Advertisement

How Do Cells Express Nutrient Limitation at the Molecular Level?

  • Nicholas H. Mann
Part of the NATO ASI Series book series (volume 38)

Abstract

Microbial growth in both marine and freshwater environments is frequently restricted by nutrient availability. The process of nutrient limitation is not a sudden transition from an actively growing to a non-growing state, but rather involves sequential changes that first enable the organism to utilize appropriate reserves, scavenge trace amounts of the limiting nutrient, or to utilize alternative less preferred sources of the nutrient and then to undergo the various physiological and ultrastructural changes that allow prolonged survival in the non-growing state. The nature of the limiting nutrient will vary in response to a range of factors (geographical, seasonal, anthropogenic etc), but will most commonly be for one of the quantitatively major nutrients, namely carbon, nitrogen, phosphorus and sulphur. Though there is evidence that trace elements such as iron and zinc may limit productivity in some environments. Furthermore, in the case of photoautotrophic micro-organisms it is reasonable to consider light as a nutrient.

Keywords

Acetyl Phosphate Histidine Protein Kinase High Affinity Transport System Starvation Survival Chloromuconate Cycloisomerase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aiba H and Mizuno T (1994) A novel gene whose expression is regulated by the response, SphR, in response to phosphate limitation in Synechococcus species PCC7942. Mol Microbiol 13: 25–34PubMedCrossRefGoogle Scholar
  2. Aiba H, Nagaya M, Mizuno T (1993) Sensor and regulator proteins from the cyanobacterium Synechococcus species PCC7942 that belong to the bacterial signal-transduction protein families: implication in the adaptive response to phosphate limitation. Mol Microbiol 8: 81–91PubMedCrossRefGoogle Scholar
  3. Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim BiophysActa 1098: 275–335CrossRefGoogle Scholar
  4. Bagg A and Neilands JB (1987) Molecular mechanism of regulation of siderophore-mediated iron assimilation. Microbiol Rev 51: 509–518.PubMedGoogle Scholar
  5. Bovy A, de Kruif J, de Vrieze G, Bornas M, Weisbeek P (1993) Iron-dependent protection of the Synechococcus ferredoxin I transcript against nucleolytic degradation requires cis-regulatory sequences in the 5′ part of the messenger RNA. Plant Mol Biol 22: 1047–1065PubMedCrossRefGoogle Scholar
  6. Bovy A, de Vrieze G, Bornas M, Weisbeek P (1992) Transcriptional regulation of the plastocyanin and cytochrome c553 genes from the cyanobacterium Anabaena species PCC 7937. Mol Microbiol 6: 1507–1513PubMedCrossRefGoogle Scholar
  7. Brahamsha B (1993) Identification of multiple RNA polymerase sigma factor omologs in cyanobacteria: group 2 sigmas in Anabaena sp. strain PCC 7120. Cyanobacterial Workshop Abstracts p22Google Scholar
  8. Briat J-F (1992) Iron assimilation and storage in prokaryotes. J Gen Microbiol 138: 2475–2483PubMedGoogle Scholar
  9. Briggs LM, Pecoraro VL, Mcintosh L (1990) Copper-induced expression, cloning, and regulatory studies of the plastocyanin gene from the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 15: 633–642PubMedCrossRefGoogle Scholar
  10. Buikema WJ and Haselkorn R (1993) Molecular genetics of cyanobacterial development. Ann Rev Plant Physiol Plant Mol Biol 44: 33–52CrossRefGoogle Scholar
  11. Burnap RL, Troyan T, Sherman LA (1993) The highly abundant chlorophyll-protein complex of iron-deficient Synechococcus sp. PCC7942 (CP43’) is encoded by the isiA gene. Plant Physiol 103: 893–902PubMedCrossRefGoogle Scholar
  12. Carr NG and Wyman M (1986) Cyanobacteria: their biology in relation to the oceanic phytoplankton. In Photosynthetic Picoplankton. Platt T, Li WKW (eds) Can Bull Fish Aquat Sci 214: 121–158Google Scholar
  13. Caslake LF and Bryant DA (1993) Characterization of sigma factors associated with the RNA polymerase of the unicellular cyanobacterium Synechococcus sp. PCC 7002. Cyanobacterial Workshop Abstracts p30Google Scholar
