Integrative analysis of large scale expression profiles reveals core transcriptional response and coordination between multiple cellular processes in a cyanobacterium

BMC Systems Biology

Volumn 4, Issue , 2010, Pages

  Singh, Abhay K ^a   Elvitigala, Thanura ^b   Cameron, Jeffrey C ^a   Ghosh, Bijoy K ^c   Bhattacharyya Pakrasi, Maitrayee ^a   Pakrasi, Himadri B ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^c TEXAS TECH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYANOBACTERIA; PROKARYOTA; SYNECHOCYSTIS; SYNECHOCYSTIS SP. PCC 6803;

BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GENE; BAYES THEOREM; BIOLOGY; CYTOLOGY; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENETIC DATABASE; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; METHODOLOGY; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROTEIN SYNTHESIS; SYNECHOCYSTIS;

BACTERIAL PROTEINS; BAYES THEOREM; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENES, BACTERIAL; PHOTOSYNTHESIS; PROTEIN BIOSYNTHESIS; STRESS, PHYSIOLOGICAL; SYNECHOCYSTIS; TRANSCRIPTION, GENETIC;

EID: 77955073512     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-4-105     Document Type: Article

References (56)

1. Bonneau R, Facciotti MT, Reiss DJ, Schmid AK, Pan M, Kaur A, Thorsson V, Shannon P, Johnson MH, Bare JC, et al. A predictive model for transcriptional control of physiology in a free living cell. Cell 2007, 131:1354-1365. 10.1016/j.cell.2007.10.053, 18160043.
2. de Godoy LM, Olsen JV, Cox J, Nielsen ML, Hubner NC, Frohlich F, Walther TC, Mann M. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 2008, 455:1251-1254. 10.1038/nature07341, 18820680.
3. Feist AM, Palsson BO. The growing scope of applications of genome-scale metabolic reconstructions using Escherichia coli. Nat Biotechnol 2008, 26:659-667. 10.1038/nbt1401, 18536691.
4. Girardot F, Monnier V, Tricoire H. Genome wide analysis of common and specific stress responses in adult Drosophila melanogaster. BMC Genomics 2004, 5:74. 10.1186/1471-2164-5-74, 526417, 15458575.
5. Hughes TR, Marton MJ, Jones AR, Roberts CJ, Stoughton R, Armour CD, Bennett HA, Coffey E, Dai H, He YD, et al. Functional discovery via a compendium of expression profiles. Cell 2000, 102:109-126. 10.1016/S0092-8674(00)00015-5, 10929718.
6. Jenner RG, Young RA. Insights into host responses against pathogens from transcriptional profiling. Nat Rev Microbiol 2005, 3:281-294. 10.1038/nrmicro1126, 15806094.
7. Joyce AR, Palsson BO. The model organism as a system: integrating 'omics' data sets. Nat Rev Mol Cell Biol 2006, 7:198-210. 10.1038/nrm1857, 16496022.
8. Komili S, Silver PA. Coupling and coordination in gene expression processes: a systems biology view. Nat Rev Genet 2008, 9:38-48. 10.1038/nrg2223, 18071322.
9. Ma S, Bohnert HJ. Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures, and cell-specific expression. Genome Biol 2007, 8:R49. 10.1186/gb-2007-8-4-r49, 1896000, 17408486.
10. Falkowski PG, Godfrey LV. Electrons, life and the evolution of Earth's oxygen cycle. Philos Trans R Soc Lond B Biol Sci 2008, 363:2705-2716. 10.1098/rstb.2008.0054, 2606772, 18487127.
11. Johnson ZI, Zinser ER, Coe A, McNulty NP, Woodward EM, Chisholm SW. Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 2006, 311:1737-1740. 10.1126/science.1118052, 16556835.
12. Kasting JF. Earth history. The rise of atmospheric oxygen. Science 2001, 293:819-820. 10.1126/science.1063811, 11486080.
13. Cavalier-Smith T. Chloroplast evolution: secondary symbiogenesis and multiple losses. Curr Biol 2002, 12:R62-64. 10.1016/S0960-9822(01)00675-3, 11818081.
14. Kasting JF, Siefert JL. Life and the evolution of Earth's atmosphere. Science 2002, 296:1066-1068. 10.1126/science.1071184, 12004117.
15. Kasting JF. When methane made climate. Sci Am 2004, 291:78-85. 10.1038/scientificamerican0704-78, 15255591.
16. Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, et al. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 1996, 3:109-136. 10.1093/dnares/3.3.109, 8905231.
