1887

Abstract

The polyphosphate glucokinases can phosphorylate glucose to glucose 6-phosphate using polyphosphate as the substrate. ORF encodes a putative polyphosphate glucokinase in the filamentous heterocyst-forming cyanobacterium sp. PCC 7120. Here, ORF was heterologously expressed in , and its purified product was characterized. Enzyme activity assays revealed that All1371 is an active polyphosphate glucokinase that can phosphorylate both glucose and mannose in the presence of divalent cations . Unlike many other polyphosphate glucokinases, for which nucleoside triphosphates (e.g. ATP or GTP) act as phosphoryl group donors, All1371 required polyphosphate to confer its enzymic activity. The enzymic reaction catalysed by All1371 followed classical Michaelis–Menten kinetics, with  = 48.2 s at pH 7.5 and 28 °C and  = 1.76 µM and 0.118 mM for polyphosphate and glucose, respectively. Its reaction mechanism was identified as a particular multi-substrate mechanism called the ‘bi-bi ping-pong mechanism’. Bioinformatic analyses revealed numerous polyphosphate-dependent glucokinases in heterocyst-forming cyanobacteria. Viability of an sp. PCC 7120 mutant strain lacking was impaired under nitrogen-fixing conditions. GFP promoter studies indicate expression of under combined nitrogen deprivation. All1371 might play a substantial role in sp. PCC 7120 under these conditions.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.081836-0
2014-12-01
2019-11-12
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/12/2807.html?itemId=/content/journal/micro/10.1099/mic.0.081836-0&mimeType=html&fmt=ahah

References

  1. Achbergerová L., Nahálka J.. ( 2011;). Polyphosphate – an ancient energy source and active metabolic regulator. . Microb Cell Fact 10:, 63. [CrossRef][PubMed]
    [Google Scholar]
  2. Adams D. G., Carr N. G., Wilcox M.. ( 1981;). The developmental biology of heterocyst and akinete formation in cyanobacteria. . Crit Rev Microbiol 9:, 45–100. [CrossRef][PubMed]
    [Google Scholar]
  3. Ahn K., Kornberg A.. ( 1990;). Polyphosphate kinase from Escherichia coli. Purification and demonstration of a phosphoenzyme intermediate. . J Biol Chem 265:, 11734–11739.[PubMed]
    [Google Scholar]
  4. Akiyama M., Crooke E., Kornberg A.. ( 1993;). An exopolyphosphatase of Escherichia coli. The enzyme and its ppx gene in a polyphosphate operon. . J Biol Chem 268:, 633–639.[PubMed]
    [Google Scholar]
  5. Allen M. B., Arnon D. I.. ( 1955;). Studies on nitrogen-fixing blue-green algae. I. Growth and nitrogen fixation by Anabaena cylindrica Lemm.. Plant Physiol 30:, 366–372. [CrossRef][PubMed]
    [Google Scholar]
  6. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.. ( 1997;). Gapped blast and psi-blast: a new generation of protein database search programs. . Nucleic Acids Res 25:, 3389–3402. [CrossRef][PubMed]
    [Google Scholar]
  7. Arora K. K., Filburn C. R., Pedersen P. L.. ( 1991;). Glucose phosphorylation. Site-directed mutations which impair the catalytic function of hexokinase. . J Biol Chem 266:, 5359–5362.[PubMed]
    [Google Scholar]
  8. Baier, A. ( 2013;). Untersuchungen zum stickstoffinduzierten Phycobilisomenabbau - NblA, ein kleines Protein mit großer Wirkung. . Doctoral thesis, Humboldt-Universität zu Berlin;.
