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A pentose bisphosphate pathway for nucleoside degradation in Archaea

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Abstract

Owing to the absence of the pentose phosphate pathway, the degradation pathway for the ribose moieties of nucleosides is unknown in Archaea. Here, in the archaeon Thermococcus kodakarensis, we identified a metabolic network that links the pentose moieties of nucleosides or nucleotides to central carbon metabolism. The network consists of three nucleoside phosphorylases, an ADP-dependent ribose-1-phosphate kinase and two enzymes of a previously identified NMP degradation pathway, ribose-1,5-bisphosphate isomerase and type III ribulose-1,5-bisphosphate carboxylase/oxygenase. Ribose 1,5-bisphosphate and ribulose 1,5-bisphosphate are intermediates of this pathway, which is thus designated the pentose bisphosphate pathway.

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Figure 1: Nucleoside metabolism in Archaea, Bacteria and Eukarya.

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References

  1. Wamelink, M.M., Struys, E.A. & Jakobs, C. The biochemistry, metabolism and inherited defects of the pentose phosphate pathway: a review. J. Inherit. Metab. Dis. 31, 703–717 (2008).

    Article  CAS  Google Scholar 

  2. Riganti, C., Gazzano, E., Polimeni, M., Aldieri, E. & Ghigo, D. The pentose phosphate pathway: an antioxidant defense and a crossroad in tumor cell fate. Free Radic. Biol. Med. 53, 421–436 (2012).

    Article  CAS  Google Scholar 

  3. Soderberg, T. Biosynthesis of ribose-5-phosphate and erythrose-4-phosphate in archaea: a phylogenetic analysis of archaeal genomes. Archaea 1, 347–352 (2005).

    Article  CAS  Google Scholar 

  4. Orita, I. et al. The ribulose monophosphate pathway substitutes for the missing pentose phosphate pathway in the archaeon. Thermococcus kodakaraensis . J. Bacteriol. 188, 4698–4704 (2006).

    Article  CAS  Google Scholar 

  5. Ezaki, S., Maeda, N., Kishimoto, T., Atomi, H. & Imanaka, T. Presence of a structurally novel type ribulose-bisphosphate carboxylase/oxygenase in the hyperthermophilic archaeon, Pyrococcus kodakaraensis KOD1. J. Biol. Chem. 274, 5078–5082 (1999).

    Article  CAS  Google Scholar 

  6. Finn, M.W. & Tabita, F.R. Synthesis of catalytically active form III ribulose 1,5-bisphosphate carboxylase/oxygenase in archaea. J. Bacteriol. 185, 3049–3059 (2003).

    Article  CAS  Google Scholar 

  7. Watson, G.M., Yu, J.P. & Tabita, F.R. Unusual ribulose 1,5-bisphosphate carboxylase/oxygenase of anoxic Archaea. J. Bacteriol. 181, 1569–1575 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Kitano, K. et al. Crystal structure of a novel-type archaeal rubisco with pentagonal symmetry. Structure 9, 473–481 (2001).

    Article  CAS  Google Scholar 

  9. Alonso, H., Blayney, M.J., Beck, J.L. & Whitney, S.M. Substrate-induced assembly of Methanococcoides burtonii D-ribulose-1,5-bisphosphate carboxylase/oxygenase dimers into decamers. J. Biol. Chem. 284, 33876–33882 (2009).

    Article  CAS  Google Scholar 

  10. Sato, T., Atomi, H. & Imanaka, T. Archaeal type III RuBisCOs function in a pathway for AMP metabolism. Science 315, 1003–1006 (2007).

    Article  CAS  Google Scholar 

  11. Nakamura, A. et al. Dynamic, ligand-dependent conformational change triggers reaction of ribose-1,5-bisphosphate isomerase from Thermococcus kodakarensis KOD1. J. Biol. Chem. 287, 20784–20796 (2012).

    Article  CAS  Google Scholar 

  12. Nishitani, Y. et al. Structure analysis of archaeal AMP phosphorylase reveals two unique modes of dimerization. J. Mol. Biol. 425, 2709–2721 (2013).

    Article  CAS  Google Scholar 

  13. Aono, R. et al. Enzymatic characterization of AMP phosphorylase and ribose-1,5-bisphosphate isomerase functioning in an archaeal AMP metabolic pathway. J. Bacteriol. 194, 6847–6855 (2012).

