1887

Abstract

Cyanobacteria are photosynthetic prokaryotes that play a crucial role in the Earth’s nitrogen and carbon cycles. Nitrogen availability is one of the most important factors in cyanobacterial growth. Interestingly, filamentous non-diazotrophic cyanobacteria, such as sp. PCC 8005, have developed survival strategies that enable them to adapt to nitrogen deprivation. Metabolic studies recently demonstrated a substantial synthesis and accumulation of glycogen derived from amino acids during nitrogen starvation. Nevertheless, the regulatory mechanism of this adaptation is poorly understood. To the best of our knowledge, this study is the first proteomic and cellular analysis of sp. PCC 8005 under nitrogen depletion. Label-free differential proteomic analysis indicated the global carbon and nitrogen reprogramming of the cells during nitrogen depletion as characterized by an upregulation of glycogen synthesis and the use of endogenous nitrogen sources. The degradation of proteins and cyanophycin provided endogenous nitrogen when exogenous nitrogen was limited. Moreover, formamides, cyanates and urea were also potential endogenous nitrogen sources. The transporters of some amino acids and alternative nitrogen sources such as ammonium permease 1 were induced under nitrogen depletion. Intriguingly, although is a non-diazotrophic cyanobacterium, we observed the upregulation of HetR and HglK proteins, which are involved in heterocyst differentiation. Moreover, after a long period without nitrate, only a few highly fluorescent cells in each trichome were observed, and they might be involved in the long-term survival mechanism of this non-diazotrophic cyanobacterium under nitrogen deprivation.

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2014-06-01
2019-12-14
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References

  1. Aichi M., Omata T.. ( 1997;). Involvement of NtcB, a LysR family transcription factor, in nitrite activation of the nitrate assimilation operon in the cyanobacterium Synechococcus sp. strain PCC 7942. . J Bacteriol 179:, 4671–4675.[PubMed]
    [Google Scholar]
  2. 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. [CrossRef][PubMed]
    [Google Scholar]
  3. Aichi M., Yoshihara S., Yamashita M., Maeda S., Nagai K., Omata T.. ( 2006;). Characterization of the nitrate-nitrite transporter of the major facilitator superfamily (the nrtP gene product) from the cyanobacterium Nostoc punctiforme strain ATCC 29133. . Biosci Biotechnol Biochem 70:, 2682–2689. [CrossRef][PubMed]
    [Google Scholar]
  4. Aikawa S., Izumi Y., Matsuda F., Hasunuma T., Chang J. S., Kondo A.. ( 2012;). Synergistic enhancement of glycogen production in Arthrospira platensis by optimization of light intensity and nitrate supply. . Bioresour Technol 108:, 211–215. [CrossRef][PubMed]
    [Google Scholar]
  5. Allen M. M., Yuen C., Medeiros L., Zizlsperger N., Farooq M., Kolodny N. H.. ( 2005;). Effects of light and chloramphenicol stress on incorporation of nitrogen into cyanophycin in Synechocystis sp. strain PCC 6308. . Biochim Biophys Acta 1725:, 241–246. [CrossRef][PubMed]
    [Google Scholar]
  6. Baier K., Lehmann H., Stephan D. P., Lockau W.. ( 2004;). NblA is essential for phycobilisome degradation in Anabaena sp. strain PCC 7120 but not for development of functional heterocysts. . Microbiology 150:, 2739–2749. [CrossRef][PubMed]
    [Google Scholar]
  7. Berman-Frank I., Lundgren P., Falkowski P.. ( 2003;). Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. . Res Microbiol 154:, 157–164. [CrossRef][PubMed]
    [Google Scholar]
  8. Berman-Frank I., Quigg A., Finkel Z. V., Irwin A. J., Haramaty L.. ( 2007;). Nitrogen-fixation strategies and Fe requirements in cyanobacteria. . Limnol Oceanogr 52:, 2260–2269. [CrossRef]
    [Google Scholar]
  9. Bradford M. M.. ( 1976;). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. . Anal Biochem 72:, 248–254. [CrossRef][PubMed]
    [Google Scholar]
  10. Brown M.. ( 1996;). Photopigment isolation and characterization: the effect of fructose and light on Anabaena azollae phycobiliproteins. Synthesis of the vegetative cell type and the akinete type. Masters thesis, Virginia Union University;, Virginia, USA:.