  9. Beadle B. M., Baase W. A., Wilson D. B., Gilkes N. R., Shoichet B. K.. ( 1999;). Comparing the thermodynamic stabilities of a related thermophilic and mesophilic enzyme. . Biochemistry 38:, 2570–2576. [CrossRef][PubMed]
    [Google Scholar]
  10. Bensadoun A., Weinstein D.. ( 1976;). Assay of proteins in the presence of interfering materials. . Anal Biochem 70:, 241–250. [CrossRef][PubMed]
    [Google Scholar]
  11. 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]
  12. Bertani G.. ( 1951;). Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. . J Bacteriol 62:, 293–300.[PubMed]
    [Google Scholar]
  13. Black T. A., Wolk C. P.. ( 1994;). Analysis of a Het- mutation in Anabaena sp. strain PCC 7120 implicates a secondary metabolite in the regulation of heterocyst spacing. . J Bacteriol 176:, 2282–2292.[PubMed]
    [Google Scholar]
  14. Black T. A., Cai Y., Wolk C. P.. ( 1993;). Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena. . Mol Microbiol 9:, 77–84. [CrossRef][PubMed]
    [Google Scholar]
  15. Cai Y. P., Wolk C. P.. ( 1990;). Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences. . J Bacteriol 172:, 3138–3145.[PubMed]
    [Google Scholar]
  16. Castenholz R. W.. ( 1988;). Culturing methods for cyanobacteria. . Methods Enzymol 167:, 68–93. [CrossRef]
    [Google Scholar]
  17. Cleland W. W.. ( 1963;). The kinetics of enzyme-catalyzed reactions with two or more substrates or products. III. Prediction of initial velocity and inhibition patterns by inspection. . Biochim Biophys Acta 67:, 188–196. [CrossRef][PubMed]
    [Google Scholar]
  18. Curatti L., Flores E., Salerno G.. ( 2002;). Sucrose is involved in the diazotrophic metabolism of the heterocyst-forming cyanobacterium Anabaena sp.. FEBS Lett 513:, 175–178. [CrossRef][PubMed]
    [Google Scholar]
  19. Dagan T., Roettger M., Stucken K., Landan G., Koch R., Major P., Gould S. B., Goremykin V. V., Rippka R.. & other authors ( 2013;). Genomes of Stigonematalean cyanobacteria (subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids. . Genome Biol Evol 5:, 31–44. [CrossRef][PubMed]
    [Google Scholar]
  20. de Marsac N. T., Houmard J.. ( 1988;). Complementary chromatic adaptation: physiological conditions and action spectra. . Methods Enzymol 167, 318–328. [CrossRef]
    [Google Scholar]
  21. Elhai J., Wolk C. P.. ( 1988a;). Conjugal transfer of DNA to cyanobacteria. . Methods Enzymol 167:, 747–754. [CrossRef][PubMed]
    [Google Scholar]
  22. Elhai J., Wolk C. P.. ( 1988b;). A versatile class of positive-selection vectors based on the nonviability of palindrome-containing plasmids that allows cloning into long polylinkers. . Gene 68:, 119–138. [CrossRef][PubMed]
    [Google Scholar]
  23. Fewer D., Friedl T., Büdel B.. ( 2002;). Chroococcidiopsis and heterocyst-differentiating cyanobacteria are each other’s closest living relatives. . Mol Phylogenet Evol 23:, 82–90. [CrossRef][PubMed]
    [Google Scholar]
  24. Flaherty B. L., Van Nieuwerburgh F., Head S. R., Golden J. W.. ( 2011;). Directional RNA deep sequencing sheds new light on the transcriptional response of Anabaena sp strain PCC 7120 to combined-nitrogen deprivation. . BMC Genomics 12:, 332. [CrossRef][PubMed]
    [Google Scholar]
  25. Flores E., Herrero A.. ( 2010;). Compartmentalized function through cell differentiation in filamentous cyanobacteria. . Nat Rev Microbiol 8:, 39–50. [CrossRef][PubMed]
    [Google Scholar]
  26. Golubic S., Hernandez-Marine M., Hoffmann L.. ( 1996;). Developmental aspects of branching in filamentous Cyanophyta/Cyanobacteria. . Arch Hydrobiol Suppl Algol Stud 83:, 303–329.
