Mutations in four regulatory genes have interrelated effects on heterocyst maturation in Anabaena sp. strain PCC 7120

Journal of Bacteriology

Volumn 188, Issue 21, 2006, Pages 7387-7395

  Lechno Yossef, Sigal ^a   Fan, Qing ^a,d   Ehira, Shigeki ^b   Sato, Naoki ^c   Wolk, C Peter ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b SAITAMA UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; GLYCOLIPID; PROTEIN HISTIDINE KINASE; PROTEIN SERINE THREONINE KINASE; REGULATOR PROTEIN;

ANABAENA; ARTICLE; AUTOREGULATION; BACTERIAL GENE; BACTERIAL STRAIN; COMPARATIVE STUDY; DOWN REGULATION; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; HENR GENE; HEPK GENE; HEPN GENE; HEPS GENE; MUTANT; NONHUMAN; PATA GENE; PRIORITY JOURNAL; REGULATOR GENE; WILD TYPE;

ANABAENA; BACTERIAL PROTEINS; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENES, REGULATOR; GLYCOLIPIDS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYSACCHARIDES, BACTERIAL; REGULON; RNA, BACTERIAL; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

ANABAENA SP.;

EID: 33750485838     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00974-06     Document Type: Article

References (76)

1. Almon, H., and H. Böhme. 1980. Components and activity of the photosynthetic electron transport system of intact heterocysts isolated from the blue-green alga Nostoc muscorum. Biochim. Biophys. Acta 592:113-120.
2. Baldi, P., and A. D. Long. 2001. A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17:509-519.
3. 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. 151:23-30.
4. Black, K., W. J. Buikema, and R. Haselkorn. 1995. The hglK gene is required for localization of heterocyst-specific glycolipids in the cyanobacterium Anabaena sp. strain PCC 7120. J. Bacteriol. 177:6440-6448.
5. 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. 9:77-84.
6. - mutation in Anabaena sp. strain PCC 7120 implicates a secondary metabolite in the regulation of heterocyst spacing. J. Bacteriol. 176:2282-2292.
7. Britton, R. A., P. Eichenberger, J. E. Gonzalez-Pastor. P. Fawcett, R. Monsun, R. Losick, and A. D. Grossman. 2002. Genome-wide analysis of the stationary-phase sigma factor (sigma-H) regulon of Bacillus subtilis. J. Bacteriol. 184:4881-4890.
8. Buikema, W. J., and R. Haselkorn. 1991. Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena 7120. Genes Dev. 5:321-330.
9. Cai, Y. 1991. Molecular genetic approaches towards the understanding of heterocyst differentiation and pattern formation in the cyanobacterium Anabaena sp. Thesis. Michigan State University. East Lansing.
10. Callahan, S. M., and W. J. Buikema. 2001. The role of HetN in maintenance of the heterocyst pattern in Anabaena sp. PCC 7120. Mol. Microbiol. 40:941-950.
11. 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. 167:251-258.
12. 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. 178:2037-2043.
13. Ehira, S.. and M. Ohmori. 2006. NrrA. a novel nitrogen-responsive response regulator facilitates heterocyst development in the cyanobacterium Anabaena sp. strain PCC 7120. Mol. Microbiol. 59:1692-1703.
14. Ehira, S., M. Ohmori, and N. Sato. 2003. Genome-wide expression analysis of the responses to nitrogen deprivation in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. DNA Res. 10:97-113.
15. Ehira, S., M. Ohmori, and N. Sato. 2005. Identitication of low-temperature-regulated ORFs in the cyanobacterium Anabaena sp. strain PCC 7120: distinguishing the effects of low temperature from the effects of photosystem II excitation pressure. Plant Cell Physiol. 46:1237-1245.
16. Fan, Q., G. Huang, S. Lechno-Yossef, C. P. Wolk, T. Kaneko, and S. Tabata. 2005. Clustered genes required for synthesis and deposition of envelope glycolipids in Anabaena sp. strain PCC 7120. Mol. Microbiol. 58:227-243.
