor NtcA, acting both as an activator and a repressor, in the cyanobacterium Anabaena PCC 7120. Biochem. J. 327:513517.
61. Katayama, M.,, and M. Ohmori. 1997. Isolation and characterization of multiple adenylate cyclase genes from the cyanobacterium Anabaena sp. strain PCC 7120. J. Bacteriol. 179:35883593.
62. Katayama, M.,, Y. Wada,, and M. Ohmori. 1995. Molecular cloning of the cyanobacterial adenylate cyclase gene from the filamentous cyanobacterium Anabaena cylindrica. J. Bacteriol. 177:38733878.
63. Khudyakov, I.,, and C. P. Wolk. Unpublished observations.
64. Khudyakov, I.,, and C. P. Wolk. 1996. Evidence that the hanA gene coding for HU protein is essential for heterocyst differentiation in, and cyano-phage A-4(L) sensitivity of, Anabaena sp. strain PCC 7120. J. Bacteriol. 178:35723577.
65. Khudyakov, I.,, and C. P. Wolk. 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 PCC 7120. J. Bacteriol 179:69716978.
66. Khudyakov, I. Y.,, and J. W. Golden. 1998. Involvement of group 2 alternative sigma factors in the regulation of diazotrophic growth of Anabaena sp. PCC 7120, abstr. B20. In Abstracts of the 6th Cyanobacterial Workshop..
67. Koksharova, O.,, and C. P. Wolk.Unpublished observations.
68. Kotani, H.,, and S. Tabata. 1998. Lessons from sequencing of the genome of a unicellular cyanobacterium, Synechocystis sp. PCC6803. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49:151171.
69. Kuritz, T.,, A. Ernst,, T. A. Black,, and C. P. Wolk. 1993. High-resolution mapping of genetic loci of Anabaena PCC 7120 required for photosynthesis and nitrogen fixation. Mol. Microbiol. 8:101110.
70. Lambelot, R. H.,, A. M. Gehring,, R. S. Flugel,, P. Zuber,, M. LaCelle,, M. A. Marabiel,, R. Reid,, C. Khosla,, and C. T. Walsh. 1996. A new enzyme superfamily—the phosphopantetheinyl transferases. Chem. Biol. 3:923936.
71. Lcganés, F. 1994. Genetic evidence that hepA gene is involved in the normal deposition of the envelope of both heterocysts and akinetes in Anabaena variabilis ATCC 29413. FEMS Microbiol. Lett. 123: 6367.
72. Leganés, F.,, F. Fernández-Piñas,, and C. P. Wolk. 1994. Two mutations that block heterocyst differentiation have different effects on akinete differentiation in Nostoc ellipsosporum. Mol. Microbiol. 12: 679684.
73. Leganés, F.,, F. Fernández-Piñas,, and C. P. Wolk. 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 144:17991805.
74. Liang, J.,, L. Scappino,, and R. Haselkorn. 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. Set. USA 89: 56555659.
75. Liang, J.,, L. Scappino,, and R. Haselkorn. 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. 175:16971704.
76. Luque, I.,, E. Flores,, and A. Herrero. 1994. Molecular mechanism for the operation of nitrogen control in cyanobacteria. EMBO J. 13:28622869.
77. Lynn, M. E.,, J. A. Bantlc,, and J. D. Ownby. 1986. Estimation of gene expression in heterocysts of Anabaena variabilis by using DNA-RNA hybridization. J. Bacteriol. 167:940946.
78. Maldener, I.. Personal communication.
79. Maldener, I.,, G. Fiedler,, A. Ernst,, F. Fernández-Piñas,, and C. P. Wolk. 1994. Characterization of devA, a gene required for the maturation of proheterocysts in the cyanobacterium Anabaena sp. strain PCC 7120. J. Bacteriol. 176:75437549.
80. Matveyev, A. V.,, E. Rutgers,, E. Soderback,, and B. Bergman. 1994. A novel genome rearrangement involved in heterocyst differentiation of the cyanobacterium Anabaena sp. PCC 7120. FEMS Microbiol. Lett. 116:201208.
81. Meeks, J. C.. Personal communication.
82. Meeks, J. C.,, E. L. Campbell,, and P. S. Bisen. 1994. Elements interrupting nitrogen fixation genes in cyanobacteria: presence and absence of a nifD element in clones of Nostoc sp. strain Mac. Microbiology 140:32253232.
83. Mitcbison, G. J.,, and M. Wilcox. 1972. Rule governing cell division in Anabaena. Nature (London) 239:110111.
84. Mitchison, G. J.,, M. Wilcox,, and R. J. Smith. 1976. Measurement of an inhibitory zone. Science 191:866868.
85. Muro-Pastor, M. I.,, and F. J. Florencio. 1994. NADP+-isocitrate dehydrogenase from the cyanobacterium Anabaena sp. strain PCC 7120: purification and characterization of the enzyme and cloning, sequencing, and disruption of the icd gene. J. Bacteriol. 176:27182726.
