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Review Article

Nitrogen metabolism in cyanobacteria: metabolic and molecular control, growth consequences and biotechnological applications

, , , & ORCID Icon
Pages 541-560 | Received 04 Aug 2017, Accepted 27 Feb 2018, Published online: 12 Mar 2018

References

  • Aichi M, Takatani N, Omata T. 2001. Role of NtcB in activation of nitrate assimilation genes in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol. 183:5840–5847.
  • Alfonso M, Perewoska I, Kirilovsky D. 2001. Redox control of ntcA gene expression in Synechocystis sp. PCC 6803. Nitrogen availability and electron transport regulate the levels of the NtcA protein. Plant Physiol. 125:969–981.
  • Allen AE, Dupont CL, Oborník M, Horák A, Nunes-Nesi A, McCrow JP, Zheng H, Johnson DA, Hu H, Fernie AR. 2011. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature. 473:203–207.
  • Altermann W, Kazmierczak J. 2003. Archean microfossils: a reappraisal of early life on Earth. Res Microbiol. 154:611–617.
  • Antia N, Harrison P, Oliveira L. 1991. The role of dissolved organic nitrogen in phytoplankton nutrition, cell biology and ecology. Phycologia. 30:1–89.
  • Asato Y. 2003. Toward an understanding of cell growth and the cell division cycle of unicellular photoautotrophic cyanobacteria. Cell Mol Life Sci. 60:663–687.
  • Asayama M, Imamura S. 2008. Stringent promoter recognition and autoregulation by the group 3 σ-factor SigF in the cyanobacterium Synechocystis sp. strain PCC 6803. Nucleic Acids Res. 36:5297–5305.
  • Azuma M, Osanai T, Hirai MY, 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.
  • Badger MR, Price GD, Long BM, Woodger FJ. 2006. The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism. J Exp Bot. 57:249–265.
  • Bandyopadhyay A, Elvitigala T, Welsh E, Stöckel J, Liberton M, Min H, Sherman LA, Pakrasi HB. 2011. Novel metabolic attributes of the genus Cyanothece, comprising a group of unicellular nitrogen-fixing cyanobacteria. mBio. 2:e00214–e00211.
  • Beck C, Hertel S, Rediger A, Lehmann R, Wiegard A, Kölsch A, Heilmann B, Georg J, Hess WR, Axmann IM. 2014. Daily expression pattern of protein-encoding genes and small noncoding RNAs in Synechocystis sp. strain PCC 6803. Appl Environ Microbiol. 80:5195–5206.
  • Beck C, Knoop H, Axmann IM, Steuer R. 2012. The diversity of cyanobacterial metabolism: genome analysis of multiple phototrophic microorganisms. BMC Genomics. 13:56.
  • Becker EW. 2007. Micro-algae as a source of protein. Biotechnol Adv. 25:207–210.
  • Bekker A, Holland HD, Wang PL, Rumble D, Stein HJ, Hannah JL, Coetzee LL, Beukes NJ. 2004. Dating the rise of atmospheric oxygen. Nature. 427:117–120.
  • Berg J, Tymoczko J, Stryer L. 2002. The glyoxylate cycle enables plants and bacteria to grow on acetate. Biochemistry (Mosc). 5th ed. New York: WH Freeman Publisher. http://www.ncbi.nlm.nih.gov/books/NBK22383.
  • Bergman B, Gallon JR, Rai AN, Stal LJ. 1997. N2 fixation by non-heterocystous cyanobacteria. FEMS Microbiol Rev. 19:139–185.
  • Bergman B, Sandh G, Lin S, Larsson J, Carpenter EJ. 2013. Trichodesmium—a widespread marine cyanobacterium with unusual nitrogen fixation properties. FEMS Microbiol Rev. 37:286–302.
  • Berman-Frank I, Lundgren P, Chen Y-B, Küpper H, Kolber Z, Bergman B, Falkowski P. 2001. Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science. 294:1534–1537.
  • Berman-Frank I, Lundgren P, Falkowski P. 2003. Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res Microbiol. 154:157–164.
  • Bird C, Wyman M. 2003. Nitrate/nitrite assimilation system of the marine picoplanktonic cyanobacterium Synechococcus sp. strain WH 8103: effect of nitrogen source and availability on gene expression. Appl Environ Microbiol. 69:7009–7018.
  • Bradley RW, Bombelli P, Lea-Smith DJ, Howe CJ. 2013. Terminal oxidase mutants of the cyanobacterium Synechocystis sp. PCC 6803 show increased electrogenic activity in biological photo-voltaic systems. Phys Chem Chem Phys. 15:13611–13618.
  • Cavalcanti JHF, Esteves-Ferreira AA, Quinhones CGS, Pereira-Lima IA, Nunes-Nesi A, Fernie AR, Araújo WL. 2014. Evolution and functional implications of the tricarboxylic acid cycle as revealed by phylogenetic analysis. Genome Biol Evol. 6:2830–2848.
  • Chang Y, Takatani N, Aichi M, Maeda S-i, Omata T. 2013. Evaluation of the effects of PII deficiency and the toxicity of PipX on growth characteristics of the PII-less mutant of the cyanobacterium Synechococcus elongatus. Plant Cell Physiol. 54:1504–1514.
  • Chávez S, Lucena JM, Reyes JC, Florencio FJ, Candau P. 1999. The presence of glutamate dehydrogenase is a selective advantage for the cyanobacterium Synechocystis sp. strain PCC 6803 under nonexponential growth conditions. J Bacteriol. 181:808–813.
