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Volume 151, Issue 8

Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses Free

Abstract

Cyanobacteria are equipped with numerous mechanisms that allow them to survive under conditions of nutrient starvation, some of which are unique to these organisms. This review surveys the molecular mechanisms underlying acclimation responses to nitrogen and phosphorus deprivation, with an emphasis on non-diazotrophic freshwater cyanobacteria. As documented for other micro-organisms, nutrient limitation of cyanobacteria elicits both general and specific responses. The general responses occur under any starvation condition and are the result of the stresses imposed by arrested anabolism. In contrast, the specific responses are acclimation processes that occur as a result of limitation for a particular nutrient; they lead to modification of metabolic and physiological routes to compensate for the restriction. First, the general acclimation processes are discussed, with an emphasis on modifications of the photosynthetic apparatus. The molecular mechanisms underlying specific responses to phosphorus and nitrogen-limitation are then outlined, and finally the cross-talk between pathways modulating specific and general responses is described.

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2005-08-01
2024-04-24
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References

  1. Aldehni M. F., Sauer J., Spielhaupter C., Schmid R., Forchhammer K. 2003; Signal transduction protein PII is required for NtcA-regulated gene expression during nitrogen deprivation in the cyanobacterium. Synechococcus elongatus strain PCC 7942. J Bacteriol 185:2582–2591 [CrossRef]
     [Google Scholar]
  2. Allen M. M. 1984; Cyanobacterial cell inclusions. Annu Rev Microbiol 38:1–25 [CrossRef]
     [Google Scholar]
  3. Allen M. M., Smith A. J. 1969; Nitrogen chlorosis in blue-green algae. Arch Mikrobiol 69:114–120 [CrossRef]
     [Google Scholar]
  4. Almiron M., Link A. J., Furlong D., Kolter R. 1992; A novel DNA-binding protein with regulatory and protective roles in starved. Escherichia coli. Genes Dev 6:2646–2654 [CrossRef]
     [Google Scholar]
  5. Arcondeguy T., Jack R., Merrick M. 2001; PII signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol Mol Biol Rev 65:80–105 [CrossRef]
     [Google Scholar]
  6. Asayama M., Imamura S., Yoshihara S. 10 other authors 2004; SigC, the group 2 sigma factor of RNA polymerase, contributes to the late-stage gene expression and nitrogen promoter recognition in the cyanobacterium. Synechocystis sp. strain PCC 6803. Biosci Biotechnol Biochem 68:477–487 [CrossRef]
     [Google Scholar]
  7. Badger M. R., Price G. D. 2003; CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609–622 [CrossRef]
     [Google Scholar]
  8. Baier K., Nicklisch S., Grundner C., Reinecke J., Lockau W. 2001; Expression of two nblA-homologous genes is required for phycobilisome degradation in nitrogen-starved Synechocystis sp. PCC6803. FEMS Microbiol Lett 195:35–39 [CrossRef]
     [Google Scholar]
  9. 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]
     [Google Scholar]
  10. Barker-Astrom K., Schelin J., Gustafsson P., Clarke A. K., Campbell D. A. 2005; Chlorosis during nitrogen starvation is altered by carbon dioxide and temperature status and is mediated by the ClpP1 protease in. Synechococcus elongatus. Arch Microbiol 183:66–69 [CrossRef]
     [Google Scholar]
  11. Bassler B. L. 2002; Small talk. Cell-to-cell communication in bacteria. Cell 109:421–424 [CrossRef]
     [Google Scholar]
  12. Bird C., Wyman M. 2003; Nitrate/nitrite assimilation system of the marine picoplanctonic cyanobacterium Synechococcus sp. strain WH 8103: effect of nitrogen source and availability on gene expression. Appl Environ Microbiol 69:7009–7018 [CrossRef]
     [Google Scholar]