    [Google Scholar]
  27. Gouet P., Courcelle E., Stuart D. I., Métoz F.. ( 1999;). ESPript: analysis of multiple sequence alignments in PostScript. . Bioinformatics 15:, 305–308. [CrossRef][PubMed]
    [Google Scholar]
  28. Harold F. M.. ( 1966;). Inorganic polyphosphates in biology: structure, metabolism, and function. . Bacteriol Rev 30:, 772–794.[PubMed]
    [Google Scholar]
  29. Hill S., Kennedy C., Kavanagh E., Goldberg R. B., Hanau R.. ( 1981;). Nitrogen fixation gene (nifL) involved in oxygen regulation of nitrogenase synthesis in K. pneumoniae. . Nature 290:, 424–426. [CrossRef][PubMed]
    [Google Scholar]
  30. Howard J. B., Rees D. C.. ( 1996;). Structural basis of biological nitrogen fixation. . Chem Rev 96:, 2965–2982. [CrossRef][PubMed]
    [Google Scholar]
  31. Hsieh P. C., Shenoy B. C., Jentoft J. E., Phillips N. F.. ( 1993;). Purification of polyphosphate and ATP glucose phosphotransferase from Mycobacterium tuberculosis H37Ra: evidence that poly(P) and ATP glucokinase activities are catalyzed by the same enzyme. . Protein Expr Purif 4:, 76–84. [CrossRef][PubMed]
    [Google Scholar]
  32. Hsieh P. C., Kowalczyk T. H., Phillips N. F.. ( 1996a;). Kinetic mechanisms of polyphosphate glucokinase from Mycobacterium tuberculosis. . Biochemistry 35:, 9772–9781. [CrossRef][PubMed]
    [Google Scholar]
  33. Hsieh P. C., Shenoy B. C., Samols D., Phillips N. F.. ( 1996b;). Cloning, expression, and characterization of polyphosphate glucokinase from Mycobacterium tuberculosis. . J Biol Chem 271:, 4909–4915. [CrossRef][PubMed]
    [Google Scholar]
  34. Imriskova I., Arreguín-Espinosa R., Guzmán S., Rodriguez-Sanoja R., Langley E., Sanchez S.. ( 2005;). Biochemical characterization of the glucose kinase from Streptomyces coelicolor compared to Streptomyces peucetius var. caesius. . Res Microbiol 156:, 361–366. [CrossRef][PubMed]
    [Google Scholar]
  35. Jensen T. E.. ( 1968;). Electron microscopy of polyphosphate bodies in a blue-green alga Nostoc pruniforme. . Arch Mikrobiol 62:, 144–152. [CrossRef]
    [Google Scholar]
  36. Kornberg A.. ( 1995;). Inorganic polyphosphate: toward making a forgotten polymer unforgettable. . J Bacteriol 177:, 491–496.[PubMed]
    [Google Scholar]
  37. Kornberg A., Kornberg S. R., Simms E. S.. ( 1956;). Metaphosphate synthesis by an enzyme from Escherichia coli. . Biochim Biophys Acta 20:, 215–227. [CrossRef][PubMed]
    [Google Scholar]
  38. Kornberg A., Rao N. N., Ault-Riché D.. ( 1999;). Inorganic polyphosphate: a molecule of many functions. . Annu Rev Biochem 68:, 89–125. [CrossRef][PubMed]
    [Google Scholar]
  39. Kumar K., Mella-Herrera R. A., Golden J. W.. ( 2010;). Cyanobacterial heterocysts. . Cold Spring Harb Perspect Biol 2:, a000315. [CrossRef][PubMed]
    [Google Scholar]
  40. Laemmli U. K.. ( 1970;). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. . Nature 227:, 680–685. [CrossRef][PubMed]
    [Google Scholar]
  41. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A.. & other authors ( 2007;). clustal w and clustal_x version 2.0. . Bioinformatics 23:, 2947–2948. [CrossRef][PubMed]
    [Google Scholar]
  42. Liao H., Myung S., Zhang Y. H.. ( 2012;). One-step purification and immobilization of thermophilic polyphosphate glucokinase from Thermobifida fusca YX: glucose-6-phosphate generation without ATP. . Appl Microbiol Biotechnol 93:, 1109–1117. [CrossRef][PubMed]
    [Google Scholar]
  43. Lichko L. P., Kulakovskaya T. V., Kulaev I. S.. ( 2010;). Properties of partially purified endopolyphosphatase of the yeast Saccharomyces cerevisiae. . Biochemistry (Mosc) 75:, 1404–1407. [CrossRef][PubMed]
    [Google Scholar]
  44. Lindner S. N., Knebel S., Pallerla S. R., Schoberth S. M., Wendisch V. F.. ( 2010;). Cg2091 encodes a polyphosphate/ATP-dependent glucokinase of Corynebacterium glutamicum. . Appl Microbiol Biotechnol 87:, 703–713. [CrossRef][PubMed]
    [Google Scholar]
  45. Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J.. ( 1951;). Protein measurement with the Folin phenol reagent. . J Biol Chem 193:, 265–275.[PubMed]
    [Google Scholar]
  46. Maldener I., Muro-Pastor A. M.. ( 2010;). Cyanobacterial heterocysts. . In eLS. Chichester:: Wiley;. [doi:10.1002/9780470015902.a0000306.pub2] [CrossRef]
    [Google Scholar]
  47. Markowitz V. M., Chen I. M., Palaniappan K., Chu K., Szeto E., Grechkin Y., Ratner A., Jacob B., Huang J.. & other authors ( 2012;). IMG: the Integrated Microbial Genomes database and comparative analysis system. . Nucleic Acids Res 40: (Database issue), D115–D122. [CrossRef][PubMed]
    [Google Scholar]
  48. Meyer A.. ( 1902;). Orientierende Untersuchungen über Verbreitung, Morphologie, und Chemie des Volutins. . Bot Zeitschr 62:, 113–152.