  14. Chastain CJ, Brusca JS, Ramasubramanian TS, Golden JW (1990) A sequence specific DNA-binding factor (VF1) from Anabaena sp. strain PCC 7120 vegetative cells binds to three adjacent sites in the xisA upstream region. J Bacteriol 172: 5044–5051PubMedGoogle Scholar
  15. Collier JL and Grossman AR (1992) Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: Not all bleaching is the same. J Bacteriol 174: 4718–4726PubMedGoogle Scholar
  16. Collier JL and Grossman AR (1993) Two novel genes involved in the biosynthesis of the photosynthetic apparatus in Synechococcus sp. strain PCC 7942. Cyanobacterial Workshop Abstracts p34Google Scholar
  17. Collier JL and Grossman AR (1994) A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO Journal 13: 1039–1047PubMedGoogle Scholar
  18. Doige CA and Ames GF (1993) ATP-dependent transport systems in bacteria and humans: relevance to cystic fibrosis and multidrug resistance. Annu Rev Microbiol 47: 291–319PubMedCrossRefGoogle Scholar
  19. Fagan MJ and Saier MH Jr (1994) P-type ATPases of eukaryotes and bacteria: Sequence analyses and construction of phylogenetic trees. J Mol Evol 38: 57–99PubMedCrossRefGoogle Scholar
  20. 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: 5710–5713PubMedGoogle Scholar
  21. Gentry DR, Hernandez VJ, Nguyen LH, Jensen DB, Cashel M (1993) Synthesis of the stationary phase sigma factor σS is positively regulated by ppGpp. J Bacteriol 175: 7982–7989PubMedGoogle Scholar
  22. Ghassemian M, Wong B, Ferreira F, Markley JL, Straus NA (1994): Cloning, sequencing and transcriptional studies of the genes for cytochrome c-555 and plastocyanin from Anabaena sp. PCC 7120. Microbiology 140: 1151–1159PubMedCrossRefGoogle Scholar
  23. Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57: 725–749PubMedGoogle Scholar
  24. Green LS and Grossman AR (1988) Changes in sulfate transport characteristics and protein composition of Anacystis nidulans during sulfur deprivation. J Bacteriol 170: 583–587PubMedGoogle Scholar
  25. Green LS, Laudenbach DE, Grossman AR (1989) A region of a cyanobacterial genome required for sulfate transport. Proc Natl Acad Sci USA 86: 1949–1953PubMedCrossRefGoogle Scholar
  26. Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Boil 8: 67–113CrossRefGoogle Scholar
  27. Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57: 725–749PubMedGoogle Scholar
  28. Guest JR (1992) Oxygen regulated gene expression in Escherichia coli. J Gen Microbiol 138: 2253–2263Google Scholar
  29. Hudson, RJM and Morel FMM (1993) Trace metal transport by marine microorganisms: implications of metal coordination kinetics. Deep-Sea Res 40: 129–150CrossRefGoogle Scholar
  30. Huisman GW and Kolter R (1994) Sensing starvation: a homoserine lactone-dependent signaling pathway in Escherichia coli. Science 265: 537–539.PubMedCrossRefGoogle Scholar
  31. Hyde SC, Emsley P, Hartshorn MJ, Mimmack MM, Gileadi U (1990) Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature 346: 362–365PubMedCrossRefGoogle Scholar
  32. Kanamaru K, Kashiwagi S, Mizuno T (1993) The cyanobacterium, Synechococcus sp. PCC7942, possesses two distinct genes encoding cation-transporting P-type ATPases. FEBS Lett 330: 99–104PubMedCrossRefGoogle Scholar
  33. Kanamaru K, Kashiwagi S, Mizuno T (1994) A copper-transporting P-type ATPase found in the thylakoid of the cyanobacterium Synechococcus species PCC7942. Mol Microbiol 13:369–377PubMedCrossRefGoogle Scholar
  34. Kerry A, Laudenbach DE, Trick CG (1988) Influence of iron limitation and nitrogen source on growth and siderophore production by cyanobacteria. J Phycol 24: 566–571.Google Scholar
  35. Kjellenberg S, Albertson N, Flärd K, Holmquist L, Jouper-Jaan Å, Marouga R, Östling J, Svenblad B, Weichart D (1993) How do non-differentiating bacteria adapt to starvation. Antonie van Leewenhoek: 63: 333–341CrossRefGoogle Scholar
  36. Kolter R, Siegele DA, Tormo A (1993) The stationary phase of the bacterial life cycle. Annu Rev Microbiol 47: 855–874PubMedCrossRefGoogle Scholar