  • Chávez S, Reyes JC, Chauvat F, Florencio FJ, Candau P. 1995. The NADP-glutamate dehydrogenase of the cyanobacterium Synechocystis 6803: cloning, transcriptional analysis and disruption of the gdhA gene. Plant Mol Biol. 28:173–188.
  • Chellamuthu VR, Alva V, Forchhammer K. 2013. From cyanobacteria to plants: conservation of PII functions during plastid evolution. Planta. 237:451–462.
  • Crespo JL, García-Domínguez M, Florencio FJ. 1998. Nitrogen control of the glnN gene that codes for GS type III, the only glutamine synthetase in the cyanobacterium Pseudanabaena sp. PCC 6903. Mol Microbiol. 30:1101–1112.
  • Díaz-Troya S, López-Maury L, Sánchez-Riego AM, Roldán M, Florencio FJ. 2014. Redox regulation of glycogen biosynthesis in the cyanobacterium Synechocystis sp. PCC 6803: analysis of the AGP and glycogen synthases. Mol Plant. 7:87–100.
  • Dutta D, De D, Chaudhuri S, Bhattacharya S. 2005. Hydrogen production by cyanobacteria. Microb Cell Fact. 4:36.
  • Eisenberg D, Gill HS, Pfluegl GMU, Rotstein SH. 2000. Structure–function relationships of glutamine synthetases. Biochim Biophys Acta. 1477:122–145.
  • Eley JH. 1988. Glyoxylate cycle enzyme activities in the cyanobacterium Anacystis nidulans. J Phycol. 24:586–588.
  • Espinosa J, Castells MA, Laichoubi KB, Contreras A. 2009. Mutations at pipX suppress lethality of PII-deficient mutants of Synechococcus elongatus PCC 7942. J Bacteriol. 191:4863–4869.
  • Espinosa J, Castells MA, Laichoubi KB, Forchhammer K, Contreras A. 2010. Effects of spontaneous mutations in PipX functions and regulatory complexes on the cyanobacterium Synechococcus elongatus strain PCC 7942. Microbiology. 156:1517–1526.
  • Espinosa J, Forchhammer K, Burillo S, 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.
  • Espinosa J, Forchhammer K, Contreras A. 2007. Role of the Synechococcus PCC 7942 nitrogen regulator protein PipX in NtcA-controlled processes. Microbiology. 153:711–718.
  • Espinosa J, Rodríguez-Mateos F, Salinas P, Lanza VF, Dixon R, de la Cruz F, Contreras A. 2014. PipX, the coactivator of NtcA, is a global regulator in cyanobacteria. Proc Natl Acad Sci USA. 111:E2423–E2430.
  • Esteves-Ferreira AA, Cavalcanti JHF, Vaz MGMV, Alvarenga LV, Nunes-Nesi A, Araújo WL. 2017. Cyanobacterial nitrogenases: phylogenetic diversity, regulation and functional predictions. Genet Mol Biol. 40:261–275.
  • Esteves-Ferreira AA, Inaba M, Obata T, Fort A, Fleming GT, Araújo WL, Fernie AR, Sulpice R. 2017. A novel mechanism, linked to cell density, largely controls cell division in Synechocystis. Plant Physiol. 174:2166–2182.
  • Fay P. 1992. Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev. 56:340–373.
  • Feria Bourrellier AB, Valot B, Guillot A, Ambard-Bretteville F, Vidal J, Hodges M. 2010. Chloroplast acetyl-CoA carboxylase activity is 2-oxoglutarate-regulated by interaction of PII with the biotin carboxyl carrier subunit. PNAS. 107:502–507.
  • Finzi-Hart JA, Pett-Ridge J, Weber PK, Popa R, Fallon SJ, Gunderson T, Hutcheon ID, Nealson KH, Capone DG. 2009. Fixation and fate of C and N in the cyanobacterium Trichodesmium using nanometer-scale secondary ion mass spectrometry. PNAS. 106:6345–6350.
  • Florencio FJ, Marqués S, Candau P. 1987. Identification and characterization of a glutamate dehydrogenase in the unicellular cyanobacterium Synechocystis PCC 6803. FEBS Lett. 223:37–41.
  • Flores E, Frías JE, Rubio LM, Herrero A. 2005. Photosynthetic nitrate assimilation in cyanobacteria. Photosyn Res. 83:117–133.
  • Flores E, Herrero A. 2005. Nitrogen assimilation and nitrogen control in cyanobacteria. Biochem Soc Trans. 33:164–167.
  • Fokina O, Chellamuthu V-R, Forchhammer K, Zeth K. 2010a. Mechanism of 2-oxoglutarate signaling by the Synechococcus elongatus PII signal transduction protein. PNAS. 107:19760–19765.
  • Fokina O, Chellamuthu V-R, Zeth K, Forchhammer K. 2010b. A novel signal transduction protein PII variant from Synechococcus elongatus PCC 7942 indicates a two-step process for NAGK–PII complex formation. J Mol Biol. 399:410–421.
  • Fokina O, Herrmann C, Forchhammer K. 2011. Signal-transduction protein P(II) from Synechococcus elongatus PCC 7942 senses low adenylate energy charge in vitro. Biochem J. 440:147–156.
  • Forcada-Nadal A, Forchhammer K, Rubio V. 2014. SPR analysis of promoter binding of Synechocystis PCC6803 transcription factors NtcA and CRP suggests cross-talk and sheds light on regulation by effector molecules. FEBS Lett. 588:2270–2276.
  • Forcada-Nadal A, Palomino-Schätzlein M, Neira JL, Pineda-Lucena A, Rubio V. 2017. The PipX protein, when not bound to its targets, has its signaling C-terminal helix in a flexed conformation. Biochemistry. 56:3211–3224.