86. Muro-Pastor, A.,, A. Valladares,, M. F. Vazquez,, A. Herrero,, and E. Flores. 1998. The cyanobacterial NtcA regulon: role of NtcA in heterocyst development, abstr. S22. In Abstracts of the 6th Cyanobacterial Workshop..
87. Murry, M. A.,, and C. P. Wolk. 1989. Evidence that the barrier to the penetration of oxygen into heterocysts depends upon two layers of the cell envelope. Arch. Microbiol. 151:469474.
88. Oxelfelt, F.,, P. Tamagnini,, and P. Lindblad. 1998. Hydrogen uptake in Nostoc sp. strain PCC 73102. Cloning and characterization of a hupSL homologue. Arch. Microbiol. 169:267274.
89. Peschek, G. A.,, M. Wastyn,, S. Fromwald,, and B. Mayer. 1995a. Occurrence of heme O in photoheterotrophically growing, semi-anaerobic cyanobacterium Synechocysiis sp. PCC6803. FEBS Lett. 371:8993.
90. Peschek, G. A.,, D. Algc,, S. Fromwald,, and B. Mayer. 1995b. Transient accumulation of heme O (cytochrome o) in the cytoplasmic membrane of semi-anaerobic Auacystis nidulans. Evidence for oxygenase-catalyzed heme O/A transformation. J. Biol. Client. 270:2793727941.
91. Peterson, R. B.,, and C. P. Wolk. 1978. High recovery of nitrogenase activity and of *sFe-labeled nitrogenase in heterocysts isolated from Anabaena variabilis. Proc. Nalt. Acad. Sci. USA 75:62716275.
92. Porchia, A. .,, and G. L. Salerno. 1996. Sucrose biosynthesis in a prokaryotic organism: presence of two sucrose-phosphate synthases in Anabaena with remarkable differences compared with the plant enzymes. Prot. Natl. Acad. Sci. USA 93:1360013604.
93. Ramasubramanian, T. S.,, T.-F. Wei,, and J. W. Golden. 1994. Two Anabaena sp. strain PCC 7120 DNA-binding factors interact with vegetative celland heterocyst-specific genes. J. Bacteriol. 176: 12141223.
94. Ramasubramanian, T. S.,, T.-F. Wei,, A. K. Oldham,, and J. W. Golden. 1996. Transcription of the Anabaena sp. strain PCC 7120 ntcA gene: multiple transcripts and NtcA binding. J. Bacteriol. 178: 922926.
95. Ramaswamy, K. S.,, C. D. Carrasco,, T. Fatma,, and J. W. Golden. 1997. Cell-type specificity of the Anabaena fdxN-element rearrangement requires xisH and xisI. Mol. Microbiol. 23:12411249.
96. Sato, N.,, and A. Wada. 1996. Disruption analysis of the gene for a cold-regulated KNA-binding protein, rbpA I, in Anabaena: cold-induced initiation of the heterocyst differentiation pathway. Plant Cell Physiol.37:11501160.
97. Schilling, N.,, and K. Ehrnsperger. 1985. Cellular differentiation of sucrose metabolism in Anabaena variabilis. Z. Naturforsch. 40c:776779.
98. Schrautemeier, B.,, U. Nevcling,, and S. Schmitz. 1995. Distinct and differently regulated Mo-dependent nitrogen-fixing systems evolved for heterocysts and vegetative cells of Anabaena variabilis ATCC 29413: characterization of the fdxH 1/2 gene regions as part of the nifl/2 gene clusters. Mol. Microbiol. 18:357369.
99. Smith, G.,, and J. D. Ownby. 1981. Cyclic AMP interferes with pattern formation in the cyanobacterium Anabaena variabilis. J.:EMS Microbiol. Lett. 11: 175180.
100. Soriente, A.,, G. Sodano,, A. Gambacorta,, and A. Trincone. 1992. Structure of the "heterocyst glycolipids" of the marine cyanobacterium Nodtilaria harveyana. Tetrahedron 48:53755384.
101. Soriente, A.,, A. Gambacorta,, A. Trincone,, C. Sili,, M. Vincenzini,, and G. Sodano. 1993. Heterocyst glycolipids of the cyanobacterium Cyanospira rippkae. Phytocheniistry 33:393396.
102. Soriente, A.,, T. Bisogno,, A. Gambacorta,, I. Romano,, C. Sili,, A. Trincone,, and G. Sodano. 1995. Reinvestigation of heterocyst glycolipids from the cyanobacterium, Anabaena cylindrica. Phytochemistry 38:641645.
