Tracing the incorporation of the “ninth sulfur” into the nitrogenase cofactor precursor with selenite and tellurite

Tanifuji, Kazuki; Jasniewski, Andrew J.; Villarreal, David; Stiebritz, Martin T.; Lee, Chi Chung; Wilcoxen, Jarett; Okhi, Yasuhiro; Chatterjee, Ruchira; Bogacz, Isabel; Yano, Junko; Kern, Jan; Hedman, Britt; Hodgson, Keith O.; Britt, R. David; Hu, Yilin; Ribbe, Markus W.

doi:10.1038/s41557-021-00799-8

Title: Tracing the incorporation of the “ninth sulfur” into the nitrogenase cofactor precursor with selenite and tellurite

Abstract

We report Molybdenum nitrogenase catalyses the reduction of N₂ to NH₃ at its cofactor, an [(R-homocitrate)MoFe₇S₉C] cluster synthesized via the formation of a [Fe₈S₉C] L-cluster prior to the insertion of molybdenum and homocitrate. We have previously identified a [Fe₈S₈C] L*-cluster, which is homologous to the core structure of the L-cluster but lacks the ‘ninth sulfur’ in the belt region. However, direct evidence and mechanistic details of the L*- to L-cluster conversion upon ‘ninth sulfur’ insertion remain elusive. Here we trace the ‘ninth sulfur’ insertion using SeO₃^2- and TeO₃^2- as ‘labelled’ SO₃^2-. Biochemical, electron paramagnetic resonance and X-ray absorption spectroscopy/extended X-ray absorption fine structure studies suggest a role of the ‘ninth sulfur’ in cluster transfer during cofactor biosynthesis while revealing the incorporation of Se^2-- and Te^2--like species into the L-cluster. Density functional theory calculations further point to a plausible mechanism involving in situ reduction of SO₃^2- to S^2-, thereby suggesting the utility of this reaction to label the catalytically important belt region for mechanistic investigations of nitrogenase.

Authors:

Tanifuji, Kazuki ^[1];

^[2]; Villarreal, David ^[3]; Stiebritz, Martin T. ^[2]; Lee, Chi Chung ^[2];

^[4];

^[5]; Chatterjee, Ruchira ^[6]; Bogacz, Isabel ^[6];

^[6];

^[6]; Hedman, Britt ^[7]; Hodgson, Keith O. ^[8];

^[3];

^[2];

^[2]

Univ. of California, Irvine, CA (United States); Kyoto Univ. (Japan)
Univ. of California, Irvine, CA (United States)
Univ. of California, Davis, CA (United States)
Univ. of Wisconsin, Madison, WI (United States)
Kyoto Univ. (Japan)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
SLAC National Accelerator Lab., Menlo Park, CA (United States)
SLAC National Accelerator Lab., Menlo Park, CA (United States); Stanford Univ., CA (United States)

Publication Date:: Mon Oct 11 00:00:00 EDT 2021

Research Org.:: SLAC National Accelerator Lab., Menlo Park, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); MEXT Japan; Kyoto University Research Fund for Young Scientist

OSTI Identifier:: 1870879

Grant/Contract Number:: AC02-76SF00515; GM67626; GM141046; R35 GM126961; GM110501; GM126289; 19H02733; 20K21207; P30GM133894

Resource Type:: Accepted Manuscript

Journal Name:: Nature Chemistry

Additional Journal Information:: Journal Volume: 13; Journal Issue: 12; Journal ID: ISSN 1755-4330

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

Subject:: 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; biocatalysis; biosynthesis; metalloproteins

Citation Formats


                    Tanifuji, Kazuki, Jasniewski, Andrew J., Villarreal, David, Stiebritz, Martin T., Lee, Chi Chung, Wilcoxen, Jarett, Okhi, Yasuhiro, Chatterjee, Ruchira, Bogacz, Isabel, Yano, Junko, Kern, Jan, Hedman, Britt, Hodgson, Keith O., Britt, R. David, Hu, Yilin, and Ribbe, Markus W. Tracing the incorporation of the “ninth sulfur” into the nitrogenase cofactor precursor with selenite and tellurite.  United States: N. p., 2021. 
Web.  doi:10.1038/s41557-021-00799-8.