  • Forchhammer K, de Marsac NT. 1995a. Phosphorylation of the PII protein (glnB gene product) in the cyanobacterium Synechococcus sp. strain PCC 7942: analysis of in vitro kinase activity. J Bacteriol. 177:5812–5817.
  • Forchhammer K, de Marsac N. 1995b. Functional analysis of the phosphoprotein PII (glnB gene product) in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol. 177:2033–2040.
  • Forchhammer K, Hedler A. 1997. Phosphoprotein PII from cyanobacteria-analysis of functional conservation with the PII signal-transduction protein from Escherichia coli. Eur J Biochem. 244:869–875.
  • Forchhammer K, Lüddecke J. 2016. Sensory properties of the PII signalling protein family. FEBS J. 283:425–437.
  • Forchhammer K. 2004. Global carbon/nitrogen control by PII signal transduction in cyanobacteria: from signals to targets. FEMS Microbiol Rev. 28:319–333.
  • Foster JS, Singh AK, Rothschild LJ, Sherman LA. 2007. Growth-phase dependent differential gene expression in Synechocystis sp. strain PCC 6803 and regulation by a group 2 sigma factor. Arch Microbiol. 187:265–279.
  • Frías JE, Mérida A, Herrero A, Martín-Nieto J, Flores E. 1993. General distribution of the nitrogen control gene ntcA in cyanobacteria. J Bacteriol. 175:5710–5713.
  • Frommeyer M, Wiefel L, Steinbüchel A. 2014. Features of the biotechnologically relevant polyamide family “cyanophycins” and their biosynthesis in prokaryotes and eukaryotes. Crit Rev Biotechnol. 36:153–164.
  • García-Domínguez M, Reyes JC, Florencio FJ. 1997. Purification and characterization of a new type of glutamine synthetase from cyanobacteria. Eur J Biochem. 244:258–264.
  • García-Domínguez M, Reyes JC, Florencio FJ. 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.
  • García-Domínguez M, Florencio FJ. 1997. Nitrogen availability and electron transport control the expression of glnB gene (encoding PII protein) in the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol. 35:723–734.
  • Ge X, Cain K, Hirschberg R. 1990. Urea metabolism and urease regulation in the cyanobacterium Anabaena variabilis. Can J Microbiol. 36:218–222.
  • Ginn HP, Pearson LA, Neilan BA. 2010. NtcA from Microcystis aeruginosa PCC 7806 is autoregulatory and binds to the microcystin promoter. Appl Environ Microbiol. 76:4362–4368.
  • González López CV, García MdCC, Fernández FGA, Bustos CS, Chisti Y, Sevilla JMF. 2010. Protein measurements of microalgal and cyanobacterial biomass. Bioresour Technol. 101:7587–7591.
  • Gründel M, Knoop H, Steuer R. 2017. Activity and functional properties of the isocitrate lyase in the cyanobacterium Cyanothece sp. PCC 7424. Microbiology. 163:731–744.
  • Guerreiro AC, Benevento M, Lehmann R, van Breukelen B, Post H, Giansanti P, Altelaar AM, Axmann IM, Heck AJ. 2014. Daily rhythms in the cyanobacterium Synechococcus elongatus probed by high-resolution mass spectrometry-based proteomics reveals a small defined set of cyclic proteins. Mol Cell Proteomics. 13:2042–2055.
  • Guerrero MG, Vega JM, Losada M. 1981. The assimilatory nitrate-reducing system and its regulation. Annu Rev Plant Physiol. 32:169–204.
  • Harano Y, Suzuki I, Maeda S-i, Kaneko T, Tabata S, Omata T. 1997. Identification and nitrogen regulation of the cyanase gene from the cyanobacteria Synechocystis sp. strain PCC 6803 and Synechococcus sp. strain PCC 7942. J Bacteriol. 179:5744–5750.
  • Hauf W, Schmid K, Gerhardt ECM, Huergo LF, Forchhammer K. 2016. Interaction of the nitrogen regulatory protein GlnB (PII) with biotin carboxyl carrier protein (BCCP) controls acetyl-CoA levels in the cyanobacterium Synechocystis sp. PCC 6803. Front Microbiol. 7:1–14.
  • Heinrich A, Maheswaran M, Ruppert U, Forchhammer K. 2004. The Synechococcus elongatus P signal transduction protein controls arginine synthesis by complex formation with N-acetyl-l-glutamate kinase. Mol Microbiol. 52:1303–1314.
  • Hendry JI, Prasannan CB, Joshi A, Dasgupta S, Wangikar PP. 2016. Metabolic model of Synechococcus sp. PCC 7002: prediction of flux distribution and network modification for enhanced biofuel production. Bioresour Technol. 213:190–197.
  • Herrero A, Muro-Pastor AM, Flores E. 2001. Nitrogen control in cyanobacteria. J Bacteriol. 183:411–425.
  • Hisbergues M, Jeanjean R, Joset F, Tandeau de Marsac N, Bédu S. 1999. Protein PII regulates both inorganic carbon and nitrate uptake and is modified by a redox signal in Synechocystis PCC 6803. FEBS Lett. 463:216–220.
  • Huergo LF, Dixon R. 2015. The emergence of 2-oxoglutarate as a master regulator metabolite. Microbiol Mol Biol Rev. 79:419–435.
  • Irmler A, Forchhammer K. 2001. A PP2C-type phosphatase dephosphorylates the PII signaling protein in the cyanobacterium Synechocystis PCC 6803. PNAS. 98:12978–12983.
