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Applied Microbiology and Biotechnology

, Volume 99, Issue 15, pp 6303–6313 | Cite as

Essentiality of tetramer formation of Cellulomonas parahominis L-ribose isomerase involved in novel L-ribose metabolic pathway

  • Yuji Terami
  • Hiromi Yoshida
  • Keiko Uechi
  • Kenji Morimoto
  • Goro Takata
  • Shigehiro Kamitori
Biotechnologically relevant enzymes and proteins

Abstract

L-Ribose isomerase from Cellulomonas parahominis MB426 (CpL-RI) can catalyze the isomerization between L-ribose and L-ribulose, which are non-abundant in nature and called rare sugars. CpL-RI has a broad substrate specificity and can catalyze the isomerization between D-lyxose and D-xylulose, D-talose and D-tagatose, L-allose and L-psicose, L-gulose and L-sorbose, and D-mannose and D-fructose. To elucidate the molecular basis underlying the substrate recognition mechanism of CpL-RI, the crystal structures of CpL-RI alone and in complexes with L-ribose, L-allose, and L-psicose were determined. The structure of CpL-RI was very similar to that of L-ribose isomerase from Acinetobacter sp. strain DL-28, previously determined by us. CpL-RI had a cupin-type β-barrel structure, and the catalytic site was detected between two large β-sheets with a bound metal ion. The bound substrates coordinated to the metal ion, and Glu113 and Glu204 were shown to act as acid/base catalysts in the catalytic reaction via a cis-enediol intermediate. Glu211 and Arg243 were found to be responsible for the recognition of substrates with various configurations at 4- and 5-positions of sugar. CpL-RI formed a homo-tetramer in crystals, and the catalytic site independently consisted of residues within a subunit, suggesting that the catalytic site acted independently. Crystal structure and site-direct mutagenesis analyses showed that the tetramer structure is essential for the enzyme activity and that each subunit of CpL-RI could be structurally stabilized by intermolecular contacts with other subunits. The results of growth complementation assays suggest that CpL-RI is involved in a novel metabolic pathway using L-ribose as a carbon source.

Keywords

Crystal structure Cupin-type β-barrel Rare sugar L-Ribose isomerase 

Notes

Acknowledgments

We thank Dr. A. Itoh and Mr. K. Yube for their technical assistant with DNA sequencing. Y. Terami is supported by a Grant-in-Aid from the Japan Society for the Promotion of Science (JSPS) Research Fellows. This study was supported in part by Grants-in-Aid for Scientific Research (25440028, 23770122, 22780068, 26450097, 22580088) from JSPS, and by the funds from the Kagawa University New Research Areas and Collaborative Research Organization. This research was performed with the approval of the Photon Factory Advisory Committee and National Laboratory for High Energy Physics (2012G550 and 2013G506) Japan.

Supplementary material

253_2015_6417_MOESM1_ESM.pdf (1.7 mb)
ESM 1 (PDF 1714 kb)

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Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Yuji Terami
    • 1
  • Hiromi Yoshida
    • 2
  • Keiko Uechi
    • 1
  • Kenji Morimoto
    • 1
  • Goro Takata
    • 1
  • Shigehiro Kamitori
    • 2
  1. 1.Rare Sugar Research Center and Faculty of AgricultureKagawa UniversityKagawaJapan
  2. 2.Life Science Research Center and Faculty of MedicineKagawa UniversityKagawaJapan

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