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                    Tanifuji, Kazuki, Jasniewski, Andrew J., Villarreal, David, Stiebritz, Martin T., Lee, Chi Chung, Wilcoxen, Jarett, Okhi, Yasuhiro, Chatterjee, Ruchira, Bogacz, Isabel, Yano, Junko, Kern, Jan, Hedman, Britt, Hodgson, Keith O., Britt, R. David, Hu, Yilin, & Ribbe, Markus W. Tracing the incorporation of the “ninth sulfur” into the nitrogenase cofactor precursor with selenite and tellurite.  United States.  https://doi.org/10.1038/s41557-021-00799-8

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                    Tanifuji, Kazuki, Jasniewski, Andrew J., Villarreal, David, Stiebritz, Martin T., Lee, Chi Chung, Wilcoxen, Jarett, Okhi, Yasuhiro, Chatterjee, Ruchira, Bogacz, Isabel, Yano, Junko, Kern, Jan, Hedman, Britt, Hodgson, Keith O., Britt, R. David, Hu, Yilin, and Ribbe, Markus W. Mon .  
"Tracing the incorporation of the “ninth sulfur” into the nitrogenase cofactor precursor with selenite and tellurite".  United States.  https://doi.org/10.1038/s41557-021-00799-8.  https://www.osti.gov/servlets/purl/1870879.

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@article{osti_1870879,

  title        = {Tracing the incorporation of the “ninth sulfur” into the nitrogenase cofactor precursor with selenite and tellurite},

  author       = {Tanifuji, Kazuki and Jasniewski, Andrew J. and Villarreal, David and Stiebritz, Martin T. and Lee, Chi Chung and Wilcoxen, Jarett and Okhi, Yasuhiro and Chatterjee, Ruchira and Bogacz, Isabel and Yano, Junko and Kern, Jan and Hedman, Britt and Hodgson, Keith O. and Britt, R. David and Hu, Yilin and Ribbe, Markus W.},

  abstractNote = {We report Molybdenum nitrogenase catalyses the reduction of N2 to NH3 at its cofactor, an [(R-homocitrate)MoFe7S9C] cluster synthesized via the formation of a [Fe8S9C] L-cluster prior to the insertion of molybdenum and homocitrate. We have previously identified a [Fe8S8C] L*-cluster, which is homologous to the core structure of the L-cluster but lacks the ‘ninth sulfur’ in the belt region. However, direct evidence and mechanistic details of the L*- to L-cluster conversion upon ‘ninth sulfur’ insertion remain elusive. Here we trace the ‘ninth sulfur’ insertion using SeO32- and TeO32- as ‘labelled’ SO32-. Biochemical, electron paramagnetic resonance and X-ray absorption spectroscopy/extended X-ray absorption fine structure studies suggest a role of the ‘ninth sulfur’ in cluster transfer during cofactor biosynthesis while revealing the incorporation of Se2-- and Te2--like species into the L-cluster. Density functional theory calculations further point to a plausible mechanism involving in situ reduction of SO32- to S2-, thereby suggesting the utility of this reaction to label the catalytically important belt region for mechanistic investigations of nitrogenase.},

  doi          = {10.1038/s41557-021-00799-8},

  journal      = {Nature Chemistry},

  number       = 12,

  volume       = 13,

  place        = {United States},

  year         = {Mon Oct 11 00:00:00 EDT 2021},

  month        = {Mon Oct 11 00:00:00 EDT 2021}

}

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Title: Tracing the incorporation of the “ninth sulfur” into the nitrogenase cofactor precursor with selenite and tellurite

Abstract

Citation Formats

All-Ferrous Titanium(III) Citrate Reduced Fe Protein of Nitrogenase: An XAS Study of Electronic and Metrical Structure journal, June 1998

X‐Ray Crystallographic Analysis of NifB with a Full Complement of Clusters: Structural Insights into the Radical SAM‐Dependent Carbide Insertion During Nitrogenase Cofactor Assembly journal, December 2020

Nitrogenase MoFe-Protein at 1.16 A Resolution: A Central Ligand in the FeMo-Cofactor journal, September 2002

Maturation of nitrogenase cofactor — the role of a class E radical SAM methyltransferase NifB journal, April 2016

Rethinking the Nitrogenase Mechanism: Activating the Active Site journal, November 2019

Electron Transfer in Nitrogenase journal, January 2020

New Synthetic Routes to Metal-Sulfur Clusters Relevant to the Nitrogenase Metallo-Clusters journal, May 2013

Spectroscopic Characterization of an Eight-Iron Nitrogenase Cofactor Precursor that Lacks the “9 th Sulfur” journal, September 2019

Structural evidence for a dynamic metallocofactor during N 2 reduction by Mo-nitrogenase journal, June 2020

Reactivity, Mechanism, and Assembly of the Alternative Nitrogenases journal, March 2020

Biosynthesis of Nitrogenase Metalloclusters journal, December 2013

Biosynthesis of the Metalloclusters of Nitrogenases journal, June 2016

Identity and function of an essential nitrogen ligand of the nitrogenase cofactor biosynthesis protein NifB journal, April 2020

[Fe4Te4(TePh)4]3⊖, the First Telluride–Tellurolate Complex journal, October 1987

Catalysis-dependent selenium incorporation and migration in the nitrogenase active site iron-molybdenum cofactor journal, December 2015