17. Rifkin SA, Kim J, White KP. Evolution of gene expression in the Drosophila melanogaster subgroup. Nat Genet 2003, 33:138-144. 10.1038/ng1086, 12548287.
18. Brauer MJ, Huttenhower C, Airoldi EM, Rosenstein R, Matese JC, Gresham D, Boer VM, Troyanskaya OG, Botstein D. Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast. Mol Biol Cell 2008, 19:352-367. 10.1091/mbc.E07-08-0779, 2174172, 17959824.
19. Lopez-Maury L, Marguerat S, Bahler J. Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat Rev Genet 2008, 9:583-593. 10.1038/nrg2398, 18591982.
20. Jiao Y, Lau OS, Deng XW. Light-regulated transcriptional networks in higher plants. Nat Rev Genet 2007, 8:217-230. 10.1038/nrg2049, 17304247.
21. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO. Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 2000, 11:4241-4257. 15070, 11102521.
22. Murray JI, Whitfield ML, Trinklein ND, Myers RM, Brown PO, Botstein D. Diverse and specific gene expression responses to stresses in cultured human cells. Mol Biol Cell 2004, 15:2361-2374. 10.1091/mbc.E03-11-0799, 404029, 15004229.
23. Tanay A, Steinfeld I, Kupiec M, Shamir R. Integrative analysis of genome-wide experiments in the context of a large high-throughput data compendium. Mol Syst Biol 2005, 1:2005 0002. 10.1038/msb4100005, 1681453, 16729037.
24. Quackenbush J. Microarray data normalization and transformation. Nat Genet 2002, 32(Suppl):496-501. 10.1038/ng1032, 12454644.
25. Singh AK, Elvitigala T, Bhattacharyya-Pakrasi M, Aurora R, Ghosh B, Pakrasi HB. Integration of carbon and nitrogen metabolism with energy production is crucial to light acclimation in the cyanobacterium Synechocystis. Plant Physiol 2008, 148:467-478. 10.1104/pp.108.123489, 2528105, 18599646.
26. Alfonso M, Perewoska I, Kirilovsky D. Redox control of psbA gene expression in the cyanobacterium Synechocystis PCC 6803. Involvement of the cytochrome b(6)/f complex. Plant Physiol 2000, 122:505-516. 10.1104/pp.122.2.505, 58887, 10677443.
27. Pfannschmidt T, Brautigam K, Wagner R, Dietzel L, Schroter Y, Steiner S, Nykytenko A. Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding. Ann Bot (Lond) 2009, 103:599-607.
28. Singh AK, Sherman LA. Pleiotropic effect of a histidine kinase on carbohydrate metabolism in Synechocystis sp. strain PCC 6803 and its requirement for heterotrophic growth. J Bacteriol 2005, 187:2368-2376. 10.1128/JB.187.7.2368-2376.2005, 1065225, 15774880.
29. Suzuki I, Kanesaki Y, Hayashi H, Hall JJ, Simon WJ, Slabas AR, Murata N. The histidine kinase Hik34 is involved in thermotolerance by regulating the expression of heat shock genes in Synechocystis. Plant Physiol 2005, 138:1409-1421. 10.1104/pp.104.059097, 1176413, 15965020.
30. Jantaro S, Ali Q, Lone S, He Q. Suppression of the lethality of high light to a quadruple HLI mutant by the inactivation of the regulatory protein PfsR in Synechocystis PCC 6803. J Biol Chem 2006, 281:30865-30874. 10.1074/jbc.M606252200, 16914546.
31. Kobayashi M, Ishizuka T, Katayama M, Kanehisa M, Bhattacharyya-Pakrasi M, Pakrasi HB, Ikeuchi M. Response to oxidative stress involves a novel peroxiredoxin gene in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 2004, 45:290-299. 10.1093/pcp/pch034, 15047877.
32. Li H, Singh AK, McIntyre LM, Sherman LA. Differential gene expression in response to hydrogen peroxide and the putative PerR regulon of Synechocystis sp. Strain PCC 6803. J Bacteriol 2004, 186:3331-3345. 10.1128/JB.186.11.3331-3345.2004, 415769, 15150218.
33. Houot L, Floutier M, Marteyn B, Michaut M, Picciocchi A, Legrain P, Aude JC, Cassier-Chauvat C, Chauvat F. Cadmium triggers an integrated reprogramming of the metabolism of Synechocystis PCC6803, under the control of the Slr1738 regulator. BMC Genomics 2007, 8:350. 10.1186/1471-2164-8-350, 2190772, 17910763.
34. Tottey S, Waldron KJ, Firbank SJ, Reale B, Bessant C, Sato K, Cheek TR, Gray J, Banfield MJ, Dennison C, Robinson NJ. Protein-folding location can regulate manganese-binding versus copper- or zinc-binding. Nature 2008, 455:1138-1142. 10.1038/nature07340, 18948958.