  • Jiang F, Wisén S, Widersten M, Bergman B, Mannervik B. 2000. Examination of the transcription factor NtcA-binding motif by in vitro selection of DNA sequences from a random library. J Mol Biol. 301:783–793.
  • Kamennaya NA, Chernihovsky M, Post AF. 2008. The cyanate utilization capacity of marine unicellular cyanobacteria. Limnol Oceanogr. 53:2485–2494.
  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S. 1996. 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. 3:109–136.
  • Kirilovsky D. 2007. Photoprotection in cyanobacteria: the orange carotenoid protein (OCP)-related non-photochemical-quenching mechanism. Photosyn Res. 93:7–16.
  • Klähn S, Schaal C, Georg J, Baumgartner D, Knippen G, Hagemann M, Muro-Pastor AM, Hess WR. 2015. The sRNA NsiR4 is involved in nitrogen assimilation control in cyanobacteria by targeting glutamine synthetase inactivating factor IF7. Proc Natl Acad Sci USA. 112:E6243–E6252.
  • Kleiner D. 1981. The transport of NH3 and NH4+ across biological membranes. Biochim Biophys Acta. 639:41–52.
  • Kloft N, Forchhammer K. 2005. Signal transduction protein PII phosphatase PphA is required for light-dependent control of nitrate utilization in Synechocystis sp. strain PCC 6803. J Bacteriol. 187:6683–6690.
  • Kloft N, Rasch G, Forchhammer K. 2005. Protein phosphatase PphA from Synechocystis sp. PCC 6803: the physiological framework of PII-P dephosphorylation. Microbiology. 151:1275–1283.
  • Knoop H, Gründel M, Zilliges Y, Lehmann R, Hoffmann S, Lockau W, Steuer R. 2013. Flux balance analysis of cyanobacterial metabolism: the metabolic network of Synechocystis sp. PCC 6803. PLoS Comput Biol. 9:e1003081.
  • Kobayashi M, Rodrı´guez Ro Lara C, Omata T. 1997. Involvement of the C-terminal domain of an ATP-binding subunit in the regulation of the ABC-type nitrate/nitrite transporter of the cyanobacterium Synechococcus sp. strain PCC 7942. J Biol Chem. 272:27197–27201.
  • Kobayashi M, Takatani N, Tanigawa M, Omata T. 2005. Posttranslational regulation of nitrate assimilation in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol. 187:498–506.
  • Komárek J, Kastovský J. 2003. Coincidences of structural and molecular characters in evolutionary lines of cyanobacteria. Algo Stud. 109:305–325.
  • Kornberg H. 2000. Krebs and his trinity of cycles. Nat Rev Mol Cell Biol. 1:225–228.
  • Kuniyoshi TM, Gonzalez A, Lopez-Gomollon S, Valladares A, Bes MT, Fillat MF, Peleato ML. 2011. 2-Oxoglutarate enhances NtcA binding activity to promoter regions of the microcystin synthesis gene cluster. FEBS Lett. 585:3921–3926.
  • Labella JI, Obrebska A, Espinosa J, Salinas P, Forcada-Nadal A, Tremiño L, Rubio V, Contreras A. 2016. Expanding the cyanobacterial nitrogen regulatory network: the GntR-like regulator PlmA interacts with the PII-PipX complex. Front Microbiol. 7:1677.
  • Laichoubi KB, Beez S, Espinosa J, Forchhammer K, Contreras A. 2011. The nitrogen interaction network in Synechococcus WH5701, a cyanobacterium with two PipX and two PII-like proteins. Microbiology. 157:1220–1228.
  • Laichoubi KB, Espinosa J, Castells MA, Contreras A. 2012. Mutational analysis of the cyanobacterial nitrogen regulator PipX. PLoS One. 7:e35845.
  • Lee H-M, Flores E, Herrero A, Houmard J, Tandeau de Marsac N. 1998. A role for the signal transduction protein PII in the control of nitrate/nitrite uptake in a cyanobacterium. FEBS Lett. 427:291–295.
  • Lee H-M, Vázquez-Bermúdez MF, de Marsac NT. 1999. The global nitrogen regulator NtcA regulates transcription of the signal transducer PII (GlnB) and influences its phosphorylation level in response to nitrogen and carbon supplies in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol. 181:2697–2702.
  • Liu H, Zhang H, Niedzwiedzki DM, Prado M, He G, Gross ML, Blankenship RE. 2013. Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science. 342:1104–1107.
  • Llácer JL, Contreras A, Forchhammer K, Marco-Marín C, Gil-Ortiz F, Maldonado R, Fita I, Rubio V. 2007. The crystal structure of the complex of PII and acetylglutamate kinase reveals how PII controls the storage of nitrogen as arginine. PNAS. 104:17644–17649.
  • Llácer JL, Espinosa J, Castells MA, Contreras A, Forchhammer K, Rubio V. 2010. Structural basis for the regulation of NtcA-dependent transcription by proteins PipX and PII. PNAS. 107:15397–15402.
  • Llácer JL, Fita I, Rubio V. 2008. Arginine and nitrogen storage. Curr Opin Struct Biol. 18:673–681.
  • Lüddecke J, Forchhammer K. 2013. From PII signaling to metabolite sensing: a novel 2-oxoglutarate sensor that details PII-NAGK complex formation. PLoS One. 8:e83181.
  • Lüddecke J, Francois L, Spät P, Watzer B, Chilczuk T, Poschet G, Hell R, Radlwimmer B, Forchhammer K. 2017. PII protein-derived FRET sensors for quantification and live-cell imaging of 2-oxoglutarate. Sci Rep. 7:1–13.