    [Google Scholar]
  11. Buchholz B. E., Hayes P. K., Walsby A. E.. ( 1993;). The distribution of the outer gas vesicle protein, GvpC, on the Anabaena gas vesicle, and its ratio to GvpA. . J Gen Microbiol 139:, 2353–2363. [CrossRef][PubMed]
    [Google Scholar]
  12. Collier J. L., Grossman A. R.. ( 1992;). Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same. . J Bacteriol 174:, 4718–4726.[PubMed]
    [Google Scholar]
  13. 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. [CrossRef][PubMed]
    [Google Scholar]
  14. Fay P.. ( 1992;). Oxygen relations of nitrogen fixation in cyanobacteria. . Microbiol Rev 56:, 340–373.[PubMed]
    [Google Scholar]
  15. Flores E., Herrero A.. ( 1994;). Assimilatory nitrogen metabolism and its regulation. . In The Molecular Biology of Cyanobacteria, pp. 487–517. Edited by Bryant D. A... Dordrecht:: Klüwer Academic Publishers;. [CrossRef]
    [Google Scholar]
  16. Flores E., Frías J. E., Rubio L. M., Herrero A.. ( 2005;). Photosynthetic nitrate assimilation in cyanobacteria. . Photosynth Res 83:, 117–133. [CrossRef][PubMed]
    [Google Scholar]
  17. Fokina O., Chellamuthu V. R., Forchhammer K., Zeth K.. ( 2010;). Mechanism of 2-oxoglutarate signaling by the Synechococcus elongatus PII signal transduction protein. . Proc Natl Acad Sci U S A 107:, 19760–19765. [CrossRef][PubMed]
    [Google Scholar]
  18. 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. [CrossRef][PubMed]
    [Google Scholar]
  19. Forchhammer K.. ( 2008;). PII signal transducers: novel functional and structural insights. . Trends Microbiol 16:, 65–72. [CrossRef][PubMed]
    [Google Scholar]
  20. Forchhammer K., Tandeau de Marsac N.. ( 1995a;). Functional analysis of the phosphoprotein PII (glnB gene product) in the cyanobacterium Synechococcus sp. strain PCC 7942. . J Bacteriol 177:, 2033–2040.[PubMed]
    [Google Scholar]
  21. Forchhammer K., Tandeau de Marsac N.. ( 1995b;). 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.[PubMed]
    [Google Scholar]
  22. Forchhammer K., Irmler A., Kloft N., Ruppert U.. ( 2004;). P signalling in unicellular cyanobacteria: analysis of redox-signals and energy charge. . Physiol Plant 120:, 51–56. [CrossRef][PubMed]
    [Google Scholar]
  23. Görl M., Sauer J., Baier T., Forchhammer K.. ( 1998;). Nitrogen-starvation-induced chlorosis in Synechococcus PCC 7942: adaptation to long-term survival. . Microbiology 144:, 2449–2458. [CrossRef][PubMed]
    [Google Scholar]
  24. Hasunuma T., Kikuyama F., Matsuda M., Aikawa S., Izumi Y., Kondo A.. ( 2013;). Dynamic metabolic profiling of cyanobacterial glycogen biosynthesis under conditions of nitrate depletion. . J Exp Bot 64:, 2943–2954. [CrossRef][PubMed]
    [Google Scholar]
  25. Heinemann U., Engels D., Bürger S., Kiziak C., Mattes R., Stolz A.. ( 2003;). Cloning of a nitrilase gene from the cyanobacterium Synechocystis sp. strain PCC6803 and heterologous expression and characterization of the encoded protein. . Appl Environ Microbiol 69:, 4359–4366. [CrossRef][PubMed]
    [Google Scholar]
  26. Hendrickx L., De Wever H., Hermans V., Mastroleo F., Morin N., Wilmotte A., Janssen P., Mergeay M.. ( 2006;). Microbial ecology of the closed artificial ecosystem MELiSSA (Micro-Ecological Life Support System Alternative): reinventing and compartmentalizing the Earth’s food and oxygen regeneration system for long-haul space exploration missions. . Res Microbiol 157:, 77–86. [CrossRef][PubMed]
    [Google Scholar]
  27. Herrero A., Flores E.. ( 2008;). Nitrogen assimilation and C/N balance sensing. . In The Cyanobacteria: Molecular Biology, Genomics, and Evolution, pp. 335–382. Edited by Herrero A., Flores E... Norfolk:: Caister Academic Press;.
