Lanthanide-dependent alcohol dehydrogenases require an essential aspartate residue for metal coordination and enzymatic function

Good, Nathan M.; Fellner, Matthias; Demirer, Kemal; Hu, Jian; Hausinger, Robert P.; Martinez-Gomez, N. Cecilia

doi:10.1074/jbc.ra120.013227

Title: Lanthanide-dependent alcohol dehydrogenases require an essential aspartate residue for metal coordination and enzymatic function

Journal Article · Mon May 04 00:00:00 EDT 2020 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.ra120.013227· OSTI ID:1637968

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^[2]; Demirer, Kemal ^[3]; Hu, Jian ^[1];

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Michigan State Univ., East Lansing, MI (United States)
Michigan State Univ., East Lansing, MI (United States); Univ. of Otago, Dunedin (New Zeland)
Michigan State Univ., East Lansing, MI (United States); Okemos High School, MI (United States)

The lanthanide elements (Ln³⁺), those with atomic numbers 57–63 (excluding promethium, Pm³⁺), form a cofactor complex with pyrroloquinoline quinone (PQQ) in bacterial XoxF methanol dehydrogenases (MDHs) and ExaF ethanol dehydrogenases (EDHs), expanding the range of biological elements and opening novel areas of metabolism and ecology. Other MDHs, known as MxaFIs, are related in sequence and structure to these proteins, yet they instead possess a Ca²⁺-PQQ cofactor. An important missing piece of the Ln³⁺ puzzle is defining what features distinguish enzymes that use Ln³⁺-PQQ cofactors from those that do not. In this work, using XoxF1 MDH from the model methylotrophic bacterium Methylorubrum extorquens AM1, we investigated the functional importance of a proposed lanthanide-coordinating aspartate residue. We report two crystal structures of XoxF1, one with and another without PQQ, both with La³⁺ bound in the active-site region and coordinated by Asp³²⁰. Using constructs to produce either recombinant XoxF1 or its D320A variant, we show that Asp³²⁰ is needed for in vivo catalytic function, in vitro activity, and La³⁺ coordination. XoxF1 and XoxF1 D320A, when produced in the absence of La³⁺, coordinated Ca²⁺ but exhibited little or no catalytic activity. We also generated the parallel substitution in ExaF to produce ExaF D319S and found that this variant loses the capacity for efficient ethanol oxidation with La³⁺. These results provide evidence that a Ln³⁺-coordinating aspartate is essential for the enzymatic functions of XoxF MDHs and ExaF EDHs, supporting the notion that sequences of these enzymes, and the genes that encode them, are markers for Ln³⁺ metabolism.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Science Foundation (NSF)

Grant/Contract Number:: 1750003; CHE-1516126

OSTI ID:: 1637968

Journal Information:: Journal of Biological Chemistry, Vol. 295, Issue 24; 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: 25 works

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59 BASIC BIOLOGICAL SCIENCES
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
one-carbon metabolism
metalloprotein
alcohol dehydrogenase (ADH)
crystallography
aspartate (aspartic acid)
cofactor coordination
ExaF
lanthanide
methanol dehydrogenase
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ethanol dehydrogenase
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Title: Lanthanide-dependent alcohol dehydrogenases require an essential aspartate residue for metal coordination and enzymatic function

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