Successes, challenges, and opportunities for quantum chemistry in understanding metalloenzymes for solar fuels research

Orio, Maylis; Pantazis, Dimitrios A.

doi:10.1039/d1cc00705j

Cited by 28 publications

(35 citation statements)

References 334 publications

(435 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Water oxidation is catalyzed by the Mn 4 Ca cluster in photosystem II (PSII). Our understanding of water oxidation by the Mn 4 Ca cluster has progressed rapidly in recent years because of advances in structural, computational, and biophysical methods (for review, see refs − ). PSII is a large dimeric protein complex that is integral to the thylakoid membrane and is surrounded by a light-harvesting apparatus that increases the light-absorbing cross-section of PSII and transfers excitation energy to the PSII core.…”

Section: Introductionmentioning

confidence: 99%

Alteration of the O₂-Producing Mn₄Ca Cluster in Photosystem II by the Mutation of a Metal Ligand

Debus

2021

Biochemistry

View full text Add to dashboard Cite

The O 2 -evolving Mn 4 Ca cluster in photosystem II (PSII) is arranged as a distorted Mn 3 Ca cube that is linked to a fourth Mn ion (denoted as Mn4) by two oxo bridges. The Mn4 and Ca ions are bridged by residue D1-D170. This is also the only residue known to participate in the high-affinity Mn(II) site that participates in the light-driven assembly of the Mn 4 Ca cluster. In this study, we use Fourier transform infrared difference spectroscopy to characterize the impact of the D1-D170E mutation. On the basis of analyses of carboxylate and carbonyl stretching modes and the O−H stretching modes of hydrogen-bonded water molecules, we show that this mutation alters the extensive network of hydrogen bonds that surrounds the Mn 4 Ca cluster in the same manner as that of many other mutations. It also alters the equilibrium between conformers of the Mn 4 Ca cluster in the dark-stable S 1 state so that a high-spin form of the S 2 state is produced during the S 1 -to-S 2 transition instead of the low-spin form that gives rise to the S 2 state multiline electron paramagnetic resonance signal. The mutation may also change the coordination mode of the carboxylate group at position 170 to unidentate ligation of Mn4. This is the first mutation of a metal ligand in PSII that substantially impacts the spectroscopic signatures of the Mn 4 Ca cluster without substantially eliminating O 2 evolution. The results have significant implications for our understanding of the roles of alternate active/inactive conformers of the Mn 4 Ca cluster in the mechanism of O 2 formation.

show abstract

Section: Introductionmentioning

confidence: 99%

Alteration of the O₂-Producing Mn₄Ca Cluster in Photosystem II by the Mutation of a Metal Ligand

Debus

2021

Biochemistry

View full text Add to dashboard Cite

show abstract

“…4,80,124 The S 3 B,unbound state may either evolve to S 3 A,W via S 3 B,W after (reversible) water binding by the "pivot" or "carousel" mechanism 43,44,120,132−134 through the route (e) → (f) and then advance to the O 2 formation routes described above, or, as suggested by Pantazis and collaborators, directly proceed to S 4 B,unbound without water binding by the route (g) → (h). 68,69,87 The latter pathway involves a penta-coordinate Mn4(IV) center and would lead to Mn4(V) where nucleophilic Ox-O5 coupling 68,69,87 or hydroxo-oxo coupling between W2 and O5 might be possible. We note that the finding in the present study can provide an additional route (a) → (c) → (i) → (h) from S 3 A,W to S 4 B,unbound (other than from S 3 B,unbound…”

mentioning

confidence: 99%

Reversible Structural Isomerization of Nature’s Water Oxidation Catalyst Prior to O–O Bond Formation

