In Vitro Biosynthesis of the [Fe]-Hydrogenase Cofactor Verifies the Proposed Biosynthetic Precursors

Sebastian Schaupp; Francisco J. Arriaza-Gallardo; Hui jie Pan; Jörg Kahnt; Georgia Angelidou; Nicole Paczia; Kyle Costa; Xile Hu; Seigo Shima

doi:10.1002/anie.202200994

In Vitro Biosynthesis of the [Fe]-Hydrogenase Cofactor Verifies the Proposed Biosynthetic Precursors

Sebastian Schaupp, Francisco J. Arriaza-Gallardo, Hui jie Pan, Jörg Kahnt, Georgia Angelidou, Nicole Paczia, Kyle Costa, Xile Hu, Seigo Shima

Plant and Microbial Biology

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11 Scopus citations

Abstract

In the FeGP cofactor of [Fe]-hydrogenase, low-spin Fe^II is in complex with two CO ligands and a pyridinol derivative; the latter ligates the iron with a 6-acylmethyl substituent and the pyridinol nitrogen. A guanylylpyridinol derivative, 6-carboxymethyl-3,5-dimethyl-4-guanylyl-2-pyridinol (3), is produced by the decomposition of the FeGP cofactor under irradiation with UV-A/blue light and is also postulated to be a precursor of FeGP cofactor biosynthesis. HcgC and HcgB catalyze consecutive biosynthesis steps leading to 3. Here, we report an in vitro biosynthesis assay of the FeGP cofactor using the cell extract of the ΔhcgBΔhcgC strain of Methanococcus maripaludis, which does not biosynthesize 3. We chemically synthesized pyridinol precursors 1 and 2, and detected the production of the FeGP cofactor from 1, 2 and 3. These results indicated that 1, 2 and 3 are the precursors of the FeGP cofactor, and the carboxy group of 3 is converted to the acyl ligand.

Original language	English (US)
Article number	e202200994
Journal	Angewandte Chemie - International Edition
Volume	61
Issue number	22
DOIs	https://doi.org/10.1002/anie.202200994
State	Published - May 23 2022

Bibliographical note

Funding Information:
We thank Thomas Lie and John A. Leigh for providing us with the mutated strains. We thank Johann Heider and Rudolf K. Thauer for helpful discussion. This work was supported by Deutsche Forschungsgemeinschaft, Priority Program, Iron‐Sulfur for Life (SPP1927, SH87/1‐1 and SH87/1‐2) and by the Max Planck Society to S.Sh. and by the Swiss National Science Foundation (200021_181977) to X.H. Open Access funding enabled and organized by Projekt DEAL. M. maripaludis

Publisher Copyright:
© 2022 The Authors. Angewandte Chemie International Edition published by Wiley-VCH GmbH.

Keywords

Acyl Ligands
Biosynthesis
FeGP Cofactor
Guanylylpyridinol
[Fe]-Hydrogenase
Ligands
Catalysis
Iron-Sulfur Proteins/chemistry
Hydrogenase/metabolism
Iron/chemistry

PubMed: MeSH publication types

Research Support, Non-U.S. Gov't
Journal Article

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10.1002/anie.202200994

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title = "In Vitro Biosynthesis of the [Fe]-Hydrogenase Cofactor Verifies the Proposed Biosynthetic Precursors",

abstract = "In the FeGP cofactor of [Fe]-hydrogenase, low-spin FeII is in complex with two CO ligands and a pyridinol derivative; the latter ligates the iron with a 6-acylmethyl substituent and the pyridinol nitrogen. A guanylylpyridinol derivative, 6-carboxymethyl-3,5-dimethyl-4-guanylyl-2-pyridinol (3), is produced by the decomposition of the FeGP cofactor under irradiation with UV-A/blue light and is also postulated to be a precursor of FeGP cofactor biosynthesis. HcgC and HcgB catalyze consecutive biosynthesis steps leading to 3. Here, we report an in vitro biosynthesis assay of the FeGP cofactor using the cell extract of the ΔhcgBΔhcgC strain of Methanococcus maripaludis, which does not biosynthesize 3. We chemically synthesized pyridinol precursors 1 and 2, and detected the production of the FeGP cofactor from 1, 2 and 3. These results indicated that 1, 2 and 3 are the precursors of the FeGP cofactor, and the carboxy group of 3 is converted to the acyl ligand.",

keywords = "Acyl Ligands, Biosynthesis, FeGP Cofactor, Guanylylpyridinol, [Fe]-Hydrogenase, Ligands, Catalysis, Iron-Sulfur Proteins/chemistry, Hydrogenase/metabolism, Iron/chemistry",

author = "Sebastian Schaupp and Arriaza-Gallardo, {Francisco J.} and Pan, {Hui jie} and J{\"o}rg Kahnt and Georgia Angelidou and Nicole Paczia and Kyle Costa and Xile Hu and Seigo Shima",