  37. Laudenbach DE (1993) The involvement of a plasmid in the acclimation of cyanobacteria to sulfur stress. Cyanobacterial Workshop Abstracts p69Google Scholar
  38. Laudenbach DE and Grossman AR (1991) Characterization and mutagenesis of sulfur-regulated genes in a cyanobacterium: Evidence for function in sulfate transport. J Bacteriol 173: 2739–2750PubMedGoogle Scholar
  39. Laudenbach DE, Reith ME, Straus NA (1988) Isolation, sequence analysis and transcriptional studies of the flavodoxin gene from Anacystis nidulans R2. J Bacteriol 170: 258–265PubMedGoogle Scholar
  40. Laulhère JP, Labouré AM, van Wuytswinkel O, Gagnon J and Briat JF (1992) Purification, characterization and function of bacterioferritin from the cyanobacterium Synechocystis PCC 6803. Biochem J 281: 785–793PubMedGoogle Scholar
  41. Leonhardt K and Straus NA (1992) An iron stress operon involved in photosynthetic electron transport in the marine cyanobacterium Synechococcus sp. PCC 7002. J Gen Microbiol 138: 1613–1621PubMedGoogle Scholar
  42. Lukat GS, McCleary WR, Stock AM, Stock JB Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc Natl Acad Sci USA 89: 718–722.Google Scholar
  43. Luque I, Flores E, Herrero A (1994) Molecular mechanism for the operation of nitrogen control in cyanobacteria. EMBO J 13: 2862–2869PubMedGoogle Scholar
  44. Mann N and Carr NG (1974) Control of macromolecular composition and cell division in the blue-green alga Anacystis nidulans. J Gen Microbiol 83: 399–405.Google Scholar
  45. Mann N, Carr NG, Midgley JEM (1975) RNA synthesis and the accumulation of guanine nucleotides during growth shift down in the blue-green alga Anacystis nidulans. Biochim Biophys Acta 402: 41–50Google Scholar
  46. Mann NH, Scanlan DJ (1994) The SphX protein of Synechococcus species PCC 7942 belongs to a family of phosphate binding proteins. Mol Microbiol. In pressGoogle Scholar
  47. Mazel D and Marlière P (1989) Adaptive eradication of methionine and cysteine from cyanobacterial light harvesting proteins. Nature 341: 245–248PubMedCrossRefGoogle Scholar
  48. Matin A, Auger EA, Blum PH, Schultz JE (1989) Genetic basis of starvation survival in nondifferentiating bacteria. Annu Rev Microbiol 43: 293–316PubMedCrossRefGoogle Scholar
  49. McCleary WR, Stock JB, Ninfa AJ (1993) Is acetyl phosphate a global signal in Escherichia coli? J Bacteriol 175: 2793–2798PubMedGoogle Scholar
  50. Morel FMM, Reinfelder JR, Roberts SB, Chamberlain CP, Lee JG, Yee D (1994) Zinc and carbon cO-limitation of marine phytoplankton. Nature 369: 740–742.CrossRefGoogle Scholar
  51. Nagaya M, Aiba H, Mizuno T (1994) The sphR product, a two-component system response regulator protein, regulates phosphate assimilation in Synechococcus sp. strain PCC 7942 by binding to two sites upstream from the phoA promoter. J Bacteriol 176: 2210–2215PubMedGoogle Scholar
  52. Nakamura M, Yamagishi M, Yoshizaki F, Sugimura Y (1992) The syntheses of plastocyanin and cytochrome c-553 are regulated by copper at the pre-translational level in a green alga, Pediastrum boryanum. J Biochem 111: 219–224PubMedGoogle Scholar
  53. Nyström T (1994) The glucose-starvation stimulon of Escherichia coli: induced and repressed synthesis of enzymes of central metabolic pathways and role of acetyl phosphate in gene expression and starvation survival. Mol Microbiol 12: 833–843PubMedCrossRefGoogle Scholar
  54. Omata T (1991) Cloning and characterization of the nrtA gene that encodes a 45 kDa protein involved in nitrate transport in the cyanobacterium Synechococcus PCC 7942. Plant Cell Physiol 32: 151–157Google Scholar
  55. 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: 193–202PubMedCrossRefGoogle Scholar
  56. Omata T and Ogawa T (1987) Immunochemical studies on the major proteins in cytoplasmic membranes of cyanobacteria. In Progress in photosynthesis research, Biggins J (ed) Vol 4. Martinus Nijhoff, Dordrecht, 309–302Google Scholar