    Article  CAS  Google Scholar 

  14. Hansen, T., Arnfors, L., Ladenstein, R. & Schönheit, P. The phosphofructokinase-B (MJ0406) from Methanocaldococcus jannaschii represents a nucleoside kinase with a broad substrate specificity. Extremophiles 11, 105–114 (2007).

    Article  CAS  Google Scholar 

  15. Elkin, S.R., Kumar, A., Price, C.W. & Columbus, L. A broad specificity nucleoside kinase from Thermoplasma acidophilum. Proteins 81, 568–582 (2013).

    Article  CAS  Google Scholar 

  16. Park, J. & Gupta, R.S. Adenosine kinase and ribokinase—the RK family of proteins. Cell. Mol. Life Sci. 65, 2875–2896 (2008).

    Article  CAS  Google Scholar 

  17. Kengen, S.W. et al. Evidence for the operation of a novel Embden-Meyerhof pathway that involves ADP-dependent kinases during sugar fermentation by Pyrococcus furiosus. J. Biol. Chem. 269, 17537–17541 (1994).

    CAS  PubMed  Google Scholar 

  18. Kengen, S.W., Tuininga, J.E., de Bok, F.A., Stams, A.J. & de Vos, W.M. Purification and characterization of a novel ADP-dependent glucokinase from the hyperthermophilic archaeon Pyrococcus furiosus. J. Biol. Chem. 270, 30453–30457 (1995).

    Article  CAS  Google Scholar 

  19. Tuininga, J.E. et al. Molecular and biochemical characterization of the ADP-dependent phosphofructokinase from the hyperthermophilic archaeon Pyrococcus furiosus. J. Biol. Chem. 274, 21023–21028 (1999).

    Article  CAS  Google Scholar 

  20. Sakuraba, H. et al. ADP-dependent glucokinase/phosphofructokinase, a novel bifunctional enzyme from the hyperthermophilic archaeon Methanococcus jannaschii. J. Biol. Chem. 277, 12495–12498 (2002).

    Article  CAS  Google Scholar 

  21. Guixé, V. & Merino, F. The ADP-dependent sugar kinase family: kinetic and evolutionary aspects. IUBMB Life 61, 753–761 (2009).

    Article  Google Scholar 

  22. Merino, F., Rivas-Pardo, J.A., Caniuguir, A., García, I. & Guixé, V. Catalytic and regulatory roles of divalent metal cations on the phosphoryl-transfer mechanism of ADP-dependent sugar kinases from hyperthermophilic archaea. Biochimie 94, 516–524 (2012).

    Article  CAS  Google Scholar 

  23. Castro-Fernandez, V., Bravo-Moraga, F., Herrera-Morande, A. & Guixe, V. Bifunctional ADP-dependent phosphofructokinase/glucokinase activity in the order Methanococcales—biochemical characterization of the mesophilic enzyme from Methanococcus maripaludis. FEBS J. 281, 2017–2029 (2014).

    Article  CAS  Google Scholar 

  24. Ronimus, R.S. & Morgan, H.W. Cloning and biochemical characterization of a novel mouse ADP-dependent glucokinase. Biochem. Biophys. Res. Commun. 315, 652–658 (2004).

    Article  CAS  Google Scholar 

  25. Marbaix, A.Y. et al. Extremely conserved ATP- or ADP-dependent enzymatic system for nicotinamide nucleotide repair. J. Biol. Chem. 286, 41246–41252 (2011).

    Article  CAS  Google Scholar 

  26. Kengen, S.W. et al. ADP-dependent glucokinase and phosphofructokinase from Pyrococcus furiosus. Methods Enzymol. 331, 41–53 (2001).

    Article  CAS  Google Scholar 

  27. Boyer, P.D. & Robbins, E.A. Determination of the equilibrium of the hexokinase reaction and the free energy of hydrolysis of adenosine triphosphate. J. Biol. Chem. 224, 121–135 (1957).

    CAS  PubMed  Google Scholar 

  28. Minakami, S. & Yoshikawa, H. Thermodynamic considerations on erythrocyte glycolysis. Biochem. Biophys. Res. Commun. 18, 345–349 (1965).

    Article  CAS  Google Scholar 

  29. Cacciapuoti, G., Bertoldo, C., Brio, A., Zappia, V. & Porcelli, M. Purification and characterization of 5′-methylthioadenosine phosphorylase from the hyperthermophilic archaeon Pyrococcus furiosus: substrate specificity and primary structure analysis. Extremophiles 7, 159–168 (2003).

    Article  CAS  Google Scholar 

  30. Cacciapuoti, G. et al. Biochemical and structural characterization of mammalian-like purine nucleoside phosphorylase from the Archaeon Pyrococcus furiosus. FEBS J. 274, 2482–2495 (2007).