    [Google Scholar]
  49. Mitschke J., Vioque A., Haas F., Hess W. R., Muro-Pastor A. M.. ( 2011;). Dynamics of transcriptional start site selection during nitrogen stress-induced cell differentiation in Anabaena sp. PCC7120. . Proc Natl Acad Sci U S A 108:, 20130–20135. [CrossRef][PubMed]
    [Google Scholar]
  50. Mitsui A., Kumazawa S., Takahashi A., Ikemoto H., Cao S., Arai T.. ( 1986;). Strategy by which nitrogen-fixing unicellular cyanobacteria grow photoautotrophically. . Nature 323:, 720–722. [CrossRef]
    [Google Scholar]
  51. Mukai T., Kawai S., Matsukawa H., Matuo Y., Murata K.. ( 2003;). Characterization and molecular cloning of a novel enzyme, inorganic polyphosphate/ATP-glucomannokinase, of Arthrobacter sp. strain KM. . Appl Environ Microbiol 69:, 3849–3857. [CrossRef][PubMed]
    [Google Scholar]
  52. Mukai T., Kawai S., Mori S., Mikami B., Murata K.. ( 2004;). Crystal structure of bacterial inorganic polyphosphate/ATP-glucomannokinase. Insights into kinase evolution. . J Biol Chem 279:, 50591–50600. [CrossRef][PubMed]
    [Google Scholar]
  53. Nakao M., Okamoto S., Kohara M., Fujishiro T., Fujisawa T., Sato S., Tabata S., Kaneko T., Nakamura Y.. ( 2010;). CyanoBase: the cyanobacteria genome database update 2010. . Nucleic Acids Res 38: (Database issue), D379–D381. [CrossRef][PubMed]
    [Google Scholar]
  54. Nürnberg D. J., Mariscal V., Parker J., Mastroianni G., Flores E., Mullineaux C. W.. ( 2014;). Branching and intercellular communication in the Section V cyanobacterium Mastigocladus laminosus, a complex multicellular prokaryote. . Mol Microbiol 91:, 935–949. [CrossRef][PubMed]
    [Google Scholar]
  55. Pepin C. A., Wood H. G.. ( 1986;). Polyphosphate glucokinase from Propionibacterium shermanii. Kinetics and demonstration that the mechanism involves both processive and nonprocessive type reactions. . J Biol Chem 261:, 4476–4480.[PubMed]
    [Google Scholar]
  56. Phillips N. F., Horn P. J., Wood H. G.. ( 1993;). The polyphosphate- and ATP-dependent glucokinase from Propionibacterium shermanii: both activities are catalyzed by the same protein. . Arch Biochem Biophys 300:, 309–319. [CrossRef][PubMed]
    [Google Scholar]
  57. Phillips N. F., Hsieh P. C., Kowalczyk T. H.. ( 1999;). Polyphosphate glucokinase. . Prog Mol Subcell Biol 23:, 101–125. [CrossRef][PubMed]
    [Google Scholar]
  58. Picossi S., Flores E., Herrero A.. ( 2014;). ChIP analysis unravels an exceptionally wide distribution of DNA binding sites for the NtcA transcription factor in a heterocyst-forming cyanobacterium. . BMC Genomics 15:, 22. [CrossRef][PubMed]
    [Google Scholar]
  59. Rao N. N., Gómez-García M. R., Kornberg A.. ( 2009;). Inorganic polyphosphate: essential for growth and survival. . Annu Rev Biochem 78:, 605–647. [CrossRef][PubMed]
    [Google Scholar]
  60. Rashid M. H., Kornberg A.. ( 2000;). Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. . Proc Natl Acad Sci U S A 97:, 4885–4890. [CrossRef][PubMed]
    [Google Scholar]
  61. Rashid M. H., Rao N. N., Kornberg A.. ( 2000;). Inorganic polyphosphate is required for motility of bacterial pathogens. . J Bacteriol 182:, 225–227. [CrossRef][PubMed]
    [Google Scholar]
  62. Remonsellez F., Orell A., Jerez C. A.. ( 2006;). Copper tolerance of the thermoacidophilic archaeon Sulfolobus metallicus: possible role of polyphosphate metabolism. . Microbiology 152:, 59–66. [CrossRef][PubMed]
    [Google Scholar]
  63. Resnick S. M., Zehnder A. J.. ( 2000;). In vitro ATP regeneration from polyphosphate and AMP by polyphosphate : AMP phosphotransferase and adenylate kinase from Acinetobacter johnsonii 210A. . Appl Environ Microbiol 66:, 2045–2051. [CrossRef][PubMed]