17. Fan, Q., S. Lechno-Yossef, S. Ehira, T. Kaneko, M. Ohmori, N. Sato, S. Tahata, and C. P. Wolk. 2006. Signal transduction genes required for heterocyst maturation in Anabaena sp. strain PCC 7120. J. Bacteriol. 188:6688-6693.
18. Fay, P. 1992. Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol. Rev. 56:340-373.
19. Fiedler, G., M. Arnold, S. Hannus, und I. Maldener. 1998. The DevBCA exporter is essential for envelope formation in heterocysts of the cyanobacterium Anabaena sp. strain PCC 7120. Mol. Microbiol. 27:1193-1202.
20. Fiedler, G., M. Arnold, and I. Maldener. 1998. Sequence and mutational analysis of the devBCA gene cluster encoding a putative ABC transporter in the cyanobacterium Anabaena variabilis ATCC 29413. Biochim. Biophys. Acta 1375:140-143.
21. Flores, E., and A. Herrero. 2005. Nitrogen assimilation and nitrogen control in cyanobacteria. Biochem. Soc. Trans. 33:164-167.
22. Fogg, G. E. 1951. Growth and heterocyst production in Anabaena cylindrica Lemm. III. The cytology of heterocysts. Ann. Bot. N.S. 15:23-35.
23. 2. New Phytol. 122:571-609.
24. Hanks, S. K., and T. Hunter. 1995. Protein kinases. 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 9:576-596.
25. Haselkorn, R., D. Rice, S. E. Curtis, and S. J. Robinson. 1983. Organization and transcription of genes important in Anabaena heterocyst differentiation. Ann. Microbiol. (Paris). I34B:181-193.
26. Haury, J. F., and C. P. Wolk. 1978. Classes of Anabaena variabilis mutants with oxygen-sensitive nitrogenase activity. J. Bacteriol. 136:688-692.
27. Hebbar, P. B., and S. E. Curtis. 2000. Characterization of devH, a gene encoding a putative DNA binding protein required for heterocyst function in Anabaena sp. strain PCC 7120. J. Bacteriol. 182:3572-3581.
28. Hegde, P., R. Qi, K. Abernathy, C. Gay, S. Dharap, R. Gaspard, J. E. Hughes, E. Snesrud, N. Lee, and J. Quackenbush. 2000. A concise guide to cDNA microarray analysis. BioTechniques 29:548-562.
29. Hernández, J. A., S. López-Gomollón, M. T. Bes, M. F. Fillat, and M. L. Peleato. 2004. Three fur homologues from Anabaena sp. PCC7120: exploring reciprocal protein-promoter recognition. FEMS Microbiol. Lett. 236:275-282.
30. Hernández, J. A., A. M. Muro-Pastor, E. Flores, M. T. Bes. M. L. Peleato, and M. F. Fillat. 2006. Identification of a furA cis antisense RNA in the cyanobacterium Anabaena sp. PCC 7120. J. Mol. Biol. 355:325-334.
31. Herrero, A., A. M. Muro-Pastor, A. Valladares, and E. Flores. 2004. Cellular differentiation and the NtcA transcription factor in filamentous cyanobacteria. FEMS Microbiol. Rev. 28:469-487.
32. 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. 172:3131-3137.
33. Huang, G., Q. Fan, S. Lechno-Yossef, E. Wojciuch, C. P. Wolk, T. Kaneko, and S. Tahata. 2005. Clustered genes required for the synthesis of heterocyst envelope polysaccharide in Anabaena sp. strain PCC 7120. J. Bacteriol. 187:1114-1123.
34. Huang, X., Y. Dong, and J. Zhao. 2004. HetR homodimer is a DNA- binding protein required for heterocyst differentiation, and the DNA-binding activity is inhibited by PatS. Proc. Natl. Acad. Sci. USA 101:4848-4853.
35. Hung, S., P. Baldi, and G. W. Hatfield. 2002. Global gene expression profiling in Escherichia coli K12. The effects of leucine-responsive regulatory protein. J. Biol. Chem. 277:40309-40323.
36. Kaiman, L. V., Y. L. Cheng, and D. Kaiser. 1994. The Myxococcus xanthus dsg gene product performs functions of translation initiation factor If3 in vivo. J. Bacteriol. 176:1434-1442.