35. Allen JF. Photosynthesis: the processing of redox signals in chloroplasts. Curr Biol 2005, 15:R929-932. 10.1016/j.cub.2005.10.061, 16303553.
36. Puthiyaveetil S, Allen JF. Chloroplast two-component systems: evolution of the link between photosynthesis and gene expression. Proc Biol Sci 2009, 276(1665):2133-2145. 10.1098/rspb.2008.1426, 2677595, 19324807.
37. Hihara Y, Sonoike K, Kanehisa M, Ikeuchi M. DNA microarray analysis of redoxresponsive genes in the genome of the cyanobacterium Synechocystis sp. Strain PCC 6803. J Bacteriol 2003, 185:1719-1725. 10.1128/JB.185.5.1719-1725.2003, 148065, 12591891.
38. Fuangthong M, Herbig AF, Bsat N, Helmann JD. Regulation of the Bacillus subtilis fur and perR genes by PerR: not all members of the PerR regulon are peroxide inducible. J Bacteriol 2002, 184:3276-3286. 10.1128/JB.184.12.3276-3286.2002, 135084, 12029044.
39. Irmler A, Forchhammer K. A PP2C-type phosphatase dephosphorylates the PII signaling protein in the cyanobacterium Synechocystis PCC 6803. Proc Natl Acad Sci USA 2001, 98:12978-12983. 10.1073/pnas.231254998, 60810, 11687619.
40. Forchhammer K. Global carbon/nitrogen control by PII signal transduction in cyanobacteria: from signals to targets. FEMS Microbiol Rev 2004, 28:319-333. 10.1016/j.femsre.2003.11.001, 15449606.
41. Mooney RA, Schweimer K, Rosch P, Gottesman M, Landick R. Two structurally independent domains of E. coli NusG create regulatory plasticity via distinct interactions with RNA polymerase and regulators. J Mol Biol 2009, 391:341-358. 10.1016/j.jmb.2009.05.078, 19500594.
42. Koide T, Pang WL, Baliga NS. The role of predictive modelling in rationally reengineering biological systems. Nat Rev Microbiol 2009, 7:297-305. 2734281, 19252506.
43. Chen D, Toone WM, Mata J, Lyne R, Burns G, Kivinen K, Brazma A, Jones N, Bahler J. Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 2003, 14:214-229. 10.1091/mbc.E02-08-0499, 140239, 12529438.
44. Massey FJ. The Kolmogorov-Smimov test for goodness-of-fit. J Amer Statist Assoc 1951, 46:68-78.
45. Jensen FV, Nielsen TD. Bayesian Networks and Decision Graphs 2007, New York: Springer-Verlag Inc.
46. Herrero A, Muro-Pastor AM, Flores E. Nitrogen control in cyanobacteria. J Bacteriol 2001, 183:411-425. 10.1128/JB.183.2.411-425.2001, 94895, 11133933.
47. Singh AK, Bhattacharyya-Pakrasi M, Elvitigala T, Ghosh B, Aurora R, Pakrasi HB. A systems level analysis of the effects of light quality on the metabolism of a cyanobacterium. Plant Physiol 2009, 151:1596-1608. 10.1104/pp.109.144824, 2773086, 19759342.
48. Flores E, Herrero A. Nitrogen assimilation and nitrogen control in cyanobacteria. Biochem Soc Trans 2005, 33:164-167. 10.1042/BST0330164, 15667295.
49. Gourse RL, Gaal T, Bartlett MS, Appleman JA, Ross W. rRNA transcription and growth rate-dependent regulation of ribosome synthesis in Escherichia coli. Annu Rev Microbiol 1996, 50:645-677. 10.1146/annurev.micro.50.1.645, 8905094.
50. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30:207-210. 10.1093/nar/30.1.207, 99122, 11752295.
51. Kanehisa M, Goto S, Kawashima S, Nakaya A. The KEGG databases at GenomeNet. Nucleic Acids Res 2002, 30:42-46. 10.1093/nar/30.1.42, 99091, 11752249.
52. Hamming RW. Error Detecting and Error Correcting Codes. Bell System Technical Journal 1950, 26:147-160.
53. Pourret O, Naim P, Marcot B. Bayesian Networks: A practical Guide to Applications 2008, John Willey and Sons Ltd.
54. Chickering DM. Optimal structure identification with greedy search. Journal of Machine Learning Research 2002, 3:507-554.
55. Elvitigala T, Singh AK, Pakrasi HB, Ghosh B. Bayesian Network Approach to understand Regulation of Biological Processes in Cyanobacteria. IEEE Conference on Decision and Control; Shanghai, China 2009,
56. Ebert-Uphoff I. Measuring Connection Strengths and Link Strengths in Discrete Bayesian Networks. 2007, Georgia Institute of Technology.