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A Novel Glucose 6-Phosphate Isomerase from Listeria monocytogenes

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Abstract

d-Arabinose 5-phosphate isomerases (APIs) catalyze the interconversion of d-ribulose 5-phosphate and d-arabinose 5-phosphate (A5P). A5P is an intermediate in the biosynthesis of 3-deoxy-d-manno-octulosonate (Kdo), an essential component of lipopolysaccharide, the lipopolysaccharide found in the outer membrane of Gram-negative bacteria. The genome of the Gram-positive pathogen Listeria monocytogenes contains a gene encoding a putative sugar isomerase domain API, Q723E8, with significant similarity to c3406, the only one of four APIs from Escherichia coli CFT073 that lacks a cystathionine-β-synthase domain. However, L. monocytogenes lacks genes encoding any of the other enzymes of the Kdo biosynthesis pathway. Realizing that the discovery of an API in a Gram-positive bacterium could provide insight into an alternate physiological role of A5P in the cell, we prepared and purified recombinant Q723E8. We found that Q723E8 does not possess API activity, but instead is a novel GPI (d-glucose 6-phosphate isomerase). However, the GPI activity of Q723E8 is weak compared with previously described GPIs. L. monocytogenes contains an ortholog of the well-studied two-domain bacterial GPI, so this maybe redundant. Based on this evidence glucose utilization is likely not the primary physiological role of Q723E8.

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Abbreviations

A5P:

d-Arabinose 5-phosphate

API:

d-Arabinose 5-phosphate isomerase

Bis–tris propane:

2,2′-(Propane-1,3-diyldiimino)bis[2-(hydroxymethyl)propane-1,3-diol]

BLAST:

Basic local alignment search tool

CBS:

Cystathionine-β-synthase

F6P:

d-Fructose 6-phosphate

G6P:

d-Glucose 6-phosphate

GPI:

d-Glucose 6-phosphate isomerase

HEPES:

2-[4-(2-Hydroxyethyl)piperazin-1-yl]ethanesulfonic acid

IPTG:

Isopropyl β-d-1-thiogalactopyranoside

Kdo:

3-Deoxy-d-manno-octulosonate

LPS:

Lipopolysaccharide

MES:

2-(N-morpholino)ethanesulfonic acid

MOPS:

3-(N-morpholino)propanesulfonic acid

MW:

Molecular weight

Rf:

Relative mobility

PTS:

Phosphoenolpyruvate:sugar phosphotransferase

Ru5P:

d-Ribulose 5-phosphate

SIS:

Sugar isomerase

Tris:

2-Amino-2-hydroxymethyl-propane-1,3-diol

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Acknowledgments

This work was supported, in part, by National Institutes of Health Grant AI-061531 (to R.W.W.). The authors thank Jim Windak and Paul Lennon of the University of Michigan Department of Chemistry Mass Spectroscopy facility for performing the LC–MS analysis of recombinant lmof2365_0531, and Ted Houston of the University of Michigan Department of Geology’s W.M. Keck Elemental Geochemistry Laboratory for performing the metals analysis.

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Authors and Affiliations

  1. Department of Medicinal Chemistry, University of Michigan, 428 Church Street, Ann Arbor, MI, 48109-1065, USA

    David L. Cech, Pan-Fen Wang, Melissa C. Holt, Jeffrey M. Schaub, Tod P. Holler & Ronald W. Woodard

  2. Interdisciplinary Program in Chemical Biology, University of Michigan, Ann Arbor, MI, USA

    Victoria A. Assimon

Authors
  1. David L. Cech
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  2. Pan-Fen Wang
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  3. Melissa C. Holt
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  4. Victoria A. Assimon
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  5. Jeffrey M. Schaub
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  6. Tod P. Holler
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  7. Ronald W. Woodard
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Correspondence to Ronald W. Woodard.

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Cech, D.L., Wang, PF., Holt, M.C. et al. A Novel Glucose 6-Phosphate Isomerase from Listeria monocytogenes . Protein J 33, 447–456 (2014). https://doi.org/10.1007/s10930-014-9577-7

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