37. Kaneko, T., Y. Nakamura, C. P. Wolk, T. Kuritz, S. Sasamoto, A. Watanahe, M. Iriguchi, A. Ishikawa, K. Kawashima, T. Kimura, Y. Kishida, M. Kohara, M. Matsumoto, A. Matsuno, A. Muraki, N. Nakazaki, S. Shimpo, M. Sugimoto, M. Takazawa, M. Yamada, M. Yasuda, and S. Tahata. 2001. Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res. 8:205-213.
38. Koksharova, O. A., and C. P. Wolk. 2002. Novel DNA-hinding proteins in the cyanobacterium Anabaena sp. strain PCC 7120. J. Bacteriol. 184:3931-3940.
39. Laurent, S., H. Chen, S. Bédu, F. Ziarelli, L. Peng, and C.-C. Zhang. 2005. Nonmetabolizable analogue of 2-oxoglutarate elicits heterocyst differentiation under repressive conditions in Anabaena sp. PCC 7120. Proc. Natl. Acad. Sci. USA 102:9907-9912.
40. n is involved in the regulation of nitrogen metabolism in the cyanobacterium Anabaena PCC 7120. FEBS Lett. 576:261-265.
41. Leganés, F., A. Blanco-Rivero, F. Fernández-Piñas, M. Redondo, F. Fernández-Valiente, Q. Fan, S. Lechno-Yossef, and C. P. Wolk. 2005. Wide variation in the cyanobacterial complement of presumptive penicillin-binding proteins. Arch. Microbiol. 184:234-248.
42. LeProust, E., H. Zhang, P. Yu, X. Zhou, and X. Gao. 2001. Characterization of oligodeoxyribonucleotide synthesis on glass plates. Nucleic Acids Res. 29:2171-2180.
43. Liang, J., L. Scappino, and R. Haselkorn. 1992. The patA gene product, which contains a region similar to ChcY of Escherichia coli, controls heterocyst pattern formation in the cyanobacterium Anabaena 7120. Proc. Natl. Acad. Sci. USA 89:5055-5659.
44. Loos, A., C. Glanemann, L. B. Willis, X. M. O'Brien, P. A. Lessard, R. Gerstmeir, S. Guillouet, and A. J. Sinskey. 2001. Development and validation of Corynebacterium DNA microarrays. Appl. Environ. Microbiol. 67:2310-2318.
45. 44a. López-Gomollón, S., J. A. Hernández, C. P. Wolk. M. L. Peleato, and M. F. Fillat. Expression of furA is modulated by NtcA and strongly enhanced in heterocysts of Anabaena sp. PCC 7120. Microbiology, in press.
46. Makarova, K. S., E. V. Koonin, R. Haselkorn, and M. Y. Galperin. 2006. Cyanobacterial response regulator PatA contains a conserved N-terminal domain (PATAN) with an alpha-helical insertion. Bioinformatics 22:1297-1301.
47. Maldener, I., S. Hanmis, and M. Kammerer. 2003. Description of live mutants of the cyanobacterium Anabaena sp. strain PCC 7f20 affected in heterocyst differentiation and identification of the transposon-tagged genes. FEMS Microbiol. Lett. 224:205-213.
48. Maldener, I., W. Lockau, Y. P. Cai, and C. P. Wolk. 1991. Calcium-dependent protease of the cyanobacterium Anabaena: molecular cloning and expression of the gene in Escherichia coli. sequencing and site-directed mutagenesis. Mol. Gen. Genet. 225:1 13-120.
49. Mohamed, A., and C. Jansson. 1989. Influence of light on accumulation of photosynthesis-specific transcripts in the cyanobacterium Synechocystis 6803. Plant Mol. Biol. 13:693-700.
50. Murata, N., and I. Suzuki. 2006. Exploitation of genomic sequences in a systematic analysis to access how cyanobacteria sense environmental stress. J. Exp. Bot. 57:235-247.
51. 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. 151:469-474.
52. Ning, D., and X. Xu. 2004. alr0117. a two-component histidine kinase gene, is involved in heterocyst development in Anabaena sp. PCC 7120. Microbiology 150:447-453.
53. Ohmori, M., M. Ikeuchi, N. Sato, P. Wolk, T. Kaneko, T. Ogawa, M. Kanehisa, S. Goto, S. Kawashima, S. Okamoto, H. Yoshimura, H. Katoh, T. Fujisawa, S. Ehira, A. Kamei, S. Yoshihara, R. Narikawa, and S. Tabata. 2001. Characterization of genes encoding multi-domain proteins in the genome of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res. 8:271-284.
