Terminal Hydride Species in [FeFe]‐Hydrogenases Are Vibrationally Coupled to the Active Site Environment

Pham, Cindy C.; Mulder, David W.; Pelmenschikov, Vladimir; King, Paul W.; Ratzloff, Michael W.; Wang, Hongxin; Mishra, Nakul; Ercan, E.; Zhao, Jiyong; Hu, Michael Y.; Tamasaku, Kenji; Yoda, Yoshitaka; Cramer, Stephen P.

doi:10.1002/ange.201805144

Cited by 9 publications

(26 citation statements)

References 31 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…1). 38,39 (Fig. 4) led to a downshift of the vCO bands owing to binding and activation of H 2 or D 2 accompanied by reduction of the resting state H cluster (Fig.…”

Section: Resultsmentioning

confidence: 99%

The Hydricity and Reactivity Relationship in [ FeFe ]-hydrogenases

Artz¹,

Mulder²,

Ratzloff³

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

Reactivity of transition metal catalysts is controlled by covalent and non-covalent interactions that tune thermodynamic properties including hydricity. Hydricity is critical to catalytic activity and for modulating the reduction or oxidation of chemical compounds. Likewise, enzymes can employ transition metal cofactors and use metal-hydride intermediates tuned by protein frameworks to selectively control reactivity. One example, the [FeFe]-hydrogenases, catalyze reversible H2 activation with H2 oxidation to H+ reduction ratios spanning ~107 in rate, offering a model to determine the extent that hydricity controls reactivity. To address this question, the hydricity of the catalytic H cluster of two [FeFe]-hydrogenases, CpI and CpII, were compared. We show that for CpI, the higher rates of H+ reduction correspond to a more hydridic H cluster, whereas CpII, which strongly favors H2 oxidation, has a less hydridic H cluster. The results demonstrate that enzymes manipulate metal cofactor hydricity to enable an extraordinary range of chemical reactivity.

show abstract

“…1). 38,39 (Fig. 4) led to a downshift of the vCO bands owing to binding and activation of H 2 or D 2 accompanied by reduction of the resting state H cluster (Fig.…”

Section: Resultsmentioning

confidence: 99%

The Hydricity and Reactivity Relationship in [ FeFe ]-hydrogenases

Artz¹,

Mulder²,

Ratzloff³

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…[77,78] We note that the models we suggest have distinct molecular and electronic structures that should be spectroscopically distinguishable, if experimental problems associated with low accumulation of reduced FeMoco states can be overcome or if belt Fe-selective 57 Fe isotope labelling of FeMoco becomes possible. [79] Apart from ENDOR, direct detection of a hydride (or possibly the terminal SH group) through, for example, 57 Fe nuclear resonance vibrational spectroscopy (as has recently been successfully applied to hydrogenase enzymes [80][81][82][83][84] ) could become possible and a spectroscopic experiment sensitive to Fe oxidation state (e. g., Mössbauer or Fe X-ray absorption) should in principle allow a clear distinction between E 2 -hyd and E 2 -nonhyd models.…”

Section: Discussionmentioning

confidence: 99%

The E₂ state of FeMoco: Hydride Formation versus Fe Reduction and a Mechanism for H₂ Evolution

Thorhallsson

Björnsson

2021

Chemistry A European J

View full text Add to dashboard Cite

The iron-molybdenum cofactor (FeMoco) is responsible for dinitrogen reduction in Mo nitrogenase. Unlike the resting state, E 0 , reduced states of FeMoco are much less well characterized. The E 2 state has been proposed to contain a hydride but direct spectroscopic evidence is still lacking. The E 2 state can, however, relax back the E 0 state via a H 2 sidereaction, implying a hydride intermediate prior to H 2 formation. This E 2 !E 0 pathway is one of the primary mechanisms for H 2 formation under low-electron flux conditions. In this study we present an exploration of the energy surface of the E 2 state. Utilizing both cluster-continuum and QM/MM calculations, we explore various classes of E 2 models: including terminal hydrides, bridging hydrides with a closed or open sulfide-bridge, as well as models without. Impor-tantly, we find the hemilability of a protonated belt-sulfide to strongly influence the stability of hydrides. Surprisingly, nonhydride models are found to be almost equally favorable as hydride models. While the cluster-continuum calculations suggest multiple possibilities, QM/MM suggests only two models as contenders for the E 2 state. These models feature either i) a bridging hydride between Fe 2 and Fe 6 and an open sulfide-bridge with terminal SH on Fe 6 (E 2 -hyd) or ii) a double belt-sulfide protonated, reduced cofactor without a hydride (E 2 -nonhyd). We suggest both models as contenders for the E 2 redox state and further calculate a mechanism for H 2 evolution. The changes in electronic structure of FeMoco during the proposed redox-state cycle, E 0 !E 1 !E 2 !E 0 , are discussed.

