Global transcription profiles of the nitrogen stress response resulting in heterocyst or hormogonium development in Nostoc punctiforme

Journal of Bacteriology

Volumn 193, Issue 24, 2011, Pages 6874-6886

  Christman, Harry D ^a   Campbell, Elsie L ^a   Meeks, John C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NITROGEN;

ARTICLE; BAYES THEOREM; CELL TYPE; COMPUTER PROGRAM; DNA MICROARRAY; DOWN REGULATION; GENE EXPRESSION; GENE FUNCTION; GENE REGULATORY NETWORK; GENE STRUCTURE; GENETIC TRANSCRIPTION; GENOME; HETEROCYST; HORMOGONIUM; NONHUMAN; NOSTOC; OPEN READING FRAME; PRIORITY JOURNAL; STRESS; TRANSCRIPTION INITIATION; UPREGULATION;

BACTERIAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; NITROGEN; NOSTOC; STRESS, PHYSIOLOGICAL;

NOSTOC PUNCTIFORME; NOSTOC SP.;

EID: 84855829776     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.05999-11     Document Type: Article

References (60)

1. Adams, D. G. 2000. Symbiotic interactions, p. 523-561. In B. A. Whitton and M. Potts (ed.), The ecology of cyanobacteria, their diversity in time and space. Kluwer Academic Publishers, Dordrecht, Netherlands.
2. Aldea, M. R., R. A. Mella-Herrera, and J. W. Golden. 2007. Sigma factor genes sigC, sigE, and sigG are upregulated in heterocysts of the cyanobacterium Anabaena sp. PCC7120. J. Bacteriol. 189:8392-8396.
3. Allan, M. B., and D. I. Arnon. 1955. Studies on nitrogen-fixing blue-green algae. I. Growth and nitrogen fixation by Anabaena cylindrica Lemm. Plant Physiol. 30:366-372.
4. Angelini, C., L. Cutillo, D. De Canditii, M. Mutarelli, and M. Pensky. 2008. BATS: a Bayesian user-friendly software for analyzing time series microarray experiments. BMC Bioinformatics 9:415.
5. Armstrong, R. E., P. K. Hayes, and A. E. Walsby. 1983. Gas vacuole formation in hormogonia of Nostoc muscorum. J. Gen. Microbiol. 128:263-270.
6. Ashby, M. K., and C. W. Mullineaux. 1999. Cyanobacterial ycf27 gene products regulate energy transfer from phycobilisomes to photosystems I and II. FEMS Microbiol. Lett. 181:253-260.
7. Baier, K., H. Lehm, D. P. Stephan, and W. Lockau. 2004. NblA is essential for phycobilisome degradation in Anabaena sp. strain PCC 7120 but not for development of functional heterocysts. Microbiology 150:2739-2749.
8. Buikema, W. J., and R. Haselkorn. 2001. Expression of the Anabaena hetR gene from a copper-regulated promoter leads to heterocyst differentiation under repressing conditions. Proc. Natl. Acad. Sci. U. S. A. 98:2729-2734.
9. Cai, Y., and C. P. Wolk. 1997. Anabaena sp. strain PCC 7120 responds to nitrogen deprivation with a cascade-like sequence of transcriptional activations. J. Bacteriol. 179:267-271.
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., and J. C. Meeks. 1989. Characteristics of hormogonia formation by symbiotic Nostoc spp. in response to the presence of Anthoceros punctatus or its extracellular products. Appl. Environ. Microbiol. 55:125-131.
12. Campbell, E. L., H. Christman, and J. C. Meeks. 2008. DNA microarray comparisons of plant factor- and nitrogen deprivation-induced hormogonia reveal decision-making transcriptional regulation patterns in Nostoc punctiforme. J. Bacteriol. 190:7382-7391.
13. Campbell, E. L., M. L. Summers, H. Christman, M. E. Martin, and J. C. Meeks. 2007. Global gene expression patterns of Nostoc punctiforme in steady-state dinitrogen-grown heterocyst-containing cultures and at single time points during the differentiation of akinetes and hormogonia. J. Bacteriol. 189:5247-5256.
14. 2-fixing cyanobacterium Anabaena cylindrica. FEMS Microbiol. Lett. 28:65-68.
15. Damerval, T., G. Guglielmi, J. Houmard, and N. T. de Marsac. 1991. Hormogonium differentiation in the cyanobacterium Calothrix: a photoregulated developmental process. Plant Cell 3:191-201.
