Metabolomic analysis reveals rewiring of Synechocystissp. PCC 6803 primary metabolism by ntcA overexpression

Environmental Microbiology

Volumn 16, Issue 10, 2014, Pages 3304-3317

  Osanai, Takashi ^a,b   Oikawa, Akira ^a,c   Iijima, Hiroko ^a   Kuwahara, Ayuko ^a   Asayama, Munehiko ^d   Tanaka, Kan ^e   Ikeuchi, Masahiko ^f   Saito, Kazuki ^a,g   Hirai, Masami Yokota ^a  

^a RIKEN Center for Sustainable Resource Science   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c YAMAGATA UNIVERSITY   (Japan)

^d IBARAKI UNIVERSITY   (Japan)

^e TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^f UNIVERSITY OF TOKYO   (Japan)

^g CHIBA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DNA BINDING PROTEIN; NITROGEN; NTCA PROTEIN, SYNECHOCOCCUS; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METABOLOME; METABOLOMICS; SYNECHOCYSTIS;

BACTERIAL PROTEINS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; METABOLOME; METABOLOMICS; NITROGEN; SYNECHOCYSTIS; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84907854012     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12554     Document Type: Article

References (39)

1. Aguirre von Wobeser, E., Ibelings, B.W., Bok, J., Krasikov, V., Huisman, J., and Matthijs, H.C. (2011) Concerted changes in gene expression and cell physiology of the cyanobacterium Synechocystis sp. strain PCC 6803 during transitions between nitrogen and light-limited growth. Plant Physiol 155: 1445-1457.
2. Allen, M.M., and Smith, A.J. (1969) Nitrogen chlorosis in blue-green algae. Arch Microbiol 69: 114-120.
3. Azuma, M., Osanai, T., Hirai, M.Y., and Tanaka, K. (2011) A response regulator Rre37 and an RNA polymerase sigma factor SigE represent two parallel pathways to activate sugar catabolism in a cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 52: 404-412.
4. Badawy, A.A., Morgan, C.J., and Turner, J.A. (2008) Application of the Phenomenex EZ:faasttrade mark amino acid analysis kit for rapid gas-chromatographic determination of concentration of plasma tryptophan and its brain uptake competitors. Amino Acids 34: 587-596.
5. Espinosa, J., Forchhammer, K., Burillo, S., and Contreras, A. (2006) Interaction network in cyanobacterial nitrogen regulation: PipX, a protein that interacts in a 2-oxoglutarate dependent manner with PII and NtcA. Mol Microbiol 61: 457-469.
6. García-Domínguez, M., Reyes, J.C., and Florencio, F.J. (2000) NtcA represses transcription of gifA and gifB, genes that encode inhibitors of glutamine synthetase type I from Synechocystis sp. PCC 6803. Mol Microbiol 35: 1192-1201.
7. Gorl, M., Sauer, J., Baier, T., and Forchhammer, K. (1998) Nitrogen-starvation-induced chlorosis in Synechococcus PCC 7942: adaptation to long-term survival. Microbiology 144: 2449-2458.
8. Hakkila, K., Antal, T., Gunnelius, L., Kurkela, J., Matthijs, H.C., Tyystjärvi, E., and Tyystjärvi, T. (2013) Group 2 sigma factor mutant ΔsigCDE of the cyanobacterium Synechocystis sp. PCC 6803 reveals functionality of both carotenoids and flavodiiron proteins in photoprotection of photosystem II. Plant Cell Physiol 54: 1780-1790.
9. Hasunuma, T., Kikuyama, F., Matsuda, M., Aikawa, S., Izumi, Y., and Kondo, A. (2013) Dynamic metabolic profiling of cyanobacterial glycogen biosynthesis under conditions of nitrate depletion. J Exp Bot 64: 2943-2954.
10. Hauf, W., Schlebusch, M., Hüge, J., Kopka, J., Hagemann, M., and Forchhammer, K. (2013) Metabolic changes in Synechocystis PCC6803 upon nitrogen-starvation: excess NADPH sustains polyhydroxybutyrate accumulation. Metabolites 3: 101-118.
11. Herrero, A., Muro-Pastor, A.M., and Flores, E. (2001) Nitrogen control in cyanobacteria. J Bacteriol 183: 411-425.
12. Imamura, S., Yoshihara, S., Nakano, S., Shiozaki, N., Yamada, A., Tanaka, K., etal. (2003) Purification, characterization, and gene expression of all sigma factors of RNA polymerase in a cyanobacterium. J Mol Biol 325: 857-872.
13. Kanesaki, Y., Shiwa, Y., Tajima, N., Suzuki, M., Watanabe, S., Sato, N., etal. (2012) Identification of substrain-specific mutations by massively parallel whole-genome resequencing of Synechocystis sp. PCC 6803. DNA Res 19: 67-79.
14. Krasikov, V., Aguirre von Wobeser, E., Dekker, H.L., Huisman, J., and Matthijs, H.C. (2012) Time-series resolution of gradual nitrogen starvation and its impact on photosynthesis in the cyanobacterium Synechocystis PCC 6803. Physiol Plant 145: 426-439.
15. Luque, I., Flores, E., and Herrero, A. (1994) Molecular mechanism for the operation of nitrogen control in cyanobacteria. EMBO J 13: 2862-2869.
16. Mitschke, J., Vioque, A., Haas, F., Hess, W.R., and Muro-Pastor, A.M. (2011) Dynamics of transcriptional start site selection during nitrogen stress-induced cell differentiation in Anabaena sp. PCC7120. Proc Natl Acad Sci USA 108: 20130-20135.