103. Stragier, P.,, and R. Losick. 1996. Molecular genetics of spomlation in Bacillus subtilis. Annu. Rev. Genet. 30:297341.
104. Summers, M. L.,, J. G. Wallis,, E. L. Campbell,, and J. C. Meeks. 1995. Genetic evidence of a major role for glucose-6-phosphate dehydrogenase in nitrogen fixation and dark growth of the cyanobacterium iYoifofsp. strain ATCC 29133. J. Bacteriol. 177:61846194.
105. Sutherland, J. M.,, W. D. P. Stewart,, and M. Herdman. 1985. Akinetes of the cyanobacterium Nostoc PCC 7524: morphological changes during synchronous germination. Arch. Microbiol. 142: 269274.
106. Thiel, T. 1993. Characterization of genes for an alternative nitrogenase in the cyanobacterium Anabaena variabilis. J. Bacteriol. 175:62766286.
107. Thiel, T., 1994. Genetic analysis of cyanobacteria, p. 581611. In D. A. Bryant (ed.), The Molecular Biology of Cyanobacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands.
108. Thiel, T. 1996. Isolation and characterization of the vnfEN genes of the cyanobacterium Anabaena variabilis. J. Bacteriol. 178:44934499.
109. Thiel, T.,, E. M. Lyons,, J. C. Erkcr,, and A. Ernst. 1995. A second nitrogenase in vegetative cells of a heterocyst-fomiing cyanobacterium. Proc. Natl. Acad. Sci. USA 92:93589362.
110. Thiel, T.,, E. M. Lyons,, and J. C. Erker. 1997. Characterization of genes for a second Mo-dependent nitrogenase in the cyanobacterium Anabaena variabilis. J. Bacteriol. 179:52225225.
111. Thomas, J.,, J. C. Meeks,, C. P. Wolk,, P. W. Shaffer,, S. M. Austin,, and W.-S. Chien. 1977. Formation of glutamine from [13N]ammonia, | uN)dinitrogen, and [14C|glutamate by heterocysts isolated from Anabaena cylindrica. J. Bacteriol. 129:15451555.
112. Turner, N. E.,, S.J. Robinson,, and R. Haselkorn. 1983. Different promoters for the Anabaena glutamine synthetase gene during growth using molecular or fixed nitrogen. Nature (London) 306:337342.
113. Walsby, A. E. 1985. The pemieability of heterocysts to the gases nitrogen and oxygen. Proc. R. Soc. Land. B 226:345366.
114. Wei, T.-F.,, T. S. Ramasubramanian,, and J. W. Golden. 1994. Anabaena sp. strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development. J. Bacteriol. 176:44734482.
115. Wilcox, M. 1970. One-dimensional pattern found in blue-green algae. Nature (London) 228:686687.
116. Wilcox, M.,, G. J. Mitchison,, and R. J. Smith. 1973a. Pattern formation in the blue-green alga, Anabaena. I. Basic mechanisms. J. Cell Sci. 12: 707725.
117. Wilcox, M.,, G. J. Mitchison,, and R. J. Smith. 1973b. Pattern formation in the blue-green alga, Anabaena. II. Controlled proheterocyst regression. J. Cell Set. 13:637649.
118. Wilcox, M.,, G. J. Mitchison,, and R. J. Smith. 1975. Mutants of Anabaena cylindrica altered in heterocyst spacing. Arch. .Microbiol. 103:219223.
119. Winkcnbach, F.,, and C. P. Wolk. 1973. Activities of enzymes of the oxidative and the reductive pentose phosphate pathways in heterocysts of a blue-green alga. Plant Physiol. 52:480482.
120. Winkcnbach, F.,, C. P. Wolk,, and M. Jost. 1972. Lipids of membranes and of the cell envelope in heterocysts of a blue-green alga. Planta 107:6980.
121. Wolk, C. P. 1964. Experimental studies on the development of a blue-green alga. Ph.D. thesis. Rockefeller Institute, New York, N.Y..
122. Wolk, C. P. 1967. Physiological basis of the pattern of vegetative growth of a blue-green alga. Proc. Natl. Acad. Sci. USA 57:12461251.
123. Wolk, C. P. 1968. Movement of carbon from vegetative cells to heterocysts in Anabaena cylindrica. J. Bacteriol. 96:21382143.
124. Wolk, C. P. 1973. Physiology and cytological chemistry of blue-green algae. Bacteriol. Rev. 37:32101.
125. Wolk, C. P., 1982. Heterocysts, p. 359386. In N. G. Can,, and B. A. Whitton (ed.). The Biology of Cyanobacteria. Blackwell, Oxford, United Kingdom.