    [Google Scholar]
  28. Herrero A., Flores E., Guerrero M. G.. ( 1981;). Regulation of nitrate reductase levels in the cyanobacteria Anacystis nidulans, Anabaena sp. strain 7119, and Nostoc sp. strain 6719. . J Bacteriol 145:, 175–180.[PubMed]
    [Google Scholar]
  29. Herrero A., Muro-Pastor A. M., Flores E.. ( 2001;). Nitrogen control in cyanobacteria. . J Bacteriol 183:, 411–425. [CrossRef][PubMed]
    [Google Scholar]
  30. Irmler A., Forchhammer K.. ( 2001;). A PP2C-type phosphatase dephosphorylates the PII signaling protein in the cyanobacterium Synechocystis PCC 6803. . Proc Natl Acad Sci U S A 98:, 12978–12983. [CrossRef][PubMed]
    [Google Scholar]
  31. Janssen P. J., Morin N., Mergeay M., Leroy B., Wattiez R., Vallaeys T., Waleron K., Waleron M., Wilmotte A.. & other authors ( 2010;). Genome sequence of the edible cyanobacterium Arthrospira sp. PCC 8005. . J Bacteriol 192:, 2465–2466. [CrossRef][PubMed]
    [Google Scholar]
  32. Kebede E.. ( 1997;). Response of Spirulina platensis ( = Arthrospira fusiformis) from Lake Chitu, Ethiopia, to salinity stress from sodium salts. . J Appl Phycol 9:, 551–558.
    [Google Scholar]
  33. Kobayashi M., Rodríguez R., 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. [CrossRef][PubMed]
    [Google Scholar]
  34. Kolodny N. H., Bauer D., Bryce K., Klucevsek K., Lane A., Medeiros L., Mercer W., Moin S., Park D.. & other authors ( 2006;). Effect of nitrogen source on cyanophycin synthesis in Synechocystis sp. strain PCC 6308. . J Bacteriol 188:, 934–940. [CrossRef][PubMed]
    [Google Scholar]
  35. Krasikov V., Aguirre von Wobeser E., Dekker H. L., Huisman J., 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. [CrossRef][PubMed]
    [Google Scholar]
  36. Kumar K., Mella-Herrera R. A., Golden J. W.. ( 2010;). Cyanobacterial heterocysts. . Cold Spring Harb Perspect Biol 2:, a000315. [CrossRef][PubMed]
    [Google Scholar]
  37. Laurent S., Chen H., Bédu S., Ziarelli F., Peng L., Zhang C. C.. ( 2005;). Nonmetabolizable analogue of 2-oxoglutarate elicits heterocyst differentiation under repressive conditions in Anabaena sp. PCC 7120. . Proc Natl Acad Sci U S A 102:, 9907–9912. [CrossRef][PubMed]
    [Google Scholar]
  38. 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. [CrossRef][PubMed]
    [Google Scholar]
  39. Llácer J. L., Espinosa J., Castells M. A., Contreras A., Forchhammer K., Rubio V.. ( 2010;). Structural basis for the regulation of NtcA-dependent transcription by proteins PipX and PII. . Proc Natl Acad Sci U S A 107:, 15397–15402. [CrossRef][PubMed]
    [Google Scholar]
  40. Ludwig M., Bryant D. A.. ( 2012;). Acclimation of the global transcriptome of the cyanobacterium Synechococcus sp. strain PCC 7002 to nutrient limitations and different nitrogen sources. . Front Microbiol 3:, 145. [CrossRef][PubMed]
    [Google Scholar]
  41. Luque I., Flores E., Herrero A.. ( 1994;). Molecular mechanism for the operation of nitrogen control in cyanobacteria. . EMBO J 13:, 5794.[PubMed]
    [Google Scholar]
  42. 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. [CrossRef][PubMed]
    [Google Scholar]
  43. Maldener I., Muro-Pastor A. M.. ( 2010;). Cyanobacterial heterocysts. . In Encyclopedia of Life Sciences. Chichester:: Wiley;. http://dx.doi.org/10.1002/9780470015902.a0000306.pub2 [CrossRef]
    [Google Scholar]
  44. Markou G., Chatzipavlidis I., Georgakakis D.. ( 2012;). Effects of phosphorus concentration and light intensity on the biomass composition of Arthrospira (Spirulina) platensis.. World J Microbiol Biotechnol 28:, 2661–2670. [CrossRef][PubMed]