  • Ludwig M, Bryant DA. 2012. Acclimation of the global transcriptome of the cyanobacterium Synechococcus sp. strain PCC 7002 to nutrient limitations and different nitrogen sources. Front Microbiol. 3:1–15.
  • Luque I, Flores E, Herrero A. 1994a. Molecular mechanism for the operation of nitrogen control in cyanobacteria. EMBO J. 13:2862–2869.
  • Luque I, Flores E, Herrero A. 1994b. Nitrate and nitrite transport in the cyanobacterium Synechococcus sp. PCC 7942 are mediated by the same permease. Biochim Biophys Acta. 1184:296–298.
  • Luque I, Zabulon G, Contreras A, Houmard J. 2001. Convergence of two global transcriptional regulators on nitrogen induction of the stress-acclimation gene nblA in the cyanobacterium Synechococcus sp. PCC 7942. Mol Microbiol. 41:937–947.
  • Ma C-W, Lüddecke J, Forchhammer K, Zeng A-P. 2014. Population shift of binding pocket size and dynamic correlation analysis shed new light on the anticooperative mechanism of P(II) protein. Proteins. 82:1048–1059.
  • Maeda S-i, Murakami A, Ito H, Tanaka A, Omata T. 2015. Functional characterization of the FNT family nitrite transporter of marine picocyanobacteria. Life. 5:432–446.
  • Maeda S-i, Omata T. 2009. Nitrite transport activity of the ABC-type cyanate transporter of the cyanobacterium Synechococcus elongatus. J Bacteriol. 191:3265–3272.
  • Maheswaran M, Ziegler K, Lockau W, Hagemann M, Forchhammer K. 2006. PII-regulated arginine synthesis controls accumulation of cyanophycin in Synechocystis sp. strain PCC 6803. J Bacteriol. 188:2730–2734.
  • Marino GT, Asato Y. 1986. Characterization of cell cycle events in the dark in Anacystis nidulans. Microbiology. 132:2123–2127.
  • McCormick AJ, Bombelli P, Lea-Smith DJ, Bradley RW, Scott AM, Fisher AC, Smith AG, Howe CJ. 2013. Hydrogen production through oxygenic photosynthesis using the cyanobacterium Synechocystis sp. PCC 6803 in a bio-photoelectrolysis cell (BPE) system. Energy Environ Sci. 6:2682–2690.
  • Mehta PK, Hale TI, Christen P. 1993. Aminotransferases: demonstration of homology and division into evolutionary subgroups. Eur J Biochem. 214:549–561.
  • Mitamura O, Kawashima M, Maeda H. 2000. Urea degradation by picophytoplankton in the euphotic zone of Lake Biwa. Limnology. 1:19–26.
  • Mitamura O, Saijo Y. 1980. In situ measurement of the urea decomposition rate and its turnover rate in the Pacific Ocean. Mar Biol. 58:147–152.
  • Montesinos ML, Muro-Pastor AMa, Herrero A, Flores E. 1998. Ammonium/methylammonium permeases of a cyanobacterium: identification and analysis of three nitrogen-regulated amt genes in Synechocystis sp. J Biol Chem. 273:31463–31470.
  • Mori T, Binder B, Johnson CH. 1996. Circadian gating of cell division in cyanobacteria growing with average doubling times of less than 24 hours. PNAS. 93:10183–10188.
  • Mori T, Johnson CH. 2001. Independence of circadian timing from cell division in cyanobacteria. J Bacteriol. 183:2439–2444.
  • Mullineaux C. 2008. Phycobilisome-reaction centre interaction in cyanobacteria. Photosyn Res. 95:175–182.
  • Muro-Pastor AMa, Herrero A, Flores E. 2001. Nitrogen-regulated group 2 sigma factor from Synechocystis sp. strain PCC 6803 involved in survival under nitrogen stress. J Bacteriol. 183:1090–1095.
  • Muro-Pastor MI, Florencio FJ. 2003. Regulation of ammonium assimilation in cyanobacteria. Plant Physiol Biochem. 41:595–603.
  • Muro-Pastor MI, Reyes JC, Florencio FJ. 1996. The NADP+-isocitrate dehydrogenase gene (icd) is nitrogen regulated in cyanobacteria. J Bacteriol. 178:4070–4076.
  • Muro-Pastor MI, Reyes JC, Florencio FJ. 2005. Ammonium assimilation in cyanobacteria. Photosyn Res. 83:135–150.
  • Navarro F, Chávez S, Candau P, Florencio FJ. 1995. Existence of two ferredoxin-glutamate synthases in the cyanobacterium Synechocystis sp. PCC 6803. Isolation and insertional inactivation of gltB and gltS genes. Plant Mol Biol. 27:753–767.
  • Neilson A, Doudoroff M. 1973. Ammonia assimilation in blue-green algae. Arch Mikrobiol. 89:15–22.
  • Niu W, Kim Y, Tau G, Heyduk T, Ebright RH. 1996. Transcription activation at class II CAP-dependent promoters: two interactions between CAP and RNA polymerase. Cell. 87:1123–1134.
  • Nogales J, Gudmundsson S, Knight EM, Palsson BO, Thiele I. 2012. Detailing the optimality of photosynthesis in cyanobacteria through systems biology analysis. PNAS. 109:2678–2683.
  • Ohashi Y, Shi W, Takatani N, Aichi M, Maeda S-i, Watanabe S, Yoshikawa H, Omata T. 2011. Regulation of nitrate assimilation in cyanobacteria. J Exp Bot. 62:1411–1424.