  13. Burillo S., Luque I., Fuentes I., Contreras A. 2004; Interactions between the nitrogen signal transduction protein PII and N-acetyl glutamate kinase in organisms that perform oxygenic photosynthesis. J Bacteriol 186:3346–3354 [CrossRef]
     [Google Scholar]
  14. 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
     [Google Scholar]
  15. Collier J. L., Grossman A. R. 1994; A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO J 13:1039–1047
     [Google Scholar]
  16. de Alda J. A., Lichtle C., Thomas J. C., Houmard J. 2004; Immunolocalization of NblA, a protein involved in phycobilisome turnover, during heterocyst differentiation in cyanobacteria. Microbiology 150:1377–1384 [CrossRef]
     [Google Scholar]
  17. Delumeau O., Lewis R. J., Yudkin M. D. 2002; Protein-protein interactions that regulate the energy stress activation of sigmaB in Bacillus subtilis. J Bacteriol 184:5583–5589 [CrossRef]
     [Google Scholar]
  18. Desnues B., Cuny C., Gregori G., Dukan S., Aguilaniu H., Nystrom T. 2003; Differential oxidative damage and expression of stress defence regulons in culturable and non-culturable Escherichia coli cells. EMBO Rep 4:400–404 [CrossRef]
     [Google Scholar]
  19. Dolganov N., Grossman A. R. 1999; A polypeptide with similarity to phycocyanin alpha-subunit phycocyanobilin lyase involved in degradation of phycobilisomes. J Bacteriol 181:610–617
     [Google Scholar]
  20. Finkel S. E., Kolter R. 1999; Evolution of microbial diversity during prolonged starvation. Proc Natl Acad Sci U S A 96:4023–4027 [CrossRef]
     [Google Scholar]
  21. Flores E., Herrero A. 1994; Assimilatory nitrogen metabolism and its regulation. In The Molecular Biology of Cyanobacteria pp 487–517 Edited by Peschek G. A., Löffelhardt W., Schmetterer G. New York: Kluwer Academic;
     [Google Scholar]
  22. Forchhammer K. 1999; The PII protein in Synechococcus PCC 7942 senses and signals 2-oxoglutarate under ATP-replete conditions. In The Phototrophic Prokaryotes pp 549–553 Edited by Peschek G. A., Löffelhardt W., Schmetterer G. New York: Kluwer Academic;
     [Google Scholar]
  23. Forchhammer K. 2004; Global carbon/nitrogen control by PII signal transduction in cyanobacteria: from signals to targets. FEMS Microbiol Rev 28:319–333 [CrossRef]
     [Google Scholar]
  24. 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 [CrossRef]
     [Google Scholar]
  25. 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
     [Google Scholar]
  26. 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
     [Google Scholar]
  27. Frentzen M. 2004; Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: anionic membrane lipids and phosphate regulation. Curr Opin Plant Biol 7:270–276 [CrossRef]
     [Google Scholar]
  28. Glazer A. N. 1985; Light harvesting by phycobilisomes. Annu Rev Biophys Biophys Chem 14:47–77 [CrossRef]
     [Google Scholar]
  29. Gomez-Garcia M. R., Losada M., Serrano A. 2003; Concurrent transcriptional activation of ppa and ppx genes by phosphate deprivation in the cyanobacterium. Synechocystis sp. strain PCC 6803. Biochem Biophys Res Commun 302:601–609 [CrossRef]
     [Google Scholar]
  30. 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]
     [Google Scholar]
  31. Grillo J. F., Gibson J. 1979; Regulation of phosphate accumulation in the unicellular cyanobacterium. Synechococcus. J Bacteriol 140:508–517
     [Google Scholar]
  32. Grossman A. R., Schaefer M. R., Chiang G. G., Collier J. L. 1993; The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57:725–749
     [Google Scholar]
  33. Gruber T. M., Bryant D. A. 1998; Characterization of the alternative sigma-factors SigD and SigE in Synechococcus sp. strain PCC 7002. SigE is implicated in transcription of post-exponential-phase-specific genes. Arch Microbiol 169:211–219 [CrossRef]
     [Google Scholar]
  34. Hai T., Hein S., Steinbüchel A. 2001; Multiple evidence for widespread and general occurrence of type-III PHA synthases in cyanobacteria and molecular characterization of the PHA synthases from two thermophilic cyanobacteria. Chlorogloeopsis fritschii PCC 6912 and Synechococcus. sp. strain MA19. Microbiology 147:3047–3060