    [Google Scholar]
  45. McMaster T. J., Miles M. J., Walsby A. E.. ( 1996;). Direct observation of protein secondary structure in gas vesicles by atomic force microscopy. . Biophys J 70:, 2432–2436. [CrossRef][PubMed]
    [Google Scholar]
  46. Miller S. R., Martin M., Touchton J., Castenholz R. W.. ( 2002;). Effects of nitrogen availability on pigmentation and carbon assimilation in the cyanobacterium Synechococcus sp. strain SH-94-5. . Arch Microbiol 177:, 392–400. [CrossRef][PubMed]
    [Google Scholar]
  47. Mlouka A., Comte K., Castets A. M., Bouchier C., Tandeau de Marsac N.. ( 2004;). The gas vesicle gene cluster from Microcystis aeruginosa and DNA rearrangements that lead to loss of cell buoyancy. . J Bacteriol 186:, 2355–2365. [CrossRef][PubMed]
    [Google Scholar]
  48. Montoya J. P., Holl C. M., Zehr J. P., Hansen A., Villareal T. A., Capone D. G.. ( 2004;). High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. . Nature 430:, 1027–1032. [CrossRef][PubMed]
    [Google Scholar]
  49. Muro-Pastor M. I., Florencio F. J.. ( 2003;). Regulation of ammonium assimilation in cyanobacteria. . Plant Physiol Biochem 41:, 595–603. [CrossRef]
    [Google Scholar]
  50. Muro-Pastor M. I., Reyes J. C., Florencio F. J.. ( 2001;). Cyanobacteria perceive nitrogen status by sensing intracellular 2-oxoglutarate levels. . J Biol Chem 276:, 38320–38328.[PubMed]
    [Google Scholar]
  51. Muro-Pastor M. I., Reyes J. C., Florencio F. J.. ( 2005;). Ammonium assimilation in cyanobacteria. . Photosynth Res 83:, 135–150. [CrossRef][PubMed]
    [Google Scholar]
  52. Nomsawai P., Tandeau de Marsac N., Thomas J. C., Tanticharoen M., Cheevadhanarak S.. ( 1999;). Light regulation of phycobilisome structure and gene expression in Spirulina platensis C1 (Arthrospira sp. PCC 9438). . Plant Cell Physiol 40:, 1194–1202. [CrossRef]
    [Google Scholar]
  53. Osanai T., Tanaka K.. ( 2007;). Keeping in touch with PII: PII-interacting proteins in unicellular cyanobacteria. . Plant Cell Physiol 48:, 908–914. [CrossRef][PubMed]
    [Google Scholar]
  54. Osanai T., Oikawa A., Azuma M., Tanaka K., Saito K., Hirai M. Y., Ikeuchi M.. ( 2011;). Genetic engineering of group 2 sigma factor SigE widely activates expressions of sugar catabolic genes in Synechocystis species PCC 6803. . J Biol Chem 286:, 30962–30971. [CrossRef][PubMed]
    [Google Scholar]
  55. Page-Sharpe M., Behm C. A., Smith G. D.. ( 1998;). Cyanophycin and glycogen synthesis in a cyanobacterial Scytonema species in response to salt stress. . FEMS Microbiol Lett 160:, 11–15. [CrossRef]
    [Google Scholar]
  56. Picossi S., Valladares A., Flores E., Herrero A.. ( 2004;). Nitrogen-regulated genes for the metabolism of cyanophycin, a bacterial nitrogen reserve polymer: expression and mutational analysis of two cyanophycin synthetase and cyanophycinase gene clusters in heterocyst-forming cyanobacterium Anabaena sp. PCC 7120. . J Biol Chem 279:, 11582–11592. [CrossRef][PubMed]
    [Google Scholar]
  57. Powell E. O.. ( 1956;). Growth rate and generation time of bacteria, with special reference to continuous culture. . J Gen Microbiol 15:, 492–511. [CrossRef][PubMed]
    [Google Scholar]
  58. Richaud C., Zabulon G., Joder A., Thomas J. C.. ( 2001;). Nitrogen or sulfur starvation differentially affects phycobilisome degradation and expression of the nblA gene in Synechocystis strain PCC 6803. . J Bacteriol 183:, 2989–2994. [CrossRef][PubMed]
    [Google Scholar]