126. Wolk, C. P. 1991. Genetic analysis of cyanobacterial development. Chit. Opin. Genet. Dev. 1:336341.
127. Wolk, C. P. 1996. Heterocyst fonnation. Aunu. Rev. Genet. 30:5978.
128. Wolk, C. P.,, and R. Kong. Unpublished observations.
129. Wolk, C. P.,, and M. P. Quine. 1975. Formation of one-dimensional patterns by stochastic processes and by filamentous blue-green algae. Dev. Biol. 46: 370382.
130. Wolk, C. P.,, and K. Zarka,. 1998. Genetic dissection ofheterocyst differentiation, p. 191196. In G. Su-bramanian,, B. D. Kaushik,, and G. S. Venkataraman (ed.), Cyanobacterial Biotechnology. Proceedings of the International Symposium, Sept. 18-21, 1996. Oxford and 1BH Publishing Co., New Delhi, India.
131. Wolk, C. P.,, Y. Cai,, L. Cardemil,, E. Florcs,, B. Hohn,, M. Murry,, G. Schmetterer,, B. Schrautemeier,, and R. Wilson. 1988. Isolation and complementation of mutants of Anabaena sp. strain PCC 7120 unable to grow aerobically on dinitrogen. J. Bacteriol. 170:12391244.
132. Wolk, C. P.,, J. Elhai,, T. Kuritz,, and D. Holland. 1993. Amplified expression of a transcriptional pattern formed during development of Anabaena. Mot. Microbiol. 7:441445.
133. Wolk, C. P.,, A. Ernst,, and J. Elhai. 1994. Heterocyst metabolism and development, p. 769823. In D. Bryant (ed.), Molecular Generics of Cyanobacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands.
134. Wolk, C. P.,, J. Zhu,, and R. Kong,. 1999. Genetic analysis ofheterocyst formation, p. 509515. In G. A. Peschek,, W. Loffclhardt,, and G. Peschek (ed.), 'the Prototrophic Prokaryotes. Kluwer Academic Publishers, New York, N.Y..
135. Xu, X.. Personal communication.
136. Xu, X.,, and C. P. Wolk. Unpublished observations.
137. Xu, X.,, I. Khudyakov,, and C. P. Wolk. 1997. Lipopolysaccharide dependence of cyanophage sensitivity and aerobic nitrogen fixation in Anabaena sp. strain PCC 7120 J. Bacteriol. 179:28842891.
138. Yoon, H.-S.,, and J. W. Golden. 1998. Heterocyst pattern formation controlled by a diffusible peptide. Science 282:935938.
139. Zhang, C.-C. 1993. A gene encoding a protein related to eukaryotic protein kinases from the filamentous heterocystous cyanobacterium Anabaena PCC 7120. Proc. Natl. Acad. Sci. USA 90:1184011844.
140. Zhang, C.-C. 1996. Bacterial signalling involving eukaryotic-type protein kinases. AM Microbiol. 20: 915.
141. Zhang, C. -C., and L. Libs. 1998. Cloning and characterisation of the pknD gene encoding an eukaryotic-type protein kinase in the cyanobacterium Anabaena sp. PCC7120. Mol. Gen. Genet. 258:2633.
142. Zhang, C.,- C. S. Hugucnin,, and A. Friry. 1995. Analysis of genes encoding the cell division protein FtsZ and a glutathione synthetase homologue in the cyanobacterium Anabaena sp. PCC 7120. Res. Microbiol. 146:445455.
143. Zhang, C., C. A. Friry,, and L. Peng. 1998. Molecular and genetic analysis of two closely linked genes that encode, respectively, a protein phosphatase 1/2A/2D homolog and a protein kinase homolog in the cyanobacterium Anabaena sp. strain PCC 7120.J Bacteriol. 180:26162622.
144. Zhou, R.,, Z. Cao,, and J. Zhao. 1998a. Characterization of HetK protein turnover in Anabaena sp. PCC 7120. Arch. Microbiol. 169:417423.
145. Zhou, R.,, X. Wei,, N. Jiang,, H. Li,, Y. Dong,, K.-L. Hsi,, and J. Zhao. 1998b. Evidence that HetR protein is an unusual serine-type protease. Proc. Natl. Acad. Sci. USA 95:49594963.
146. Zhu, J.,, K. Zarka,, and C. P. Wolk. Unpublished observations.
147. Zhu, J.,, R. Kong, and C P. Wolk. 1998. Regulation of hep A of Anabaena sp. strain PCC 7120 by elements 5' from the gene and by hepK.J. Bacteriol. 180:42334242.

Tables

Generic image for table
TABLE 1

Classes of genes activated upon nitrogen stepdown and/or required for aerobic N fixation

Citation: Wolk C. 2000. Heterocyst Formation in Anabaena, p 83-104. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch4

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