    Article  CAS  Google Scholar 

  31. Cacciapuoti, G., Porcelli, M., Bertoldo, C., De Rosa, M. & Zappia, V. Purification and characterization of extremely thermophilic and thermostable 5-methylthioadenosi 5(-methylthioadenosine phosphorylase from the archaeon Sulfolobus solfataricus. Purine nucleoside phosphorylase activity and evidence for intersubunit disulfide bonds. J. Biol. Chem. 269, 24762–24769 (1994).

    CAS  PubMed  Google Scholar 

  32. Cacciapuoti, G. et al. A novel hyperthermostable 5-deoxy-5-methylthioadenosi phosphorylase from the archaeon Sulfolobus solfataricus. FEBS J. 272, 1886–1899 (2005).

    Article  CAS  Google Scholar 

  33. Fukui, T. et al. Complete genome sequence of the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1 and comparison with Pyrococcus genomes. Genome Res. 15, 352–363 (2005).

    Article  CAS  Google Scholar 

  34. Ipata, P.L., Camici, M., Micheli, V. & Tozz, M.G. Metabolic network of nucleosides in the brain. Curr. Top. Med. Chem. 11, 909–922 (2011).

    Article  CAS  Google Scholar 

  35. Tozzi, M.G., Camici, M., Mascia, L., Sgarrella, F. & Ipata, P.L. Pentose phosphates in nucleoside interconversion and catabolism. FEBS J. 273, 1089–1101 (2006).

    Article  CAS  Google Scholar 

  36. Camici, M., Tozzi, M.G. & Ipata, P.L. Methods for the determination of intracellular levels of ribose phosphates. J. Biochem. Biophys. Methods 68, 145–154 (2006).

    Article  CAS  Google Scholar 

  37. Walther, T. et al. The PGM3 gene encodes the major phosphoribomutase in the yeast Saccharomyces cerevisiae. FEBS Lett. 586, 4114–4118 (2012).

    Article  CAS  Google Scholar 

  38. Sambrook, J. & Russel, D. Molecular Cloning: a Laboratory Manual (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 2001).

    Google Scholar 

  39. Atomi, H., Fukui, T., Kanai, T., Morikawa, M. & Imanaka, T. Description of Thermococcus kodakaraensis sp. nov., a well studied hyperthermophilic archaeon previously reported as Pyrococcus sp. KOD1. Archaea 1, 263–267 (2004).

    Article  CAS  Google Scholar 

  40. Robb, F.T. & Place, A.R. Archaea: a Laboratory Manual (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1995).

    Google Scholar 

  41. Kanai, T. et al. A global transcriptional regulator in Thermococcus kodakaraensis controls the expression levels of both glycolytic and gluconeogenic enzyme–encoding genes. J. Biol. Chem. 282, 33659–33670 (2007).

    Article  CAS  Google Scholar 

  42. Kanai, T., Takedomi, S., Fujiwara, S., Atomi, H. & Imanaka, T. Identification of the Phr-dependent heat shock regulon in the hyperthermophilic archaeon, Thermococcus kodakaraensis. J. Biochem. 147, 361–370 (2010).

    Article  CAS  Google Scholar 

  43. Sato, T. et al. Genetic evidence identifying the true gluconeogenic fructose-1,6-bisphosphatase in Thermococcus kodakaraensis and other hyperthermophiles. J. Bacteriol. 186, 5799–5807 (2004).

    Article  CAS  Google Scholar 

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Acknowledgements

This study was funded by the Core Research for Evolutional Science and Technology program of the Japan Science and Technology Agency to H.A. within the research area 'Creation of Basic Technology for Improved Bioenergy Production through Functional Analysis and Regulation of Algae and Other Aquatic Microorganisms'. R.A. is a Research Fellow of the Japan Society for the Promotion of Science.

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H.A., T.I., T.S. and R.A. designed the work; R.A. carried out the experiments; R.A., T.S. and H.A. wrote the manuscript.

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Correspondence to Haruyuki Atomi.

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The authors declare no competing financial interests.

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Supplementary Results, Supplementary Tables 1–7 and Supplementary Figures 1–16. (PDF 7128 kb)

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Aono, R., Sato, T., Imanaka, T. et al. A pentose bisphosphate pathway for nucleoside degradation in Archaea. Nat Chem Biol 11, 355–360 (2015). https://doi.org/10.1038/nchembio.1786

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