  59. Sakamoto T., Inoue-Sakamoto K., Bryant D. A.. ( 1999;). A novel nitrate/nitrite permease in the marine cyanobacterium Synechococcus sp. strain PCC 7002. . J Bacteriol 181:, 7363–7372.[PubMed]
    [Google Scholar]
  60. Sant’Anna F. H., Trentini D. B., de Souto Weber S., Cecagno R., da Silva S. C., Schrank I. S.. ( 2009;). The PII superfamily revised: a novel group and evolutionary insights. . J Mol Evol 68:, 322–336. [CrossRef][PubMed]
    [Google Scholar]
  61. Sauer J., Schreiber U., Schmid R., Völker U., Forchhammer K.. ( 2001;). Nitrogen starvation-induced chlorosis in Synechococcus PCC 7942. Low-level photosynthesis as a mechanism of long-term survival. . Plant Physiol 126:, 233–243. [CrossRef][PubMed]
    [Google Scholar]
  62. Schlebusch M., 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. [CrossRef][PubMed]
    [Google Scholar]
  63. Schwarz R., Forchhammer K.. ( 2005;). Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses. . Microbiology 151:, 2503–2514. [CrossRef][PubMed]
    [Google Scholar]
  64. Simon R. D.. ( 1973;). Measurement of the cyanophycin granule polypeptide contained in the blue-green alga Anabaena cylindrica.. J Bacteriol 114:, 1213–1216.[PubMed]
    [Google Scholar]
  65. Stensjö K., Ow S. Y., Barrios-Llerena M. E., Lindblad P., Wright P. C.. ( 2007;). An iTRAQ-based quantitative analysis to elaborate the proteomic response of Nostoc sp. PCC 7120 under N2 fixing conditions. . J Proteome Res 6:, 621–635. [CrossRef][PubMed]
    [Google Scholar]
  66. 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. [CrossRef][PubMed]
    [Google Scholar]
  67. van den Heuvel R. H., Curti B., Vanoni M. A., Mattevi A.. ( 2004;). Glutamate synthase: a fascinating pathway from L-glutamine to L-glutamate. . Cell Mol Life Sci 61:, 669–681. [CrossRef][PubMed]
    [Google Scholar]
  68. Vázquez-Bermúdez M. F., 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. [CrossRef][PubMed]
    [Google Scholar]
  69. Walsby A. E.. ( 1994;). Gas vesicles. . Microbiol Rev 58:, 94–144.[PubMed]
    [Google Scholar]
  70. Walsby A. E., Jüttner F.. ( 2006;). The uptake of amino acids by the cyanobacterium Planktothrix rubescens is stimulated by light at low irradiances. . FEMS Microbiol Ecol 58:, 14–22. [CrossRef][PubMed]
    [Google Scholar]
  71. Wang Z. P., Zhao Y.. ( 2005;). Morphological reversion of Spirulina (Arthrospira) platensis (Cyanophyta): from linear to helical. . J Phycol 41:, 622–628. [CrossRef]
    [Google Scholar]
  72. Yoo S. H., Keppel C., Spalding M., Jane J. L.. ( 2007;). Effects of growth condition on the structure of glycogen produced in cyanobacterium Synechocystis sp. PCC6803. . Int J Biol Macromol 40:, 498–504. [CrossRef][PubMed]
    [Google Scholar]
  73. Zarrouk C.. ( 1966;). Contribution à l'étude du cyanophycée. Influence de divers facteurs physiques et chimiques sur la croissance et la photosynthèse de Spirulina maxima, p. 74. PhD thesis, Université de Paris;, Paris, France:.
    [Google Scholar]
  74. Zhang C. C., Laurent S., Sakr S., Peng L., Bédu S.. ( 2006;). Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. . Mol Microbiol 59:, 367–375. [CrossRef][PubMed]
    [Google Scholar]
  75. Zhang J.-Y., Chen W.-L., Zhang C.-C.. ( 2009;). hetR and patS, two genes necessary for heterocyst pattern formation, are widespread in filamentous nonheterocyst-forming cyanobacteria. . Microbiology 155:, 1418–1426. [CrossRef][PubMed]
    [Google Scholar]
  76. 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 U S A 107:, 12487–12492. [CrossRef][PubMed]
    [Google Scholar]
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