     [Google Scholar]
  35. Hecker M., Völker, U. 1998; Non-specific, general and multiple stress resistance of growth-restricted Bacillus subtilis cells by the expression of the sigmaB regulon. Mol Microbiol 29:1129–1136 [CrossRef]
     [Google Scholar]
  36. Heinrich A., Maheswaran M., Ruppert U., Forchhammer K. 2004; The Synechococcus elongatus PII signal transduction protein controls arginine synthesis by complex formation with N-acetyl-l-glutamate kinase. Mol Microbiol 52:1303–1314 [CrossRef]
     [Google Scholar]
  37. Helman Y., Tchernov D., Reinhold L., Shibata M., Ogawa T., Schwarz R., Ohad I., Kaplan A. 2003; Genes encoding A-type flavoproteins are essential for photoreduction of O2 in cyanobacteria. Curr Biol 13:230–235 [CrossRef]
     [Google Scholar]
  38. Herrero A., Muro-Pastor A. M., Flores E. 2001; Nitrogen control in cyanobacteria. J Bacteriol 183:411–425 [CrossRef]
     [Google Scholar]
  39. Herrero A., Muro-Pastor A. M., Valladares A., Flores E. 2004; Cellular differentiation and the NtcA transcription factor in filamentous cyanobacteria. FEMS Microbiol Rev 28:469–487 [CrossRef]
     [Google Scholar]
  40. Hisbergues M., Jeanjean R., Joset F., Bedu S, Tandeau de Marsac N. 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 [CrossRef]
     [Google Scholar]
  41. Hsiao H. Y., He Q., van Waasbergen L. G., Grossman A. R. 2004; Control of photosynthetic and high-light-responsive genes by the histidine kinase DspA: negative and positive regulation and interactions between signal transduction pathways. J Bacteriol 186:3882–3888 [CrossRef]
     [Google Scholar]
  42. Huckauf J., Nomura C., Forchhammer K., Hagemann M. 2000; Stress responses of Synechocystis sp. strain PCC 6803 mutants impaired in genes encoding putative alternative sigma factors. Microbiology 146:2877–2889
     [Google Scholar]
  43. Irmler A., Sanner S., Dierks H., Forchhammer K. 1997; Dephosphorylation of the phosphoprotein PII in Synechococcus PCC 7942: identification of an ATP and 2-oxoglutarate-regulated phosphatase activity. Mol Microbiol 26:81–90 [CrossRef]
     [Google Scholar]
  44. Kamberov E. S., Atkinson M. R., Ninfa A. J. 1995; The Escherichia coli PII signal transduction protein is activated upon binding 2-ketoglutarate and ATP. J Biol Chem 270:17797–17807 [CrossRef]
     [Google Scholar]
  45. Kaplan A., Reinhold L. 1999; CO2 concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 50:539–570 [CrossRef]
     [Google Scholar]
  46. Kornberg A., Rao N. N., Ault-Riche D. 1999; Inorganic polyphosphate: a molecule of many functions. Annu Rev Biochem 68:89–125 [CrossRef]
     [Google Scholar]
  47. 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]
     [Google Scholar]
  48. Lee H. M., Vazquez-Bermudez M. F., Tandeau de Marsac N. 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
     [Google Scholar]
  49. Lee H. M., Flores E., Forchhammer K., Herrero A., Tandeau de Marsac N. 2000; Phosphorylation of the signal transducer PII protein and an additional effector are required for the PII-mediated regulation of nitrate and nitrite uptake in the cyanobacterium. Synechococcus sp. PCC 7942. Eur J Biochem 267:591–600 [CrossRef]
     [Google Scholar]
  50. Li H., Sherman L. A. 2002; Characterization of Synechocystis sp. strain PCC 6803 and Delta nbl mutants under nitrogen-deficient conditions. Arch Microbiol 178:256–266 [CrossRef]
     [Google Scholar]
  51. Lindell D., Erdner D., Marie D., Prasil O., Koblizek M., LeGall F., Rippka R., Partensky F., Scanlan D. J., Post A. 2002; Nitrogen stress response of. Prochlorococcus strain PCC 9511 (oxyphotobacteria) involves contrasting regulation of ntcA and amt1. J Phycol 38:1113–1124 [CrossRef]
     [Google Scholar]
  52. Luque I., Flores E., Herrero A. 1994; Molecular mechanism for the operation of nitrogen control in cyanobacteria. EMBO J 13:2862–2869
     [Google Scholar]