  • Ohbayashi R, Watanabe S, Kanesaki Y, Narikawa R, Chibazakura T, Ikeuchi M, Yoshikawa H. 2013. DNA replication depends on photosynthetic electron transport in cyanobacteria. FEMS Microbiol Lett. 344:138–144.
  • Ohbayashi R, Yamamoto J-y, Watanabe S, Kanesaki Y, Chibazakura T, Miyagishima S-y, Yoshikawa H. 2017. Variety of DNA replication activity among cyanobacteria correlates with distinct respiration activity in the dark. Plant Cell Physiol. 58:279–286.
  • Okuhara H, Matsumura T, Fujita Y, Hase T. 1999. Cloning and inactivation of genes encoding ferredoxin- and NADH-dependent glutamate synthases in the cyanobacterium Plectonema boryanum. Imbalances in nitrogen and carbon assimilations caused by deficiency of the ferredoxin-dependent enzyme. Plant Physiol. 120:33–42.
  • Omata T, Andriesse X, Hirano A. 1993. Identification and characterization of a gene cluster involved in nitrate transport in the cyanobacterium Synechococcus sp. PCC7942. Mol Gen Genet. 236:193–202.
  • Osanai T, Azuma M, Tanaka K. 2007. Sugar catabolism regulated by light- and nitrogen-status in the cyanobacterium Synechocystis sp. PCC 6803. Photochem Photobiol Sci. 6:508–514.
  • Osanai T, Imamura S, Asayama M, Shirai M, Suzuki I, Murata N, Tanaka K. 2006. Nitrogen induction of sugar catabolic gene expression in Synechocystis sp. PCC 6803. DNA Res. 13:185–195.
  • Osanai T, Oikawa A, Iijima H, Kuwahara A, Asayama M, Tanaka K, Ikeuchi M, Saito K, Hirai MY. 2014. Metabolomic analysis reveals rewiring of Synechocystis sp. PCC 6803 primary metabolism by ntcA overexpression. Environ Microbiol. 16:3304–3317.
  • Pando BF, van Oudenaarden A. 2010. Coupling cellular oscillators-circadian and cell division cycles in cyanobacteria. Curr Opin Genet Dev. 20:613–618.
  • Parmar A, Singh NK, Pandey A, Gnansounou E, Madamwar D. 2011. Cyanobacteria and microalgae: a positive prospect for biofuels. Bioresour Technol. 102:10163–10172.
  • Paz-Yepes J, Flores E, Herrero A. 2003. Transcriptional effects of the signal transduction protein P(II) (glnB gene product) on NtcA-dependent genes in Synechococcus sp. PCC 7942. FEBS Lett. 543:42–46.
  • Paz-Yepes J, Herrero A, Flores E. 2007. The NtcA-regulated amtB gene is necessary for full methylammonium uptake activity in the cyanobacterium Synechococcus elongatus. J Bacteriol. 189:7791–7798.
  • Pearce J, Carr NG. 1967. The metabolism of acetate by the blue-green algae, Anabaena variabilis and Anacystis nidulans. J Gen Microbiol. 49:301–313.
  • Pearce J, Leach C, Carr N. 1969. The incomplete tricarboxylic acid cycle in the blue-green alga Anabaena variabilis. J Gen Microbiol. 55:371–378.
  • Peschek GA, Obinger C, Paumann M. 2004. The respiratory chain of blue-green algae (cyanobacteria). Physiol Plant. 120:358–369.
  • Pimentel JSM, Giani A. 2014. Microcystin production and regulation under nutrient stress conditions in toxic microcystis strains. Appl Environ Microbiol. 80:5836–5843.
  • Quintero MJ, Montesinos ML, Herrero A, Flores E. 2001. Identification of genes encoding amino acid permeases by inactivation of selected ORFs from the Synechocystis genomic sequence. Genome Res. 11:2034–2040.
  • Quintero MJ, Muro-Pastor AM, Herrero A, Flores E. 2000. Arginine catabolism in the cyanobacterium Synechocystis sp. strain PCC 6803 involves the urea cycle and arginase pathway. J Bacteriol. 182:1008–1015.
  • Rangel OA, Gómez-Baena G, López-Lozano A, Diez J, García-Fernández JM. 2009. Physiological role and regulation of glutamate dehydrogenase in Prochlorococcus sp. strain MIT9313. Environ Microbiol Rep. 1:56–64.
  • Rastogi RP, Sinha RP, Incharoensakdi A. 2014. The cyanotoxin-microcystins: current overview. Rev Environ Sci Biotechnol. 13:215.
  • Rees AP, Woodward EMS, Joint I. 2006. Concentrations and uptake of nitrate and ammonium in the Atlantic Ocean between 60°N and 50°S. Deep Sea Res Part 2 Top Stud Oceanogr. 53:1649–1665.
  • Reyes J, Muro-Pastor M, Florencio F. 1997. Transcription of glutamine synthetase genes (glnA and glnN) from the cyanobacterium Synechocystis sp. strain PCC 6803 is differently regulated in response to nitrogen availability. J Bacteriol. 179:2678–2689.
  • Reyes JC, Florencio FJ. 1994. A new type of glutamine synthetase in cyanobacteria: the protein encoded by the glnN gene supports nitrogen assimilation in Synechocystis sp. strain PCC 6803. J Bacteriol. 176:1260–1267.
  • Rodriguez IB, Ho T-Y. 2014. Diel nitrogen fixation pattern of Trichodesmium: the interactive control of light and Ni. Sci Rep. 4:1–5.
  • Rubin BE, Wetmore KM, Price MN, Diamond S, Shultzaberger RK, Lowe LC, Curtin G, Arkin AP, Deutschbauer A, Golden SS. 2015. The essential gene set of a photosynthetic organism. Proc Natl Acad Sci USA. 112:E6634–E6643.