17. Muro-Pastor, A.M., Herrero, A., and Flores, E. (2001a) Nitrogen-regulated group 2 sigma factor from Synechocystis sp. strain PCC 6803 involved in survival under nitrogen stress. J Bacteriol 183: 1090-1095.
18. Muro-Pastor, M.I., Reyes, J.C., and Florencio, F.J. (2001b) Cyanobacteria perceive nitrogen status by sensing intracellular 2-oxoglutarate levels. J Biol Chem 276: 38320-38328.
19. Muro-Pastor, M.I., Reyes, J.C., and Florencio, F.J. (2005) Ammonium assimilation in cyanobacteria. Photosynth Res 83: 135-150.
20. Nagarajan, S., Sherman, D.M., Shaw, I., and Sherman, L.A. (2012) Functions of the duplicated hik31 operons in central metabolism and responses to light, dark, and carbon sources in Synechocystis sp. strain PCC 6803. J Bacteriol 194: 448-459.
21. Oikawa, A., Matsuda, F., Kikuyama, M., Mimura, T., and Saito, K. (2011) Metabolomics of a single vacuole reveals metabolic dynamism in an alga Chara australis. Plant Physiol 157: 544-551.
22. Olmedo-Verd, E., Flores, E., Herrero, A., and Muro-Pastor, A.M. (2005) HetR-dependent and -independent expression of heterocyst-related genes in an Anabaena strain overproducing the NtcA transcription factor. J Bacteriol 187: 1985-1991.
23. Osanai, T., Kanesaki, Y., Nakano, T., Takahashi, H., Asayama, M., Shirai, M., etal. (2005) Positive regulation of sugar catabolic pathways in the cyanobacterium Synechocystis sp. PCC 6803 by the group 2 sigma factor SigE. J Biol Chem 280: 30653-30659.
24. Osanai, T., Imamura, S., Asayama, M., Shirai, M., Suzuki, I., Murata, N., and Tanaka, K. (2006) Nitrogen induction of sugar catabolic gene expression in Synechocystis sp. PCC 6803. DNA Res 13: 185-195.
25. Osanai, T., Oikawa, A., Azuma, M., Tanaka, K., Saito, K., Hirai, M.Y., and Ikeuchi, M. (2011) Genetic engineering of group 2 sigma factor SigE widely activates expression of sugar catabolic genes in Synechocystis species PCC 6803. J Biol Chem 286: 30962-30971.
26. Osanai, T., Kuwahara, A., Iijima, H., Toyooka, K., Sato, M., Tanaka, K., etal. (2013a) Pleiotropic effect of sigE over-expression on cell morphology, photosynthesis and hydrogen production in Synechocystis sp. PCC 6803. Plant J 76: 456-465.
27. Osanai, T., Numata, K., Oikawa, A., Kuwahara, A., Iijima, H., Doi, Y., etal. (2013b) Increased bioplastic production with an RNA polymerase sigma factor SigE during nitrogen starvation in Synechocystis sp. PCC 6803. DNA Res 20: 525-535.
28. Osanai, T., Oikawa, A., Numata, K., Kuwahara, A., Iijima, H., Doi, Y., etal. (2014a) Pathway-level acceleration of glycogen catabolism by a response regulator in the cyanobacterium Synechocystis species PCC 6803. Plant Physiol 164: 1831-1841.
29. Osanai, T., Oikawa, A., Shirai, T., Kuwahara, A., Iijima, H., Tanaka, K., etal. (2014b) Capillary electrophoresis-mass spectrometry reveals the distribution of carbon metabolites during nitrogen starvation in Synechocystis sp. PCC 6803. Environ Microbiol 16: 512-524.
30. Picossi, S., Flores, E., and Herrero, A. (2014) ChIP analysis unravels an exceptionally wide distribution of DNA binding sites for the NtcA transcription factor in a heterocyst-forming cyanobacterium. BMC Genomics 15: 22.
31. Rippka, R. (1988) Isolation and purification of cyanobacteria. Methods Enzymol 167: 3-27.
32. Schlebusch, M., and Forchhammer, K. (2010) Requirement of the nitrogen starvation-induced protein Sll0783 for polyhydroxybutyrate accumulation in Synechocystis sp. strain PCC 6803. Appl Environ Microbiol 76: 6101-6107.
33. Singh, A.K., and Sherman, L.A. (2005) Pleiotropic effect of a histidine kinase on carbohydrate metabolism in Synechocystis sp. strain PCC 6803 and its requirement for heterotrophic growth. J Bacteriol 187: 2368-2376.
34. Su, Z., Olman, V., Mao, F., and Xu, Y. (2005) Comparative genomics analysis of NtcA regulons in cyanobacteria: regulation of nitrogen assimilation and its coupling to photosynthesis. Nucleic Acids Res 33: 5156-5171.
35. Summerfield, T.C., and Sherman, L. (2007) Role of sigma factors in controlling global gene expression in light/dark transitions in the cyanobacterium Synechocystis sp. PCC 6803. J Bacteriol 189: 7829-7840.
36. Tyystjärvi, T., Huokko, T., Rantamäki, S., and Tyystjärvi, E. (2013) Impact of different group 2 sigma factors on light use efficiency and high salt stress in the cyanobacterium Synechocystis sp. PCC 6803. PLoS ONE 8: e63020.
37. Vega-Palas, M.A., Madueño, F., Herrero, A., and Flores, E. (1990) Identification and cloning of a regulatory gene for nitrogen assimilation in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 172: 643-647.
38. Vega-Palas, M.A., Herrero, A., and Flores, E. (1992) NtcA, a global nitrogen regulator from the cyanobacterium Synechococcus that belongs to the Crp family of bacterial regulators. Mol Microbiol 6: 1853-1859.
39. Williams, J.G.K. (1988) Construction of specific mutations in PSII photosynthetic reaction center by genetic engineering. Methods Enzymol 167: 766-778.