Producing glucose 6-phosphate from cellulosic biomass: Structural insights into levoglucosan bioconversion

Bacik, John -Paul; Klesmith, Justin R.; Whitehead, Timothy A.; Jarboe, Laura R.; Unkefer, Clifford J.; Mark, Brian L.; Michalczyk, Ryszard

doi:10.1074/jbc.M115.674614

Title: Producing glucose 6-phosphate from cellulosic biomass: Structural insights into levoglucosan bioconversion

Journal Article · Wed Sep 09 00:00:00 EDT 2015 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.M115.674614· OSTI ID:1258283

Bacik, John -Paul ^[1];

^[2]; Whitehead, Timothy A. ^[2]; Jarboe, Laura R. ^[3]; Unkefer, Clifford J. ^[1]; Mark, Brian L. ^[4]; Michalczyk, Ryszard ^[1]

Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Michigan State Univ., East Lansing, MI (United States)
Iowa State Univ., Ames, IA (United States)
Univ. of Manitoba, Winnipeg, MB (Canada)

The most abundant carbohydrate product of cellulosic biomass pyrolysis is the anhydrosugar levoglucosan (1,6-anhydro-β-d-glucopyranose), which can be converted to glucose 6-phosphate by levoglucosan kinase (LGK). In addition to the canonical kinase phosphotransfer reaction, the conversion requires cleavage of the 1,6-anhydro ring to allow ATP-dependent phosphorylation of the sugar O6 atom. Using x-ray crystallography, we show that LGK binds two magnesium ions in the active site that are additionally coordinated with the nucleotide and water molecules to result in ideal octahedral coordination. To further verify the metal binding sites, we co-crystallized LGK in the presence of manganese instead of magnesium and solved the structure de novo using the anomalous signal from four manganese atoms in the dimeric structure. The first metal is required for catalysis, whereas our work suggests that the second is either required or significantly promotes the catalytic rate. Although the enzyme binds its sugar substrate in a similar orientation to the structurally related 1,6-anhydro-N-acetylmuramic acid kinase (AnmK), it forms markedly fewer bonding interactions with the substrate. In this orientation, the sugar is in an optimal position to couple phosphorylation with ring cleavage. We also observed a second alternate binding orientation for levoglucosan, and in these structures, ADP was found to bind with lower affinity. These combined observations provide an explanation for the high Km of LGK for levoglucosan. Furthermore, greater knowledge of the factors that contribute to the catalytic efficiency of LGK can be used to improve applications of this enzyme for levoglucosan-derived biofuel production.

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Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1258283

Report Number(s):: LA-UR-15-27036

Journal Information:: Journal of Biological Chemistry, Vol. 290, Issue 44; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 12 works

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Title: Producing glucose 6-phosphate from cellulosic biomass: Structural insights into levoglucosan bioconversion

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