Understanding 2D-IR Spectra of Hydrogenases: A Descriptive and Predictive Computational Study
[NiFe] hydrogenases are metalloenzymes that catalyze the reversible cleavage of dihydrogen (<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><mrow><msub><mi mathvariant="normal">H</mi>...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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MDPI AG
2022-09-01
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| Series: | Catalysts |
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| Online Access: | https://www.mdpi.com/2073-4344/12/9/988 |
| _version_ | 1797490209458225152 |
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| author | Yvonne Rippers Barbara Procacci Neil T. Hunt Marius Horch |
| author_facet | Yvonne Rippers Barbara Procacci Neil T. Hunt Marius Horch |
| author_sort | Yvonne Rippers |
| collection | DOAJ |
| description | [NiFe] hydrogenases are metalloenzymes that catalyze the reversible cleavage of dihydrogen (<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><mrow><msub><mi mathvariant="normal">H</mi><mn>2</mn></msub></mrow></semantics></math></inline-formula>), a clean future fuel. Understanding the mechanism of these biocatalysts requires spectroscopic techniques that yield insights into the structure and dynamics of the [NiFe] active site. Due to the presence of CO and <inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><mrow><msup><mrow><mi>CN</mi></mrow><mo>−</mo></msup></mrow></semantics></math></inline-formula> ligands at this cofactor, infrared (IR) spectroscopy represents an ideal technique for studying these aspects, but molecular information from linear IR absorption experiments is limited. More detailed insights can be obtained from ultrafast nonlinear IR techniques like IR<sub>pump</sub>-IR<sub>probe</sub> and two-dimensional (2D-)IR spectroscopy. However, fully exploiting these advanced techniques requires an in-depth understanding of experimental observables and the encoded molecular information. To address this challenge, we present a descriptive and predictive computational approach for the simulation and analysis of static 2D-IR spectra of [NiFe] hydrogenases and similar organometallic systems. Accurate reproduction of experimental spectra from a first-coordination-sphere model suggests a decisive role of the [NiFe] core in shaping the enzymatic potential energy surface. We also reveal spectrally encoded molecular information that is not accessible by experiments, thereby helping to understand the catalytic role of the diatomic ligands, structural differences between [NiFe] intermediates, and possible energy transfer mechanisms. Our studies demonstrate the feasibility and benefits of computational spectroscopy in the 2D-IR investigation of hydrogenases, thereby further strengthening the potential of this nonlinear IR technique as a powerful research tool for the investigation of complex bioinorganic molecules. |
| first_indexed | 2024-03-10T00:27:48Z |
| format | Article |
| id | doaj.art-8892fce0703e4730b54732682adc8486 |
| institution | Directory Open Access Journal |
| issn | 2073-4344 |
| language | English |
| last_indexed | 2024-03-10T00:27:48Z |
| publishDate | 2022-09-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Catalysts |
| spelling | doaj.art-8892fce0703e4730b54732682adc84862023-11-23T15:30:30ZengMDPI AGCatalysts2073-43442022-09-0112998810.3390/catal12090988Understanding 2D-IR Spectra of Hydrogenases: A Descriptive and Predictive Computational StudyYvonne Rippers0Barbara Procacci1Neil T. Hunt2Marius Horch3Department of Physics, Freie Universität Berlin, Arnimallee 14, 14195 Berlin, GermanyDepartment of Chemistry and York Biomedical Research Institute, University of York, York YO10 5DD, UKDepartment of Chemistry and York Biomedical Research Institute, University of York, York YO10 5DD, UKDepartment of Physics, Freie Universität Berlin, Arnimallee 14, 14195 Berlin, Germany[NiFe] hydrogenases are metalloenzymes that catalyze the reversible cleavage of dihydrogen (<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><mrow><msub><mi mathvariant="normal">H</mi><mn>2</mn></msub></mrow></semantics></math></inline-formula>), a clean future fuel. Understanding the mechanism of these biocatalysts requires spectroscopic techniques that yield insights into the structure and dynamics of the [NiFe] active site. Due to the presence of CO and <inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><mrow><msup><mrow><mi>CN</mi></mrow><mo>−</mo></msup></mrow></semantics></math></inline-formula> ligands at this cofactor, infrared (IR) spectroscopy represents an ideal technique for studying these aspects, but molecular information from linear IR absorption experiments is limited. More detailed insights can be obtained from ultrafast nonlinear IR techniques like IR<sub>pump</sub>-IR<sub>probe</sub> and two-dimensional (2D-)IR spectroscopy. However, fully exploiting these advanced techniques requires an in-depth understanding of experimental observables and the encoded molecular information. To address this challenge, we present a descriptive and predictive computational approach for the simulation and analysis of static 2D-IR spectra of [NiFe] hydrogenases and similar organometallic systems. Accurate reproduction of experimental spectra from a first-coordination-sphere model suggests a decisive role of the [NiFe] core in shaping the enzymatic potential energy surface. We also reveal spectrally encoded molecular information that is not accessible by experiments, thereby helping to understand the catalytic role of the diatomic ligands, structural differences between [NiFe] intermediates, and possible energy transfer mechanisms. Our studies demonstrate the feasibility and benefits of computational spectroscopy in the 2D-IR investigation of hydrogenases, thereby further strengthening the potential of this nonlinear IR technique as a powerful research tool for the investigation of complex bioinorganic molecules.https://www.mdpi.com/2073-4344/12/9/988hydrogenasegreen hydrogenbioinorganic catalysis2D-IR spectroscopycomputational spectroscopyvibrational anharmonicity |
| spellingShingle | Yvonne Rippers Barbara Procacci Neil T. Hunt Marius Horch Understanding 2D-IR Spectra of Hydrogenases: A Descriptive and Predictive Computational Study Catalysts hydrogenase green hydrogen bioinorganic catalysis 2D-IR spectroscopy computational spectroscopy vibrational anharmonicity |
| title | Understanding 2D-IR Spectra of Hydrogenases: A Descriptive and Predictive Computational Study |
| title_full | Understanding 2D-IR Spectra of Hydrogenases: A Descriptive and Predictive Computational Study |
| title_fullStr | Understanding 2D-IR Spectra of Hydrogenases: A Descriptive and Predictive Computational Study |
| title_full_unstemmed | Understanding 2D-IR Spectra of Hydrogenases: A Descriptive and Predictive Computational Study |
| title_short | Understanding 2D-IR Spectra of Hydrogenases: A Descriptive and Predictive Computational Study |
| title_sort | understanding 2d ir spectra of hydrogenases a descriptive and predictive computational study |
| topic | hydrogenase green hydrogen bioinorganic catalysis 2D-IR spectroscopy computational spectroscopy vibrational anharmonicity |
| url | https://www.mdpi.com/2073-4344/12/9/988 |
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