show abstract

“…The further confirmation of this feature involved two more aspects: (3) a tripled incident X-ray intensity (with 0.8 meV energy resolution) at BL19LXU (vs. that at BL09XU), and (4) the H/D pair comparison, as shown in Figure 15d2. After the historical observation of this Ni-H-Fe peak, terminal X-Fe-H bending features inside several FeFe hydrogenses were also successfully observed, and their detailed structures were identified via DFT calculations [44,45,47,69]. In addition to the Fe-H bending features, Fe-D or Fe-H stretching features at highenergy regions stand out from all other features and can provide additional and better reference points for DFT calculation vs. proposed structures.…”

Section: Fe-h Vibrations and Structuresmentioning

confidence: 87%

“…People need 36-48 h to move in and set up the HRM and other instruments at the beginning of each beamtime [8]. Nevertheless, researchers are rewarded with amazing NRVS results [7,8,45,47,[65][66][67][68][69].…”

Section: High-resolution Monochromatorsmentioning

confidence: 99%

“…For example, an [FeFe] hydrogenase enzyme such as the one in Figure 2a1 often has various iron–sulfur clusters in addition to its H-cluster (a2) which hosts the reaction center [2Fe] H (a2, green circled and shaded) [ 30 , 43 ]. Nevertheless, we are now able to identify and label the two irons just inside the [2Fe] H center or six irons inside the H-cluster with 57 Fe while leaving other irons unlabeled [ 30 , 31 , 44 , 45 ]. This lets the corresponding NRVS spectra specifically represent the irons inside the [2Fe] H center (or H-cluster).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Nuclear Resonance Vibrational Spectroscopy: A Modern Tool to Pinpoint Site-Specific Cooperative Processes

et al. 2021

Self Cite

View full text Add to dashboard Cite

Nuclear resonant vibrational spectroscopy (NRVS) is a synchrotron radiation (SR)-based nuclear inelastic scattering spectroscopy that measures the phonons (i.e., vibrational modes) associated with the nuclear transition. It has distinct advantages over traditional vibration spectroscopy and has wide applications in physics, chemistry, bioinorganic chemistry, materials sciences, and geology, as well as many other research areas. In this article, we present a scientific and figurative description of this yet modern tool for the potential users in various research fields in the future. In addition to short discussions on its development history, principles, and other theoretical issues, the focus of this article is on the experimental aspects, such as the instruments, the practical measurement issues, the data process, and a few examples of its applications. The article concludes with introduction to non-57Fe NRVS and an outlook on the impact from the future upgrade of SR rings.

show abstract

Terminal Hydride Species in [FeFe]‐Hydrogenases Are Vibrationally Coupled to the Active Site Environment

Abstract: This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record.

Cited by 9 publications

References 31 publications

The Hydricity and Reactivity Relationship in [ FeFe ]-hydrogenases

The Hydricity and Reactivity Relationship in [ FeFe ]-hydrogenases

The E₂ state of FeMoco: Hydride Formation versus Fe Reduction and a Mechanism for H₂ Evolution

Nuclear Resonance Vibrational Spectroscopy: A Modern Tool to Pinpoint Site-Specific Cooperative Processes

Contact Info

Product

Resources

About

Terminal Hydride Species in [FeFe]‐Hydrogenases Are Vibrationally Coupled to the Active Site Environment

Abstract: This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record.

Cited by 9 publications

References 31 publications

The Hydricity and Reactivity Relationship in [ FeFe ]-hydrogenases

The Hydricity and Reactivity Relationship in [ FeFe ]-hydrogenases

The E2 state of FeMoco: Hydride Formation versus Fe Reduction and a Mechanism for H2 Evolution

Nuclear Resonance Vibrational Spectroscopy: A Modern Tool to Pinpoint Site-Specific Cooperative Processes

Contact Info

Product

Resources

About

The E₂ state of FeMoco: Hydride Formation versus Fe Reduction and a Mechanism for H₂ Evolution