  • Ruppert U, Irmler A, Kloft N, Forchhammer K. 2002. The novel protein phosphatase PphA from Synechocystis PCC 6803 controls dephosphorylation of the signalling protein PII. Mol Microbiol. 44:855–864.
  • Saelices L, Galmozzi CV, Florencio FJ, Muro-Pastor MI. 2011. Mutational analysis of the inactivating factors, IF7 and IF17 from Synechocystis sp. PCC 6803: critical role of arginine amino acid residues for glutamine synthetase inactivation. Mol Microbiol. 82:964–975.
  • Sakamoto T, Bryant DA. 2001. Requirement of nickel as an essential micronutrient for the utilization of urea in the marine cyanobacterium Synechococcus sp. PCC 7002. Microb Environ. 16:177–184.
  • Sakamoto T, Inoue-Sakamoto K, Bryant DA. 1999. A novel nitrate/nitrite permease in the marine cyanobacterium Synechococcus sp. strain PCC 7002. J Bacteriol. 181:7363–7372.
  • Sandh G, Ran L, Xu L, Sundqvist G, Bulone V, Bergman B. 2011. Comparative proteomic profiles of the marine cyanobacterium Trichodesmium erythraeum IMS101 under different nitrogen regimes. Proteomics. 11:406–419.
  • Sant’Anna FH, Trentini DB, de Souto Weber S, Cecagno R, da Silva SC, Schrank IS. 2009. The PII superfamily revised: a novel group and evolutionary insights. J Mol Evol. 68:322–336.
  • Sasaki Y, Nagano Y. 2004. Plant acetyl-CoA carboxylase: structure, biosynthesis, regulation, and gene manipulation for plant breeding. Biosci Biotechnol Biochem. 68:1175–1184.
  • Sauer J, Görl M, Forchhammer K. 1999. Nitrogen starvation in Synechococcus PCC 7942: involvement of glutamine synthetase and NtcA in phycobiliprotein degradation and survival. Arch Microbiol. 172:247–255.
  • Schirrmeister BE, de Vos JM, Antonelli A, Bagheri HC. 2013. Evolution of multicellularity coincided with increased diversification of cyanobacteria and the great oxidation event. PNAS. 110:1791–1796.
  • Schwamborn M. 1998. Chemical synthesis of polyaspartates: a biodegradable alternative to currently used polycarboxylate homo- and copolymers. Polym Degrad Stab. 59:39–45.
  • Singh S. 1990. Regulation of urease activity in the cyanobacterium Anabaena doliolum. FEMS Microbiol Lett. 67:79–84.
  • Singh S. 1992. Regulation of urease cellular levels in the cyanobacteria Anacystis nidulans and Nostoc muscorum. Biochem Physiol Pflanz. 188:33–38.
  • Smith AJ, London J, Stanier RY. 1967. Biochemical basis of obligate autotrophy in blue-green algae and Thiobacilli. J Bacteriol. 94:972–983.
  • Stal LJ. 2008. Nitrogen fixation in cyanobacteria. In: Encyclopedia of life sciences (ELS). Chichester: John Wiley & Sons Ltd.; p. 1–8.
  • Steinhauser D, Fernie AR, Araújo WL. 2012. Unusual cyanobacterial TCA cycles: not broken just different. Trends Plant Sci. 17:503–509.
  • Stephan DP, Ruppel HG, Pistorius EK. 2000. Interrelation between cyanophycin synthesis, l-arginine catabolism and photosynthesis in the cyanobacterium Synechocystis sp. strain PCC 6803. Z Naturforsch C Biosci. 55:927–942.
  • Steuer R, Knoop H, Machné R. 2012. Modelling cyanobacteria: from metabolism to integrative models of phototrophic growth. J Exp Bot. 63:2259–2274.
  • Steunou A-S, Jensen SI, Brecht E, Becraft ED, Bateson MM, Kilian O, Bhaya D, Ward DM, Peters JW, Grossman AR, et al. 2008. Regulation of nif gene expression and the energetics of N2 fixation over the diel cycle in a hot spring microbial mat. ISME J. 2:364–378.
  • Su Z, Olman V, Mao F, 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.
  • Suzuki I, Horie N, Sugiyama T, Omata T. 1995. Identification and characterization of two nitrogen-regulated genes of the cyanobacterium Synechococcus sp. strain PCC7942 required for maximum efficiency of nitrogen assimilation. J Bacteriol. 177:290–296.
  • Sweetlove LJ, Beard KF, Nunes-Nesi A, Fernie AR, Ratcliffe RG. 2010. Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci. 15:462–470.
  • Takatani N, Kobayashi M, Maeda S-i, Omata T. 2006. Regulation of nitrate reductase by non-modifiable derivatives of PII in the cells of Synechococcus elongatus strain PCC 7942. Plant Cell Physiol. 47:1182–1186.
  • Tamagnini P, Axelsson R, Lindberg P, Oxelfelt F, Wünschiers R, Lindblad P. 2002. Hydrogenases and hydrogen metabolism of cyanobacteria. Microbiol Mol Biol Rev. 66:1–20.
  • Tanigawa R, Shirokane M, Maeda S-i, Omata T, Tanaka K, Takahashi H. 2002. Transcriptional activation of NtcA-dependent promoters of Synechococcus sp. PCC 7942 by 2-oxoglutarate in vitro. PNAS. 99:4251–4255.
  • Thurotte A, Lopez Igual R, Wilson A, Comolet L, Bourcier de Carbon C, Xiao F, Kirilovsky D. 2015. Regulation of orange carotenoid protein activity in cyanobacterial photoprotection. Plant Physiol. 169:737–747.