note = "Funding Information: We thank Thomas Lie and John A. Leigh for providing us with the mutated strains. We thank Johann Heider and Rudolf K. Thauer for helpful discussion. This work was supported by Deutsche Forschungsgemeinschaft, Priority Program, Iron‐Sulfur for Life (SPP1927, SH87/1‐1 and SH87/1‐2) and by the Max Planck Society to S.Sh. and by the Swiss National Science Foundation (200021_181977) to X.H. Open Access funding enabled and organized by Projekt DEAL. M. maripaludis Publisher Copyright: {\textcopyright} 2022 The Authors. Angewandte Chemie International Edition published by Wiley-VCH GmbH.",

year = "2022",

month = may,

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doi = "10.1002/anie.202200994",

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T1 - In Vitro Biosynthesis of the [Fe]-Hydrogenase Cofactor Verifies the Proposed Biosynthetic Precursors

AU - Schaupp, Sebastian

AU - Arriaza-Gallardo, Francisco J.

AU - Pan, Hui jie

AU - Kahnt, Jörg

AU - Angelidou, Georgia

AU - Paczia, Nicole

AU - Costa, Kyle

AU - Hu, Xile

AU - Shima, Seigo

N1 - Funding Information: We thank Thomas Lie and John A. Leigh for providing us with the mutated strains. We thank Johann Heider and Rudolf K. Thauer for helpful discussion. This work was supported by Deutsche Forschungsgemeinschaft, Priority Program, Iron‐Sulfur for Life (SPP1927, SH87/1‐1 and SH87/1‐2) and by the Max Planck Society to S.Sh. and by the Swiss National Science Foundation (200021_181977) to X.H. Open Access funding enabled and organized by Projekt DEAL. M. maripaludis Publisher Copyright: © 2022 The Authors. Angewandte Chemie International Edition published by Wiley-VCH GmbH.

PY - 2022/5/23

Y1 - 2022/5/23

N2 - In the FeGP cofactor of [Fe]-hydrogenase, low-spin FeII is in complex with two CO ligands and a pyridinol derivative; the latter ligates the iron with a 6-acylmethyl substituent and the pyridinol nitrogen. A guanylylpyridinol derivative, 6-carboxymethyl-3,5-dimethyl-4-guanylyl-2-pyridinol (3), is produced by the decomposition of the FeGP cofactor under irradiation with UV-A/blue light and is also postulated to be a precursor of FeGP cofactor biosynthesis. HcgC and HcgB catalyze consecutive biosynthesis steps leading to 3. Here, we report an in vitro biosynthesis assay of the FeGP cofactor using the cell extract of the ΔhcgBΔhcgC strain of Methanococcus maripaludis, which does not biosynthesize 3. We chemically synthesized pyridinol precursors 1 and 2, and detected the production of the FeGP cofactor from 1, 2 and 3. These results indicated that 1, 2 and 3 are the precursors of the FeGP cofactor, and the carboxy group of 3 is converted to the acyl ligand.

AB - In the FeGP cofactor of [Fe]-hydrogenase, low-spin FeII is in complex with two CO ligands and a pyridinol derivative; the latter ligates the iron with a 6-acylmethyl substituent and the pyridinol nitrogen. A guanylylpyridinol derivative, 6-carboxymethyl-3,5-dimethyl-4-guanylyl-2-pyridinol (3), is produced by the decomposition of the FeGP cofactor under irradiation with UV-A/blue light and is also postulated to be a precursor of FeGP cofactor biosynthesis. HcgC and HcgB catalyze consecutive biosynthesis steps leading to 3. Here, we report an in vitro biosynthesis assay of the FeGP cofactor using the cell extract of the ΔhcgBΔhcgC strain of Methanococcus maripaludis, which does not biosynthesize 3. We chemically synthesized pyridinol precursors 1 and 2, and detected the production of the FeGP cofactor from 1, 2 and 3. These results indicated that 1, 2 and 3 are the precursors of the FeGP cofactor, and the carboxy group of 3 is converted to the acyl ligand.

KW - Acyl Ligands

KW - Biosynthesis

KW - FeGP Cofactor

KW - Guanylylpyridinol

KW - [Fe]-Hydrogenase

KW - Ligands

KW - Catalysis

KW - Iron-Sulfur Proteins/chemistry

KW - Hydrogenase/metabolism

KW - Iron/chemistry

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U2 - 10.1002/anie.202200994

DO - 10.1002/anie.202200994

M3 - Article

C2 - 35286742

AN - SCOPUS:85127532420

SN - 1433-7851

VL - 61

JO - Angewandte Chemie - International Edition

JF - Angewandte Chemie - International Edition

IS - 22

M1 - e202200994

ER -

In Vitro Biosynthesis of the [Fe]-Hydrogenase Cofactor Verifies the Proposed Biosynthetic Precursors

Abstract

Bibliographical note

Keywords

PubMed: MeSH publication types

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