54. Orozco, C. C., D. D. Risser, and S. M. Callahan. 2006. Epistasis analysis of four genes from Anabaena sp. strain PCC 7120 suggests a connection between PatA and PatS in heterocyst pattern formation. J. Bacteriol. 188:1808-1816.
55. Parkinson, J. S. 1993. Signal transduction schemes of bacteria. Cell 73:857-871.
56. Quackenbush, J. 2001. Computational analysis of microarray data. Nat. Rev. Genet. 2:418-427.
57. Ramírez, M. E., P. B. Hebbar, R. Zhou, C. P. Wolk, and S. E. Curtis. 2005. Anabaena sp. strain PCC 7120 gene devH is required for synthesis of the heterocyst glycolipid layer. J. Bacteriol. 187:2326-2331.
58. Salmon, K., S. P. Hung, K. Mekjian, P. Baldi, G. W. Hatfield, and R. P. Gunsalus. 2003. Global gene expression profiling in Escherichia coli K12. The effects of oxygen availability and FNR. J. Biol. Chem. 278:29837-29855.
59. Seo, J., H. Gordish-Dressman, and E. P. Hoffman. 2006. An interactive power analysis tool for microarray hypothesis testing and generation. Bioinformatics 22:808-814.
60. Smyth, G. K., and T. Speed. 2003. Normalization of cDNA microarray data. Methods Enzymol. 31:265-273.
61. Tel-Or, E., and W. D. P. Stewart. 1977. Pholosynthetic components and activities of nitrogen-fixing isolated heterocysts of Anabaena cyllindrica. Proc. R. Soc. London B 198:61-86.
62. Walsby, A. E. 1985. The permeability of heterocysts to the gases nitrogen and oxygen. Proc. R. Soc. London B 226:345-366.
63. Wang, L., Y. P. Sun, W. L. Chen, J. H. Li, and C. C. Zhang. 2002. Genomic analysis of protein kinases, protein phosphatases and two-component regulatory systems of the cyanobacterium Anabaena sp. strain PCC 7120. FEMS Microbiol. Lett. 217:155-165.
64. Winkenbach, F., C. P. Wolk, and M. Jost. 1972. Lipids of membranes and of the cell envelope in heterocysts of a blue-green alga. Planta 107:69-80.
65. Wolk, C. P. 2000. Heterocyst formation in Anabaena. p. 83-104. In Y. V. Brun and L. J. Shimkets (ed.), Prokaryotic development. ASM Press. Washington, D.C.
66. Wolk, C. P., Y. Cai, L. Cardemil, E. Flores, 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. 170:1239-1244.
67. Wolk, C. P., J. Elhai, T. Kuritz, and D. Holland. 1993. Amplified expression of a transcriptional pattern formed during development of Anabaena. Mol. Microbiol. 7:441-445.
68. Wolk, C. P., A. Ernst, and J. Elhai. 1994. Heterocyst metabolism and development, p. 769-823. In D. A. Bryant (ed.). The molecular biology of eyanobacteria. Kluwer Academic Publishers. Dordrecht, The Netherlands.
69. 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. 179:2884-2891.
70. Yeon, H.-S., and J. W. Golden. 1998. Heterocyst pattern formation controlled by a diffusible peptide. Science 282:935-938.
71. Zhang, C.-C., S. Laurent, S. Sakr, L. Peng, and S. Bédu. 2006. Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Mol. Microbiol. 59:367-375.
72. Zhao, Y., and C. P. Wolk. Developmental biology of heterocysts. In H. B. Kaplan and D. E. Whitworth (ed.). Multicellularity and differentiation among the myxobacteria and their neighbors, in press. American Society for Microbiology. Washington, D.C.
73. Zhou, R., and C. P. Wolk. 2003. A two-component system mediates developmental regulation of biosynthesis of a heterocyst polysaccharide. J. Biol. Chem. 278:19939-19946.
74. Zhu, J., K. Jäger, T. Black, K. Zarka, O. Koksharova, and C. P. Wolk. 2001. HewA, an autolysin, is required for heterocyst maturation in Anabaena sp. strain PCC 7120. J. Bacteriol. 183:6841-6851.
75. Zhu, J., K. Kong, and C. P. Wolk. 1998. Regulation of hepA of Anabaena sp. strain PCC 7120 by elements 5′ from the gene and by hepK. J. Bacteriol. 180:4233-4242.
76. Zuker, M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415.