Structural, Biochemical, and Evolutionary Characterizations of Glyoxylate/Hydroxypyruvate Reductases Show Their Division into Two Distinct Subfamilies
Abstract
The d-2-hydroxyacid dehydrogenase (2HADH) family illustrates a complex evolutionary history with multiple lateral gene transfers and gene duplications and losses. As a result, the exact functional annotation of individual members can be extrapolated to a very limited extent. Here, we revise the previous simplified view on the classification of the 2HADH family; specifically, we show that the previously delineated glyoxylate/hydroxypyruvate reductase (GHPR) subfamily consists of two evolutionary separated GHRA and GHRB subfamilies. We compare two representatives of these subfamilies from Sinorhizobium meliloti (SmGhrA and SmGhrB), employing a combination of biochemical, structural, and bioinformatics approaches. Our kinetic results show that both enzymes reduce several 2-ketocarboxylic acids with overlapping, but not equivalent, substrate preferences. SmGhrA and SmGhrB show highest activity with glyoxylate and hydroxypyruvate, respectively; in addition, only SmGhrB reduces 2-keto-d-gluconate, and only SmGhrA reduces pyruvate (with low efficiency). We present nine crystal structures of both enzymes in apo forms and in complexes with cofactors and substrates/substrate analogues. In particular, we determined a crystal structure of SmGhrB with 2-keto-d-gluconate, which is the biggest substrate cocrystallized with a 2HADH member. Here, the structures reveal significant differences between SmGhrA and SmGhrB, both in the overall structure and within the substrate-binding pocket, offering insight intomore »
- Authors:
-
[2];
[3];
[1]
- Univ. of Virginia, Charlottesville, VA (United States); Univ. of Warsaw (Poland)
- Univ. of Virginia, Charlottesville, VA (United States)
- Univ. of Warsaw (Poland)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); Michigan Economic Development Corporation; Michigan Technology Tri-Corridor; NIGMS
- OSTI Identifier:
- 1424792
- Grant/Contract Number:
- AC02-06CH11357; 085P1000817; U54-GM094662; R01-GM117080; HG008424
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Biochemistry
- Additional Journal Information:
- Journal Volume: 57; Journal Issue: 6; Journal ID: ISSN 0006-2960
- Publisher:
- American Chemical Society (ACS)
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; anions; peptides and proteins; ligands; crystal structure; chemical structure
Citation Formats
Kutner, Jan, Shabalin, Ivan G., Matelska, Dorota, Handing, Katarzyna B., Gasiorowska, Olga, Sroka, Piotr, Gorna, Maria W., Ginalski, Krzysztof, Wozniak, Krzysztof, and Minor, Wladek. Structural, Biochemical, and Evolutionary Characterizations of Glyoxylate/Hydroxypyruvate Reductases Show Their Division into Two Distinct Subfamilies. United States: N. p., 2018.
Web. doi:10.1021/acs.biochem.7b01137.
Kutner, Jan, Shabalin, Ivan G., Matelska, Dorota, Handing, Katarzyna B., Gasiorowska, Olga, Sroka, Piotr, Gorna, Maria W., Ginalski, Krzysztof, Wozniak, Krzysztof, & Minor, Wladek. Structural, Biochemical, and Evolutionary Characterizations of Glyoxylate/Hydroxypyruvate Reductases Show Their Division into Two Distinct Subfamilies. United States. https://doi.org/10.1021/acs.biochem.7b01137
Kutner, Jan, Shabalin, Ivan G., Matelska, Dorota, Handing, Katarzyna B., Gasiorowska, Olga, Sroka, Piotr, Gorna, Maria W., Ginalski, Krzysztof, Wozniak, Krzysztof, and Minor, Wladek. Mon .
"Structural, Biochemical, and Evolutionary Characterizations of Glyoxylate/Hydroxypyruvate Reductases Show Their Division into Two Distinct Subfamilies". United States. https://doi.org/10.1021/acs.biochem.7b01137. https://www.osti.gov/servlets/purl/1424792.
@article{osti_1424792,
title = {Structural, Biochemical, and Evolutionary Characterizations of Glyoxylate/Hydroxypyruvate Reductases Show Their Division into Two Distinct Subfamilies},
author = {Kutner, Jan and Shabalin, Ivan G. and Matelska, Dorota and Handing, Katarzyna B. and Gasiorowska, Olga and Sroka, Piotr and Gorna, Maria W. and Ginalski, Krzysztof and Wozniak, Krzysztof and Minor, Wladek},
abstractNote = {The d-2-hydroxyacid dehydrogenase (2HADH) family illustrates a complex evolutionary history with multiple lateral gene transfers and gene duplications and losses. As a result, the exact functional annotation of individual members can be extrapolated to a very limited extent. Here, we revise the previous simplified view on the classification of the 2HADH family; specifically, we show that the previously delineated glyoxylate/hydroxypyruvate reductase (GHPR) subfamily consists of two evolutionary separated GHRA and GHRB subfamilies. We compare two representatives of these subfamilies from Sinorhizobium meliloti (SmGhrA and SmGhrB), employing a combination of biochemical, structural, and bioinformatics approaches. Our kinetic results show that both enzymes reduce several 2-ketocarboxylic acids with overlapping, but not equivalent, substrate preferences. SmGhrA and SmGhrB show highest activity with glyoxylate and hydroxypyruvate, respectively; in addition, only SmGhrB reduces 2-keto-d-gluconate, and only SmGhrA reduces pyruvate (with low efficiency). We present nine crystal structures of both enzymes in apo forms and in complexes with cofactors and substrates/substrate analogues. In particular, we determined a crystal structure of SmGhrB with 2-keto-d-gluconate, which is the biggest substrate cocrystallized with a 2HADH member. Here, the structures reveal significant differences between SmGhrA and SmGhrB, both in the overall structure and within the substrate-binding pocket, offering insight into the molecular basis for the observed substrate preferences and subfamily differences. In addition, we provide an overview of all GHRA and GHRB structures complexed with a ligand in the active site.},
doi = {10.1021/acs.biochem.7b01137},
journal = {Biochemistry},
number = 6,
volume = 57,
place = {United States},
year = {Mon Jan 08 00:00:00 EST 2018},
month = {Mon Jan 08 00:00:00 EST 2018}
}
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