et al. 2022

View full text Add to dashboard Cite

Photosynthetic water oxidation is catalyzed by a manganese−calcium oxide cluster, which experiences five "S-states" during a light-driven reaction cycle. The unique "distorted chair"like geometry of the Mn 4 CaO 5(6) cluster shows structural flexibility that has been frequently proposed to involve "open" and "closed"cubane forms from the S 1 to S 3 states. The isomers are interconvertible in the S 1 and S 2 states, while in the S 3 state, the open-cubane structure is observed to dominate inThermosynechococcus elongatus (cyanobacteria) samples. In this work, using density functional theory calculations, we go beyond the S 3 + Y z state to the S 3 n Y z • → S 4 + Y z step, and report for the first time that the reversible isomerism, which is suppressed in the S 3 + Y z state, is fully recovered in the ensuing S 3 n Y z • state due to the proton release from a manganese-bound water ligand. The altered coordination strength of the manganese−ligand facilitates formation of the closed-cubane form, in a dynamic equilibrium with the open-cubane form. This tautomerism immediately preceding dioxygen formation may constitute the rate limiting step for O 2 formation, and exert a significant influence on the water oxidation mechanism in photosystem II.

show abstract

“…Their quality was analysed based on both objectives. The analysis for the clashes was done with standard filtering (threshold of 100 Å) 3,19,60 and post-processing the best pathways with the QM-based method to analyse noncovalent interactions in biomolecules NCIPLOT4 (ref. 62) (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Molecular modelling has become a major ally in chemical biology with outstanding contributions in drug design and biocatalysis amongst others. [1][2][3] It has also reached a prominent position in bioinorganics as demonstrated by a plethora of studies dedicated to studying the catalytic mechanism of metalloenzymes or their inhibitions. [4][5][6][7][8][9][10][11] Nowadays, modelers count on a wide variety of methods whose applicability depends on the system to treat and the molecular variables to analyse.…”

Section: Introductionmentioning

confidence: 99%

“…15 (2) The homogeneous catalyst brings a stable and well-dened rst coordination sphere of the metal and avoids creating from scratch a metal binding site based purely on natural amino acids. (3) The protein can be handled with the same protein engineering techniques as other enzymes (e.g., mutagenesis, directed evolution, etc.) to control substrate specicity and enantioselectivity.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Successes and challenges in multiscale modelling of artificial metalloenzymes: the case study of POP-Rh₂cyclopropanase

et al. 2022

View full text Add to dashboard Cite

show abstract

Successes, challenges, and opportunities for quantum chemistry in understanding metalloenzymes for solar fuels research

Abstract: Quantum chemical approaches today are a powerful tool to study the properties and reactivity of metalloenzymes. In the field of solar fuels research these involve predominantly photosystem II and hydrogenases,...

Cited by 28 publications

References 334 publications

Alteration of the O₂-Producing Mn₄Ca Cluster in Photosystem II by the Mutation of a Metal Ligand

Alteration of the O₂-Producing Mn₄Ca Cluster in Photosystem II by the Mutation of a Metal Ligand

Reversible Structural Isomerization of Nature’s Water Oxidation Catalyst Prior to O–O Bond Formation

Successes and challenges in multiscale modelling of artificial metalloenzymes: the case study of POP-Rh₂cyclopropanase

Contact Info

Product

Resources

About

Successes, challenges, and opportunities for quantum chemistry in understanding metalloenzymes for solar fuels research

Abstract: Quantum chemical approaches today are a powerful tool to study the properties and reactivity of metalloenzymes. In the field of solar fuels research these involve predominantly photosystem II and hydrogenases,...

Cited by 28 publications

References 334 publications

Alteration of the O2-Producing Mn4Ca Cluster in Photosystem II by the Mutation of a Metal Ligand

Alteration of the O2-Producing Mn4Ca Cluster in Photosystem II by the Mutation of a Metal Ligand

Reversible Structural Isomerization of Nature’s Water Oxidation Catalyst Prior to O–O Bond Formation

Successes and challenges in multiscale modelling of artificial metalloenzymes: the case study of POP-Rh2cyclopropanase

Contact Info

Product

Resources

About

Alteration of the O₂-Producing Mn₄Ca Cluster in Photosystem II by the Mutation of a Metal Ligand

Alteration of the O₂-Producing Mn₄Ca Cluster in Photosystem II by the Mutation of a Metal Ligand

Successes and challenges in multiscale modelling of artificial metalloenzymes: the case study of POP-Rh₂cyclopropanase