Structural Insights on the New Mechanism of Trehalose Synthesis by Trehalose Synthase TreT from Pyrococcus horikoshii

Eui Jeon Woo, Soo In Ryu, Hyung Nam Song, Tae Yang Jung, Sei Mee Yeon, Hyun Ah Lee, Byoung Chul Park, Kwan Hwa Park, Soo-Bok Lee

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Many microorganisms produce trehalose for stability and survival against various environmental stresses. Unlike the widely distributed trehalose-biosynthetic pathway, which utilizes uridine diphosphate glucose and glucose-6-phosphate, the newly identified enzyme trehalose glycosyltransferring synthase (TreT) from hyperthermophilic bacteria and archaea synthesizes an α,α-trehalose from nucleoside diphosphate glucose and glucose. In the present study, we determined the crystal structure of TreT from Pyrococcus horikoshii at 2.3 Å resolution to understand the detailed mechanism of this novel trehalose synthase. The conservation of essential residues in TreT and the high overall structural similarity of the N-terminal domain to that of trehalose phosphate synthase (TPS) imply that the catalytic reaction of TreT for trehalose synthesis would follow a similar mechanism to that of TPS. The acceptor binding site of TreT shows a wide and commodious groove and lacks the long flexible loop that plays a gating role in ligand binding in TPS. The observation of a wide space at the fissure between two domains and the relative shift of the N-domain in one of the crystal forms suggest that an interactive conformational change between two domains would occur, allowing a more compact architecture for catalysis. The structural analysis and biochemical data in this study provide a molecular basis for understanding the synthetic mechanism of trehalose, or the nucleotide sugar in reverse reaction of the TreT, in extremophiles that may have important industrial implications.

Original languageEnglish
Pages (from-to)247-259
Number of pages13
JournalJournal of Molecular Biology
Volume404
Issue number2
DOIs
Publication statusPublished - 2010 Nov 26

Fingerprint

Pyrococcus horikoshii
Trehalose
Phosphates
Uridine Diphosphate Glucose
Glucose
Glucose-6-Phosphate
Diphosphates
Biosynthetic Pathways
Archaea
Catalysis
Nucleosides
Nucleotides
Binding Sites
Observation
trehalose synthase
Ligands
Bacteria
Enzymes

All Science Journal Classification (ASJC) codes

  • Structural Biology
  • Molecular Biology

Cite this

Woo, Eui Jeon ; Ryu, Soo In ; Song, Hyung Nam ; Jung, Tae Yang ; Yeon, Sei Mee ; Lee, Hyun Ah ; Park, Byoung Chul ; Park, Kwan Hwa ; Lee, Soo-Bok. / Structural Insights on the New Mechanism of Trehalose Synthesis by Trehalose Synthase TreT from Pyrococcus horikoshii. In: Journal of Molecular Biology. 2010 ; Vol. 404, No. 2. pp. 247-259.
@article{c3a6bdb8e9e3485990674dc5f6d6df0e,
title = "Structural Insights on the New Mechanism of Trehalose Synthesis by Trehalose Synthase TreT from Pyrococcus horikoshii",
abstract = "Many microorganisms produce trehalose for stability and survival against various environmental stresses. Unlike the widely distributed trehalose-biosynthetic pathway, which utilizes uridine diphosphate glucose and glucose-6-phosphate, the newly identified enzyme trehalose glycosyltransferring synthase (TreT) from hyperthermophilic bacteria and archaea synthesizes an α,α-trehalose from nucleoside diphosphate glucose and glucose. In the present study, we determined the crystal structure of TreT from Pyrococcus horikoshii at 2.3 {\AA} resolution to understand the detailed mechanism of this novel trehalose synthase. The conservation of essential residues in TreT and the high overall structural similarity of the N-terminal domain to that of trehalose phosphate synthase (TPS) imply that the catalytic reaction of TreT for trehalose synthesis would follow a similar mechanism to that of TPS. The acceptor binding site of TreT shows a wide and commodious groove and lacks the long flexible loop that plays a gating role in ligand binding in TPS. The observation of a wide space at the fissure between two domains and the relative shift of the N-domain in one of the crystal forms suggest that an interactive conformational change between two domains would occur, allowing a more compact architecture for catalysis. The structural analysis and biochemical data in this study provide a molecular basis for understanding the synthetic mechanism of trehalose, or the nucleotide sugar in reverse reaction of the TreT, in extremophiles that may have important industrial implications.",
author = "Woo, {Eui Jeon} and Ryu, {Soo In} and Song, {Hyung Nam} and Jung, {Tae Yang} and Yeon, {Sei Mee} and Lee, {Hyun Ah} and Park, {Byoung Chul} and Park, {Kwan Hwa} and Soo-Bok Lee",
year = "2010",
month = "11",
day = "26",
doi = "10.1016/j.jmb.2010.09.056",
language = "English",
volume = "404",
pages = "247--259",
journal = "Journal of Molecular Biology",
issn = "0022-2836",
publisher = "Academic Press Inc.",
number = "2",