16. de Hoon, M. J. L., S. Imoto, J. Nolan, and S. Miyano. 2004. Open source clustering software. Bioinformatics 20:1453-1454.
17. Douglas, D., A. Peat, B. A. Whitton, and P. Wood. 1987. Influence of iron status on structure of the cyanobacterium (blue-green alga) Calothrix parientina. Cytobiosis 47:155-165.
18. Ehira, S., and M. Ohmori. 2006. NrrA, a nitrogen-responsive response regulator facilitates heterocyst development in the cyanobacterium Anabaena sp. strain PCC 7120. Mol. Microbiol. 59:1692-1703.
19. Ehira, S., M. Ohmori, and N. Sato. 2003. Genome-wide expression analysis of the response to nitrogen deprivation in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. DNA Res. 10:97-113.
20. 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. 9:3379-3388.
21. Fan, Q., et al. 2005. Clustered genes required for synthesis and deposition of envelope glycolipids in Anabaena sp. strain PCC 7120. Mol. Microbiol. 58: 227-243.
22. Fernandez-Pinas, F., F. Leganes, and C. P. Wolk. 1994. A third genetic locus required for the formation of heterocysts in Anabaena sp. strain PCC 7120. J. Bacteriol. 176:5277-5283.
23. Flaherty, B. L., F. Van Nieuwerburgh, S. R. Head, and J. W. Golden. 2011. Directional RNA deep sequencing sheds new light on the transcriptional response of Anabaena sp. strain PCC 7120 to combined-nitrogen deprivation. BMC Genomics 12:332.
24. Flores, E., J. E. Frias, L. M. Rubio, and A. Herrero. 2005. Photosynthetic nitrate assimilation in cyanobacteria. Photosynth. Res. 83:117-133.
25. Flores, E., and A. Herrero. 1994. Assimilatory nitrogen metabolism and its regulation, p. 487-517. In D. A. Bryant (ed.), The molecular biology of cyanobacteria. Kluwer Academic Publishers, Boston, MA.
26. 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. 179:477-486.
27. Frias, J. E., E. Flores, and A. Herrero. 2000. Activation of the Anabaena nir operon promoter requires both NtcA (CAP family) and NtcB (LysR family) transcription factors. Mol. Microbiol. 38:613-625.
28. Golden, J. W., C. D. Carrasco, M. E. Mulligan, G. J. Schneider, and R. Haselkorn. 1988. Deletion of the 55-kilobase-pair DNA element from the chromosome during heterocyst differentiation of Anabaena sp. strain PCC 7120. J. Bacteriol. 170:5034-5041.
29. Golden, J. W., and D. R. Weist. 1988. Genome rearrangement and nitrogen fixation in Anabaena blocked by inactivation of xisA gene. Science 242:1421-1423.
30. Golden, J. W., L. L. Whorff, and D. R. Wiest. 1991. Independent regulation of nifHDK operon transcription and DNA rearrangement during heterocyst differentiation in the cyanobacterium Anabaena sp. strain PCC 7120. J. Bacteriol. 173:7098-7105.
31. Herdman, M., and R. Rippka. 1988. Cellular differentiation: hormogonia and baeocytes. Methods Enzymol. 167:232-242.
32. Herrero, A., A. M. Muro-Pastor, and E. Flores. 2001. Nitrogen control in cyanobacteria. J. Bacteriol. 183:411-425.
33. Higa, K. C., and S. M. Callahan. 2010. Ectopic expression of hetP can partially bypass the need for hetR in heterocyst differentiation by Anabaena sp. strain PCC 7120. Mol. Microbiol. 77:562-574.
34. Hill, D. R., et al. 1996. GlbN (cyanoglobin) is a peripheral membrane protein that is restricted to certain Nostoc spp. J. Bacteriol. 178:6587-6598.
35. Huang, G., et al. 2005. Clustered genes required for the synthesis of heterocyst envelope polysaccharide in Anabaena sp. strain PCC 7120. J. Bacteriol. 187:1114-1123.
36. 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. U. S. A. 101:4848-4853.
37. Jones, K. M., and R. Haselkorn. 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.
38. Knight, C. D., and D. G. Adams. 1996. A method for studying chemotaxis in nitrogen fixing cyanobacterium-plant symbioses. Physiol. Mol. Plant Pathol. 49:73-77.
