X-ray Crystallography and Vibrational Spectroscopy Reveal the Key Determinants of Biocatalytic Dihydrogen Cycling by [NiFe] Hydrogenases

TY - JOUR

T1 - X-ray Crystallography and Vibrational Spectroscopy Reveal the Key Determinants of Biocatalytic Dihydrogen Cycling by [NiFe] Hydrogenases

AU - Ilina, Yulia

AU - Lorent, Christian

AU - Katz, Sagie

AU - Jeoung, Jae Hun

AU - Shima, Seigo

AU - Horch, Marius

AU - Zebger, Ingo

AU - Dobbek, Holger

N1 - © 2019 The Authors.

PY - 2019/10/25

Y1 - 2019/10/25

N2 - [NiFe] hydrogenases are complex model enzymes for the reversible cleavage of dihydrogen (H2). However, structural determinants of efficient H2 binding to their [NiFe] active site are not properly understood. Here, we present crystallographic and vibrational-spectroscopic insights into the unexplored structure of the H2-binding [NiFe] intermediate. Using an F420-reducing [NiFe]-hydrogenase from Methanosarcina barkeri as a model enzyme, we show that the protein backbone provides a strained chelating scaffold that tunes the [NiFe] active site for efficient H2 binding and conversion. The protein matrix also directs H2 diffusion to the [NiFe] site via two gas channels and allows the distribution of electrons between functional protomers through a subunit-bridging FeS cluster. Our findings emphasize the relevance of an atypical Ni coordination, thereby providing a blueprint for the design of bio-inspired H2-conversion catalysts.

AB - [NiFe] hydrogenases are complex model enzymes for the reversible cleavage of dihydrogen (H2). However, structural determinants of efficient H2 binding to their [NiFe] active site are not properly understood. Here, we present crystallographic and vibrational-spectroscopic insights into the unexplored structure of the H2-binding [NiFe] intermediate. Using an F420-reducing [NiFe]-hydrogenase from Methanosarcina barkeri as a model enzyme, we show that the protein backbone provides a strained chelating scaffold that tunes the [NiFe] active site for efficient H2 binding and conversion. The protein matrix also directs H2 diffusion to the [NiFe] site via two gas channels and allows the distribution of electrons between functional protomers through a subunit-bridging FeS cluster. Our findings emphasize the relevance of an atypical Ni coordination, thereby providing a blueprint for the design of bio-inspired H2-conversion catalysts.

KW - biocatalysis

KW - crystal structure

KW - hydrogen activation

KW - vibrational spectroscopy

KW - [NiFe] hydrogenase

UR - http://www.scopus.com/inward/record.url?scp=85074565065&partnerID=8YFLogxK

U2 - 10.1002/anie.201908258

DO - 10.1002/anie.201908258

M3 - Article

AN - SCOPUS:85074565065

SN - 1433-7851

JO - Angewandte Chemie - International Edition

JF - Angewandte Chemie - International Edition

ER -