    [Google Scholar]
  64. Rippka R., Waterbury J. B.. ( 1977;). Synthesis of nitrogenase by non-heterocystous cyanobacteria. . FEMS Microbiol Lett 2:, 83–86. [CrossRef]
    [Google Scholar]
  65. Rippka R., Deruelles J., Waterbury J. B., Herdman M., Stanier R. Y.. ( 1979;). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. . J Gen Microbiol 111:, 1–61. [CrossRef]
    [Google Scholar]
  66. Robertson B. R., Tezuka N., Watanabe M. M.. ( 2001;). Phylogenetic analyses of Synechococcus strains (cyanobacteria) using sequences of 16S rDNA and part of the phycocyanin operon reveal multiple evolutionary lines and reflect phycobilin content. . Int J Syst Evol Microbiol 51:, 861–871. [CrossRef][PubMed]
    [Google Scholar]
  67. Scherer P. A., Bochem H. P.. ( 1983;). Ultrastructural investigation of 12 Methanosarcinae and related species grown on methanol for occurrence of polyphosphatelike inclusions. . Can J Microbiol 29:, 1190–1199. [CrossRef]
    [Google Scholar]
  68. Shih P. M., Wu D., Latifi A., Axen S. D., Fewer D. P., Talla E., Calteau A., Cai F., Tandeau de Marsac N.. & other authors ( 2013;). Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. . Proc Natl Acad Sci U S A 110:, 1053–1058. [CrossRef][PubMed]
    [Google Scholar]
  69. Stal L. J.. ( 1995;). Physiological ecology of cyanobacteria in microbial mats and other communities. . New Phytol 131:, 1–32. [CrossRef]
    [Google Scholar]
  70. Szymona M., Ostrowski W.. ( 1964;). Inorganic polyphosphate glucokinase of Mycobacterium phlei. . Biochim Biophys Acta 85:, 283–295.[PubMed]
    [Google Scholar]
  71. Szymona M., Widomski J.. ( 1974;). A kinetic study on inorganic polyphosphate glucokinase from Mycobacterium tuberculosis H37RA. . Physiol Chem Phys 6:, 393–404.[PubMed]
    [Google Scholar]
  72. Tanaka S., Lee S. O., Hamaoka K., Kato J., Takiguchi N., Nakamura K., Ohtake H., Kuroda A.. ( 2003;). Strictly polyphosphate-dependent glucokinase in a polyphosphate-accumulating bacterium, Microlunatus phosphovorus. . J Bacteriol 185:, 5654–5656. [CrossRef][PubMed]
    [Google Scholar]
  73. Thompson P. A., Oh H. M., Rhee G. Y.. ( 1994;). Storage of phosphorus in nitrogen-fixing Anabaena flos-aquae (Cyanophyceae). . J Phycol 30:, 267–273. [CrossRef]
    [Google Scholar]
  74. Toepel J., Welsh E., Summerfield T. C., Pakrasi H. B., Sherman L. A.. ( 2008;). Differential transcriptional analysis of the cyanobacterium Cyanothece sp. strain ATCC 51142 during light-dark and continuous-light growth. . J Bacteriol 190:, 3904–3913. [CrossRef][PubMed]
    [Google Scholar]
  75. Tsutsumi K., Munekata M., Shiba T.. ( 2000;). Involvement of inorganic polyphosphate in expression of SOS genes. . Biochim Biophys Acta 1493:, 73–81. [CrossRef][PubMed]
    [Google Scholar]
  76. Walker P. A., Leong L. E., Ng P. W., Tan S. H., Waller S., Murphy D., Porter A. G.. ( 1994;). Efficient and rapid affinity purification of proteins using recombinant fusion proteases. . Biotechnology (N Y) 12:, 601–605. [CrossRef][PubMed]
    [Google Scholar]
  77. Wilkins M. R., Gasteiger E., Bairoch A., Sanchez J. C., Williams K. L., Appel R. D., Hochstrasser D. F.. ( 1999;). Protein identification and analysis tools in the ExPASy server. . Methods Mol Biol 112:, 531–552.[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.081836-0
Loading
/content/journal/micro/10.1099/mic.0.081836-0
Loading

Data & Media loading...

Supplements

Supplementary Data 

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error