  53. 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
     [Google Scholar]
  54. Luque I., Ochoa De Alda J. A., Richaud C., Zabulon G., Thomas J. C., Houmard J. 2003; The NblAI protein from the filamentous cyanobacterium Tolypothrix PCC 7601: regulation of its expression and interactions with phycobilisome components. Mol Microbiol 50:1043–1054 [CrossRef]
     [Google Scholar]
  55. Luque I., Vazquez-Bermudez M. F., Paz-Yepes J., Flores E., Herrero A. 2004; In vivo activity of the nitrogen control transcription factor NtcA is subjected to metabolic regulation in. Synechococcus sp. strain PCC 7942. FEMS Microbiol Lett 236:47–52 [CrossRef]
     [Google Scholar]
  56. MacColl R. 1998; Cyanobacterial phycobilisomes. J Struct Biol 124:311–334 [CrossRef]
     [Google Scholar]
  57. Maheswaran M., Urbanke C., Forchhammer K. 2004; Complex formation and catalytic activation by the PII signaling protein of. N-acetyl-l-glutamate kinase from Synechococcus elongatus strain PCC 7942. J Biol Chem 279:55202–55210 [CrossRef]
     [Google Scholar]
  58. Martinez A., Kolter R. 1997; Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J Bacteriol 179:5188–5194
     [Google Scholar]
  59. 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
     [Google Scholar]
  60. Paz-Yepes J., Flores E., Herrero A. 2003; Transcriptional effects of the signal transduction protein PII (glnB gene product) on NtcA-dependent genes in Synechococcus sp. PCC 7942. FEBS Lett 543:42–46 [CrossRef]
     [Google Scholar]
  61. Pena M. M., Bullerjahn G. S. 1995; The DpsA protein of Synechococcus sp. strain PCC7942 is a DNA-binding hemoprotein. Linkage of the Dps and bacterioferritin protein families. J Biol Chem 270:22478–22482 [CrossRef]
     [Google Scholar]
  62. Pena M. M., Burkhart W., Bullerjahn G. S. 1995; Purification and characterization of a Synechococcus sp. strain PCC 7942 polypeptide structurally similar to the stress-induced Dps/PexB protein of. Escherichia coli. Arch Microbiol 163:337–344 [CrossRef]
     [Google Scholar]
  63. Perelman A., Uzan A., Hacohen D., Schwarz R. 2003; Oxidative stress in Synechococcus sp. strain PCC 7942: various mechanisms for H2O2 detoxification with different physiological roles. J Bacteriol 185:3654–3660 [CrossRef]
     [Google Scholar]
  64. Perelman A., Shaltiel J., Sendersky E., Schwarz R. 2004; Use of flow cytometry for efficient isolation of cyanobacterial mutants deficient in modulation of pigment level. Biotechniques 36:948–950952
     [Google Scholar]
  65. Ray J. M., Bhaya D., Block M. A., Grossman A. R. 1991; Isolation, transcription, and inactivation of the gene for an atypical alkaline phosphatase of. Synechococcus sp. strain PCC 7942. J Bacteriol 173:4297–4309
     [Google Scholar]
  66. Reyes J. C., Muro-Pastor M. I., Florencio F. J. 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
     [Google Scholar]
  67. 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]
     [Google Scholar]
  68. 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 [CrossRef]
     [Google Scholar]
  69. Sauer J., Forchhammer K, Görl M. 1999; Nitrogen starvation in Synechococcus PCC 7942: involvement of glutamine synthetase and NtcA in phycobiliprotein degradation and survival. Arch Microbiol 172:247–255 [CrossRef]
     [Google Scholar]
  70. Sauer J., Dirmeier U., Forchhammer K. 2000; The Synechococcus strain PCC 7942 glnN product (glutamine synthetase III) helps recovery from prolonged nitrogen chlorosis. J Bacteriol 182:5615–5619 [CrossRef]
     [Google Scholar]
  71. 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]
     [Google Scholar]
  72. Scanlan D. J., West N. J. 2002; Molecular ecology of the marine cyanobacterial genera. Prochlorococcus and Synechococcus. FEMS Microbiol Ecol 40:1–12 [CrossRef]
     [Google Scholar]
  73. Schwarz R., Grossman A. R. 1998; A response regulator of cyanobacteria integrates diverse environmental signals and is critical for survival under extreme conditions. Proc Natl Acad Sci U S A 95:11008–11013 [CrossRef]