  • Tian J, Bryk R, Itoh M, Suematsu M, Nathan C. 2005. Variant tricarboxylic acid cycle in Mycobacterium tuberculosis: identification of α-ketoglutarate decarboxylase. PNAS. 102:10670–10675.
  • Ting CS, Rocap G, King J, Chisholm SW. 2002. Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies. Trends Microbiol. 10:134–142.
  • Valladares A, Montesinos ML, Herrero A, Flores E. 2002. An ABC-type, high-affinity urea permease identified in cyanobacteria. Mol Microbiol. 43:703–715.
  • van Alphen P, Hellingwerf KJ. 2015. Sustained circadian rhythms in continuous light in Synechocystis sp. PCC6803 growing in a well-controlled photobioreactor. PLoS One. 10:e0127715.
  • van de Meene AML, Hohmann-Marriott MF, Vermaas WFJ, Roberson RW. 2006. The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Arch Microbiol. 184:259–270.
  • Vázquez-Bermúdez MaF, Herrero A, Flores E. 2002. 2-Oxoglutarate increases the binding affinity of the NtcA (nitrogen control) transcription factor for the Synechococcus glnA promoter. FEBS Lett. 512:71–74.
  • Vázquez-Bermúdez MF, Herrero A, Flores E. 2000. Uptake of 2-oxoglutarate in Synechococcus strains transformed with the Escherichia coli kgtP gene. J Bacteriol. 182:211–215.
  • Vega-Palas M, Flores E, Herrero A. 1992. NtcA, a global nitrogen regulator from the cyanobacterium Synechococcus that belongs to the Crp family of bacterial regulators. Mol Microbiol. 6:1853–1859.
  • Wang H-L, Postier BL, Burnap RL. 2004. Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator. J Biol Chem. 279:5739–5751.
  • Wang Y, Xu W, Chitnis PR. 2009. Identification and bioinformatic analysis of the membrane proteins of Synechocystis sp. PCC 6803. Proteome Sci. 7:1–12.
  • Watzer B, Engelbrecht A, Hauf W, Stahl M, Maldener I, Forchhammer K. 2015. Metabolic pathway engineering using the central signal processor P(II). Microb Cell Fact. 14:1–12.
  • Xiong W, Brune D, Vermaas WF. 2014. The γ-aminobutyric acid shunt contributes to closing the tricarboxylic acid cycle in Synechocystis sp. PCC 6803. Mol Microbiol. 93:786–796.
  • Xu K, Jiang H, Juneau P, Qiu B. 2012. Comparative studies on the photosynthetic responses of three freshwater phytoplankton species to temperature and light regimes. J Appl Phycol. 24:1113–1122.
  • Xu Y, Carr PD, Clancy P, Garcia-Dominguez M, Forchhammer K, Florencio F, Tandeau de Marsac N, Vasudevan SG, Ollis DL. 2003. The structures of the PII proteins from the cyanobacteria Synechococcus sp. PCC 7942 and Synechocystis sp. PCC 6803. Acta Crystallogr D Biol Crystallogr. 59:2183–2190.
  • Yang C, Hua Q, Shimizu K. 2002. Metabolic flux analysis in Synechocystis using isotope distribution from 13C-labeled glucose. Metab Eng. 4:202–216.
  • Yang F, Shen G, Schluchter WM, Zybailov B, Ganago A, Golbeck JH, Bryant DA. 1999. Structural and functional analyses of cyanobacterial photosystem I. In: Peschek GA, Löffelhardt W, Schmetterer G, editors. The phototrophic prokaryotes. Boston (MA): Springer; p. 21–33.
  • Yang Q, Pando BF, Dong G, Golden SS, van Oudenaarden A. 2010. Circadian gating of the cell cycle revealed in single cyanobacterial cells. Science. 327:1522–1526.
  • Yu J, Liberton M, Cliften PF, Head RD, Jacobs JM, Smith RD, Koppenaal DW, Brand JJ, Pakrasi HB. 2015. Synechococcus elongatus UTEX 2973, a fast growing cyanobacterial chassis for biosynthesis using light and CO2. Sci Rep. 5:1–10.
  • Zalutskaya Z, Kharatyan N, Forchhammer K, Ermilova E. 2015. Reduction of PII signaling protein enhances lipid body production in Chlamydomonas reinhardtii. Plant Sci. 240:1–9.
  • Zeth K, Fokina O, Forchhammer K. 2014. Structural basis and target-specific modulation of ADP sensing by the Synechococcus elongatus P(II) signaling protein. J Biol Chem. 289:8960–8972.
  • Zhang S, Bryant DA. 2011. The tricarboxylic acid cycle in cyanobacteria. Science. 334:1551–1553.
  • Zhang S, Bryant DA. 2015. Biochemical validation of the glyoxylate cycle in the cyanobacterium Chlorogloeopsis fritschii strain PCC 9212. J Biol Chem. 290:14019–14030.
  • Zhang S, Qian X, Chang S, Dismukes GC, Bryant DA. 2016. Natural and synthetic variants of the tricarboxylic acid cycle in cyanobacteria: introduction of the GABA shunt into Synechococcus sp. PCC 7002. Front Microbiol. 7:1–13.
  • Zhao M-X, Jiang Y-L, He Y-X, Chen Y-F, Teng Y-B, Chen Y, Zhang C-C, Zhou C-Z. 2010. Structural basis for the allosteric control of the global transcription factor NtcA by the nitrogen starvation signal 2-oxoglutarate. Proc Natl Acad Sci USA. 107:12487–12492.

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