}

Structural Insights on the New Mechanism of Trehalose Synthesis by Trehalose Synthase TreT from Pyrococcus horikoshii. / Woo, Eui Jeon; Ryu, Soo In; Song, Hyung Nam; Jung, Tae Yang; Yeon, Sei Mee; Lee, Hyun Ah; Park, Byoung Chul; Park, Kwan Hwa; Lee, Soo-Bok.

In: Journal of Molecular Biology, Vol. 404, No. 2, 26.11.2010, p. 247-259.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Structural Insights on the New Mechanism of Trehalose Synthesis by Trehalose Synthase TreT from Pyrococcus horikoshii

AU - Woo, Eui Jeon

AU - Ryu, Soo In

AU - Song, Hyung Nam

AU - Jung, Tae Yang

AU - Yeon, Sei Mee

AU - Lee, Hyun Ah

AU - Park, Byoung Chul

AU - Park, Kwan Hwa

AU - Lee, Soo-Bok

PY - 2010/11/26

Y1 - 2010/11/26

N2 - Many microorganisms produce trehalose for stability and survival against various environmental stresses. Unlike the widely distributed trehalose-biosynthetic pathway, which utilizes uridine diphosphate glucose and glucose-6-phosphate, the newly identified enzyme trehalose glycosyltransferring synthase (TreT) from hyperthermophilic bacteria and archaea synthesizes an α,α-trehalose from nucleoside diphosphate glucose and glucose. In the present study, we determined the crystal structure of TreT from Pyrococcus horikoshii at 2.3 Å resolution to understand the detailed mechanism of this novel trehalose synthase. The conservation of essential residues in TreT and the high overall structural similarity of the N-terminal domain to that of trehalose phosphate synthase (TPS) imply that the catalytic reaction of TreT for trehalose synthesis would follow a similar mechanism to that of TPS. The acceptor binding site of TreT shows a wide and commodious groove and lacks the long flexible loop that plays a gating role in ligand binding in TPS. The observation of a wide space at the fissure between two domains and the relative shift of the N-domain in one of the crystal forms suggest that an interactive conformational change between two domains would occur, allowing a more compact architecture for catalysis. The structural analysis and biochemical data in this study provide a molecular basis for understanding the synthetic mechanism of trehalose, or the nucleotide sugar in reverse reaction of the TreT, in extremophiles that may have important industrial implications.

AB - Many microorganisms produce trehalose for stability and survival against various environmental stresses. Unlike the widely distributed trehalose-biosynthetic pathway, which utilizes uridine diphosphate glucose and glucose-6-phosphate, the newly identified enzyme trehalose glycosyltransferring synthase (TreT) from hyperthermophilic bacteria and archaea synthesizes an α,α-trehalose from nucleoside diphosphate glucose and glucose. In the present study, we determined the crystal structure of TreT from Pyrococcus horikoshii at 2.3 Å resolution to understand the detailed mechanism of this novel trehalose synthase. The conservation of essential residues in TreT and the high overall structural similarity of the N-terminal domain to that of trehalose phosphate synthase (TPS) imply that the catalytic reaction of TreT for trehalose synthesis would follow a similar mechanism to that of TPS. The acceptor binding site of TreT shows a wide and commodious groove and lacks the long flexible loop that plays a gating role in ligand binding in TPS. The observation of a wide space at the fissure between two domains and the relative shift of the N-domain in one of the crystal forms suggest that an interactive conformational change between two domains would occur, allowing a more compact architecture for catalysis. The structural analysis and biochemical data in this study provide a molecular basis for understanding the synthetic mechanism of trehalose, or the nucleotide sugar in reverse reaction of the TreT, in extremophiles that may have important industrial implications.

UR - http://www.scopus.com/inward/record.url?scp=78349313324&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=78349313324&partnerID=8YFLogxK

U2 - 10.1016/j.jmb.2010.09.056

DO - 10.1016/j.jmb.2010.09.056

M3 - Article

C2 - 20888836

AN - SCOPUS:78349313324

VL - 404

SP - 247

EP - 259

JO - Journal of Molecular Biology

JF - Journal of Molecular Biology

SN - 0022-2836

IS - 2

ER -