Thioester synthesis by a designed nickel enzyme models prebiotic energy conversion

Manesis, Anastasia C.; Yerbulekova, Alina; Shearer, Jason; Shafaat, Hannah S.

doi:10.1073/pnas.2123022119

Thioester synthesis by a designed nickel enzyme models prebiotic energy conversion

Journal Article · Mon Jul 18 00:00:00 EDT 2022 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.2123022119· OSTI ID:1876508

^[1]; ^[1]; Shearer, Jason ^[2]; ^[3]

The Ohio State Biochemistry Program, The Ohio State University, Columbus, OH 43210
Department of Chemistry, Trinity University, San Antonio, TX 78212
The Ohio State Biochemistry Program, The Ohio State University, Columbus, OH 43210, Department of Chemistry and Biochemistry, The Ohio State University, Columbus, OH 43210

The formation of carbon–carbon bonds from prebiotic precursors such as carbon dioxide represents the foundation of all primordial life processes. In extant organisms, this reaction is carried out by the carbon monoxide dehydrogenase (CODH)/acetyl coenzyme A synthase (ACS) enzyme, which performs the cornerstone reaction in the ancient Wood–Ljungdahl metabolic pathway to synthesize the key biological metabolite, acetyl-CoA. Despite its significance, a fundamental understanding of this transformation is lacking, hampering efforts to harness analogous chemistry. To address these knowledge gaps, we have designed an artificial metalloenzyme within the azurin protein scaffold as a structural, functional, and mechanistic model of ACS. We demonstrate the intermediacy of the Ni ^I species and requirement for ordered substrate binding in the bioorganometallic carbon–carbon bond-forming reaction from the one-carbon ACS substrates. The electronic and geometric structures of the nickel-acetyl intermediate have been characterized using time-resolved optical, electron paramagnetic resonance, and X-ray absorption spectroscopy in conjunction with quantum chemical calculations. Moreover, we demonstrate that the nickel-acetyl species is chemically competent for selective acyl transfer upon thiol addition to biosynthesize an activated thioester. Drawing an analogy to the native enzyme, a mechanism for thioester generation by this ACS model has been proposed. The fundamental insight into the enzymatic process provided by this rudimentary ACS model has implications for the evolution of primitive ACS-like proteins. Ultimately, these findings offer strategies for development of highly active catalysts for sustainable generation of liquid fuels from one-carbon substrates, with potential for broad applications across diverse fields ranging from energy storage to environmental remediation.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0018020

OSTI ID:: 1876508

Alternate ID(s):: OSTI ID: 2472017

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 30 Vol. 119; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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Thioester synthesis by a designed nickel enzyme models prebiotic energy conversion

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