     [Google Scholar]
  74. Singh A. K., Sherman L. A. 2000; Identification of iron-responsive, differential gene expression in the cyanobacterium Synechocystis sp. strain PCC 6803 with a customized amplification library. J Bacteriol 182:3536–3543 [CrossRef]
     [Google Scholar]
  75. Suzuki S., Ferjani A., Suzuki I., Murata N. 2004; The SphS-SphR two component system is the exclusive sensor for the induction of gene expression in response to phosphate limitation in. Synechocystis. J Biol Chem 279:13234–13240 [CrossRef]
     [Google Scholar]
  76. Tandeau de Marsac N., Lee H. M. 1999; Regulation of carbon and nitrogen metabolism in the unicellular cyanobacteria Synechococcus spp. In The Phototrophic Prokaryotes pp 549–553 Edited by Peschek G. A., Loffelhardt W., Schmetterer G. New York: Kluwer Academic;
     [Google Scholar]
  77. Tanigawa R., Shirokane M., Maeda S. S., Omata T., Tanaka K., Takahashi H. 2002; Transcriptional activation of NtcA-dependent promoters of. Synechococcus sp. PCC 7942 by 2-oxoglutarate in vitro. Proc Natl Acad Sci U S A 99:4251–4255 [CrossRef]
     [Google Scholar]
  78. Tu C. J., Shrager J., Burnap R. L., Postier B. L., Grossman A. R. 2004; Consequences of a deletion in dspA on transcript accumulation in. Synechocystis. sp. strain PCC6803. J Bacteriol 186:3889–3902 [CrossRef]
     [Google Scholar]
  79. van Waasbergen L. G., Dolganov N., Grossman A. R. 2002; nblS, a gene involved in controlling photosynthesis-related gene expression during high light and nutrient stress in. Synechococcus elongatus PCC 7942. J Bacteriol 184:2481–2490 [CrossRef]
     [Google Scholar]
  80. Vazquez-Bermudez M. F., Paz-Yepes J., Herrero A., Flores E. 2002a; The NtcA-activated amt1 gene encodes a permease required for uptake of low concentrations of ammonium in the cyanobacterium Synechococcus sp. PCC 7942: Microbiology 148861–869
     [Google Scholar]
  81. Vazquez-Bermudez M. F., Herrero A., Flores E. 2002b; 2-Oxoglutarate increases the binding affinity of the NtcA (nitrogen control) transcription factor for the Synechococcus glnA promoter. FEBS Lett 512:71–74 [CrossRef]
     [Google Scholar]
  82. Vazquez-Bermudez M. F., Flores E., Herrero A. 2002c; Analysis of binding sites for the nitrogen-control transcription factor NtcA in the promoters of Synechococcus nitrogen-regulated genes. Biochim Biophys Acta 157895–98 [CrossRef]
     [Google Scholar]
  83. Vazquez-Bermudez M., Herrero A., Flores E. 2003; Carbon supply and 2-oxoglutarate effects on expression of nitrate reductase and nitrogen-regulated genes in. Synechococcus sp. strain PCC 7942. FEMS Microbiology Lett 221:155–159 [CrossRef]
     [Google Scholar]
  84. Wagner K. U., Masepohl B., Pistorius E. K. 1995; The cyanobacterium Synechococcus sp. strain PCC 7942 contains a second alkaline phosphatase encoded by phoV. Microbiology 141:3049–3058 [CrossRef]
     [Google Scholar]
  85. Wanner G., Henkelmann G., Schmidt A., Kost H. P. 1986; Nitrogen and sulfur starvation of the cyanobacterium Synechococcus 6301 – an ultrastructural, morphometrical, and biochemical comparison. Z Naturforsch, C, J Biosci 41:741–750
     [Google Scholar]
  86. Wolf S. G., Frenkiel D., Arad T., Finkel S. E., Kolter R., Minsky A. 1999; DNA protection by stress-induced biocrystallization. Nature 400:83–85 [CrossRef]
     [Google Scholar]
  87. Zubkov M. V., Fuchs B. M., Tarran G. A., Burkill P. H., Amann R. 2003; High rate of uptake of organic nitrogen compounds by Prochlorococcus cyanobacteria as a key to their dominance in oligotrophic oceanic waters. Appl Environ Microbiol 69:1299–1304 [CrossRef]
     [Google Scholar]
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Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses
Microbiology 151, 2503 (2005); https://doi.org/10.1099/mic.0.27883-0
/content/journal/micro/10.1099/mic.0.27883-0
/content/journal/micro/10.1099/mic.0.27883-0
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