39. 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. Sci. U. S. A. 89:5655-5659.
40. Lynn, M. E., J. A. Bantle, and J. D. Ownby. 1986. Estimation of gene expression in heterocysts of Anabaena variabilis by using DNA-RNA hybridizations. J. Bacteriol. 167:940-946.
41. Meeks, J. C., E. L. Campbell, M. L. Summers, and F. C. Wong. 2002. Cellular differentiation in the cyanobacterium Nostoc punctiforme. Arch. Microbiol. 178:395-403.
42. Meeks, J. C., and R. W. Castenholz. 1971. Growth and photosynthesis in an extreme thermophile Synechococcus lividus (Cyanophyta). Arch. Mikrobiol. 78:25-41.
43. Meeks, J. C., and J. Elhai. 2002. Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol. Mol. Biol. Rev. 66:94-1231.
44. Meeks, J. C., et al. 2001. An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosyn. Res. 70:85-106.
45. Muro-Pastor, A. M., E. Olmedo-Verd, and E. Flores. 2006. All4312, an NtcA-regulated two-component response regulator in Anabaena sp. strain PCC7120. FEMS Microbiol. Lett. 256:171-177.
46. Mutarelli, M., et al. 2008. Time-course analysis of genome-wide gene expression data from hormone-responsive human breast cancer cells. BMC Bioinformatics 9:1-14.
47. Saha, S. K., and J. W. Golden. 2011. Overexpression of pknE blocks heterocyst development in Anabaena sp. strain PCC 7120. J. Bacteriol. 193:2619-2629.
48. Saldanha, A. J. 2004. Java Treeview: extensible visualization of microarray data. Bioinform. Appl. Notes 20:3246-3248.
49. Smyth, G. K. 2005. Limma: linear models for microarray data, p. 397-420. In R. Gentleman, V. Carry, S. Dudoit, R. Irizarry, and W. Huber (ed.), Bioinformatics and computational biology solutions using R and Bioconductor. Springer, New York, NY.
50. Suzuki, I., N. Horie, T. Sugiyama, and T. Omata. 1995. Identification and characterization of two nitrogen-regulated genes of the cyanobacterium Synechococcus sp. strain PCC 7942 required for maximum efficiency of nitrogen assimilation. J. Bacteriol. 177:290-296.
51. Thiel, T. 2004. Nitrogen fixation in heterocyst-forming cyanobacteria, p. 73-110. In W. Klipp, B. Masepohl, J. R. Gallon, and W. E. Newton (ed.), Genetics and regulation of nitrogen-fixing bacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands.
52. Valladares, A., M. L. Montesinos, A. Herrero, and E. Flores. 2002. An ABC-type, high-affinity urea permease identified in cyanobacteria. Mol. Microbiol. 43:703-715.
53. Wang, Q., H. Li, and A. F. Post. 2000. Nitrate assimilation genes of the marine diazotrophic, filamentous cyanobacterium Trichodesmium sp. strain WH9601. J. Bacteriol. 182:1764-1767.
54. 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 cyanobacteria. Kluwer Academic Publishers, Boston, MA.
55. Wong, F .C. Y., and J. C. Meeks. 2001. The hetF gene product is essential to heterocyst differentiation and affects HetR function in the cyanobacterium Nostoc punctiforme. J. Bacteriol. 183:2654-2661.
56. Wu, X., D. Liu, M. H. Lee, and J. W. Golden. 2004. patS minigenes inhibit heterocyst development of Anabaena sp. strain 7120. J. Bacteriol. 186:6422-6429.
57. Xu, X., J. Elhai, and C. P. Wolk. 2007. Transcriptional and developmental responses by Anabaena to deprivation of fixed nitrogen, p. 383-422. In A. Herrero and E. Flores (ed.), The Cyanobacteria: molecular biology, genomics and evolution. Horizon Scientific Press, Norwich, United Kingdom.
58. Yoon, H. S., and J. W. Golden. 1998. Heterocyst pattern formation controlled by a diffusible peptide. Science 282:935-938.
59. 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/2B homolog and a protein kinase homolog in the cyanobacterium Anabaena sp. strain PCC 7120. J. Bacteriol. 180:2616-2622.
60. Zhang, C.-C., S. Laurent, S. Sakr, L. Peng, and S. Bedu. 2006. Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Mol. Microbiol. 59:367-375.