Lanthanide-dependent alcohol dehydrogenases require an essential aspartate residue for metal coordination and enzymatic function
Abstract
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 andmore »
- Authors:
-
[1];
[2];
[1];
[1]
- 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)
- Publication Date:
- Research Org.:
- Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- National Science Foundation (NSF)
- OSTI Identifier:
- 1637968
- Grant/Contract Number:
- 1750003; CHE-1516126
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Volume: 295; Journal Issue: 24; Journal ID: ISSN 0021-9258
- Publisher:
- American Society for Biochemistry and Molecular Biology
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 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; XoxF; ethanol dehydrogenase; pyrroloquinoline quinone
Citation Formats
Good, Nathan M., Fellner, Matthias, Demirer, Kemal, Hu, Jian, Hausinger, Robert P., and Martinez-Gomez, N. Cecilia. Lanthanide-dependent alcohol dehydrogenases require an essential aspartate residue for metal coordination and enzymatic function. United States: N. p., 2020.
Web. doi:10.1074/jbc.ra120.013227.
Good, Nathan M., Fellner, Matthias, Demirer, Kemal, Hu, Jian, Hausinger, Robert P., & Martinez-Gomez, N. Cecilia. Lanthanide-dependent alcohol dehydrogenases require an essential aspartate residue for metal coordination and enzymatic function. United States. https://doi.org/10.1074/jbc.ra120.013227
Good, Nathan M., Fellner, Matthias, Demirer, Kemal, Hu, Jian, Hausinger, Robert P., and Martinez-Gomez, N. Cecilia. Mon .
"Lanthanide-dependent alcohol dehydrogenases require an essential aspartate residue for metal coordination and enzymatic function". United States. https://doi.org/10.1074/jbc.ra120.013227. https://www.osti.gov/servlets/purl/1637968.
@article{osti_1637968,
title = {Lanthanide-dependent alcohol dehydrogenases require an essential aspartate residue for metal coordination and enzymatic function},
author = {Good, Nathan M. and Fellner, Matthias and Demirer, Kemal and Hu, Jian and Hausinger, Robert P. and Martinez-Gomez, N. Cecilia},
abstractNote = {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.},
doi = {10.1074/jbc.ra120.013227},
journal = {Journal of Biological Chemistry},
number = 24,
volume = 295,
place = {United States},
year = {Mon May 04 00:00:00 EDT 2020},
month = {Mon May 04 00:00:00 EDT 2020}
}
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