  57. Price NM and Morel FMM (1990) Cadmium and cobalt substitution for zinc in a marine diatom. Nature 344: 658–660CrossRefGoogle Scholar
  58. Rao NN and Torriani A (1990) Molecular aspects of phosphate transport in Escherichia coli Mol Microbiol 4: 1083–1090Google Scholar
  59. Ray JM, Bhaya D, Block MA and Grossman AR (1991) Isolation, transcription, and inactivation of the gene for an atypical alkaline phosphatase of Synechococcus sp. strain PCC 7942. J Bacteriol 173: 4297–4309PubMedGoogle Scholar
  60. Reddy KJ, Bullerjahn GS, Sherman DM and Sherman LA (1988) Cloning, nucleotide sequence, and mutagenesis of a gene (irpA) involved in iron-deficient growth of the cyanobacterium Synechococcus sp. strain PCC7942. J Bacteriol 170: 4466–4476PubMedGoogle Scholar
  61. Ronen-Tarazi M, Schwarz R, Bouevitch A, Lieman-Hurwitz J, Erez J, Kaplan A (1995) Response of photosynthetic microorganisms to changing ambient concentrations of CO2- This volume 323–334Google Scholar
  62. Scanlan DJ, Mann NH, Carr NG (1993) The response of the picoplanktonic marine cyanobacterium Synechococcus species WH7803 to phosphate starvation involves a protein homologous to the periplasmic phosphate-binding protein of Escherichia coli. Mol Microbiol 10: 181–191PubMedCrossRefGoogle Scholar
  63. Shaw DJ, Rice DW, Guest JR (1983) Homology between CAP and Fnr, a regulator of anaerobic respiration in Escherichia coli. J Mol Biol 166: 241–247PubMedCrossRefGoogle Scholar
  64. Siegele DA and Kolter R (1992) Life after log. J Bacteriol 174: 345–348PubMedGoogle Scholar
  65. Stock JB, Ninfa AJ, Stock AM (1989) Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev 53: 450–490PubMedGoogle Scholar
  66. Swift S, Bainton NJ, Winson MK (1994) Gram-negative bacterial communication by N-acyl homoserine lactones: a universal language? Trends Microbiol 2: 193–198PubMedCrossRefGoogle Scholar
  67. Tandeau de Marsac N, Houmard J (1993) Adaptation of cyanobacteria to environmental stimuli: new steps towards molecular mechanisms. FEMS Microbiol Rev 104: 119–190.CrossRefGoogle Scholar
  68. Vega-Pala MA, 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: 1853–1859CrossRefGoogle Scholar
  69. Vega-Palas MA, Madueño F, Herrero A, Flores E (1990) Identification and cloning of a regulatory gene for nitrogen assimilation in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 172: 643–647PubMedGoogle Scholar
  70. Wagner F, Gimona M, Ahorn H, Peschek G A, Falkner G (1994) Isolation and functional reconstitution of a phosphate binding protein of the cyanobacterium Anacystis nidulans induced during phosphate-limited growth. J Biol Chem 269:5509–5511PubMedGoogle Scholar
  71. Wanner BL and Wilmes-Riesenberg MR (1992) Involvement of phospho-transacetylase, acetate kinase, and acetyl phosphate synthesis in control of the phosphate regulon in Escherichia coli. J Bacteriol 174: 2124–2130PubMedGoogle Scholar
  72. Wei TF, Ramasubramanian TS, Pu F, Golden JW (1993) Anabaena sp. strain PCC 7120 bifA gene encoding a sequence-specific DNA-binding protein cloned by in vivo transcriptional interference selection. J Bacteriol 175: 4025–4035PubMedGoogle Scholar
  73. Wei TF, Ramasubramanian TS, Golden JW (1994) Anabaena sp. strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development. J Bacteriol 176: 4473–4482PubMedGoogle Scholar
  74. Young CC and Bernlohr RW (1991) Elongation factor Tu is methylated in response to nutrient deprivation in Escherichia coli. J Bacteriol 173: 3096–3100.PubMedGoogle Scholar
  75. Zhang L, McSpadden B, Pakrasi HB, Whitmarsh J (1992) Copper-mediated regulation of cytochrome c553 and plastocyanin in the cyanobacterium Synechocystis 6803. J Biol Chem 267: 19054–19059PubMedGoogle Scholar
  76. Zinkel SS and Crothers DM (1991) Catabolite activator protein-induced DNA bending in transcriptional initiation. J Mol Biol 219: 201–205.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1995

Authors and Affiliations

  • Nicholas H. Mann
    • 1
  1. 1.Department of Biological SciencesUniversity of WarwickCoventryUK

Personalised recommendations