Nitrogenase Fe protein: A molybdate/homocitrate insertase journal, October 2006

Radical SAM-Dependent Carbon Insertion into the Nitrogenase M-Cluster journal, September 2012

Evidence for Interstitial Carbon in Nitrogenase FeMo Cofactor journal, November 2011

FeMo cofactor maturation on NifEN journal, October 2006

Ligand binding to the FeMo-cofactor: Structures of CO-bound and reactivated nitrogenase journal, September 2014

Probing the coordination and function of Fe4S4 modules in nitrogenase assembly protein NifB journal, July 2018

The tetranuclear trianion [Fe4Te4(SC6H5)4]3-: crystal and molecular structure and magnetic properties journal, September 1990

Acidities of Arsenic (III) and Arsenic (V) Thio- and Oxyacids in Aqueous Solution using the CBS-QB3/CPCM Method journal, April 2009

Mechanism of Molybdenum Nitrogenase journal, January 1996

Developments in the Biomimetic Chemistry of Cubane-Type and Higher Nuclearity Iron–Sulfur Clusters journal, January 2014

Selenium substitution in [Fe4S4(SR)4]2-: synthesis and comparative properties of [Fe4X4(YC6H5)4]2- (X, Y = sulfur, selenium) and the structure of [(CH3)4N]2[Fe4Se4(SC6H5)4] journal, June 1978

Synthetic nickel-iron NiFe3Q4 cubane-type clusters (S = 3/2) by reductive rearrangement of linear [Fe3Q4(SEt)4]3- (Q = sulfur, selenium) journal, October 1990

Tracing the ‘ninth sulfur’ of the nitrogenase cofactor via a semi-synthetic approach journal, April 2018

All-Ferrous Titanium(III) Citrate Reduced Fe Protein of Nitrogenase: An XAS Study of Electronic and Metrical Structure
journal, June 1998

X‐Ray Crystallographic Analysis of NifB with a Full Complement of Clusters: Structural Insights into the Radical SAM‐Dependent Carbide Insertion During Nitrogenase Cofactor Assembly
journal, December 2020

Nitrogenase MoFe-Protein at 1.16 A Resolution: A Central Ligand in the FeMo-Cofactor
journal, September 2002

Maturation of nitrogenase cofactor — the role of a class E radical SAM methyltransferase NifB
journal, April 2016

Rethinking the Nitrogenase Mechanism: Activating the Active Site
journal, November 2019

Electron Transfer in Nitrogenase
journal, January 2020

New Synthetic Routes to Metal-Sulfur Clusters Relevant to the Nitrogenase Metallo-Clusters
journal, May 2013

Spectroscopic Characterization of an Eight-Iron Nitrogenase Cofactor Precursor that Lacks the “9 ^th Sulfur”
journal, September 2019

Structural evidence for a dynamic metallocofactor during N ₂ reduction by Mo-nitrogenase
journal, June 2020

Reactivity, Mechanism, and Assembly of the Alternative Nitrogenases
journal, March 2020

Biosynthesis of Nitrogenase Metalloclusters
journal, December 2013

Biosynthesis of the Metalloclusters of Nitrogenases
journal, June 2016

Identity and function of an essential nitrogen ligand of the nitrogenase cofactor biosynthesis protein NifB
journal, April 2020

[Fe4Te4(TePh)4]3⊖, the First Telluride–Tellurolate Complex
journal, October 1987

Catalysis-dependent selenium incorporation and migration in the nitrogenase active site iron-molybdenum cofactor
journal, December 2015

Nitrogenase Fe protein: A molybdate/homocitrate insertase
journal, October 2006

Radical SAM-Dependent Carbon Insertion into the Nitrogenase M-Cluster
journal, September 2012

Evidence for Interstitial Carbon in Nitrogenase FeMo Cofactor
journal, November 2011

FeMo cofactor maturation on NifEN
journal, October 2006

Ligand binding to the FeMo-cofactor: Structures of CO-bound and reactivated nitrogenase
journal, September 2014

Probing the coordination and function of Fe4S4 modules in nitrogenase assembly protein NifB
journal, July 2018

The tetranuclear trianion [Fe4Te4(SC6H5)4]3-: crystal and molecular structure and magnetic properties
journal, September 1990

Acidities of Arsenic (III) and Arsenic (V) Thio- and Oxyacids in Aqueous Solution using the CBS-QB3/CPCM Method
journal, April 2009

Mechanism of Molybdenum Nitrogenase
journal, January 1996

Developments in the Biomimetic Chemistry of Cubane-Type and Higher Nuclearity Iron–Sulfur Clusters
journal, January 2014

Selenium substitution in [Fe4S4(SR)4]2-: synthesis and comparative properties of [Fe4X4(YC6H5)4]2- (X, Y = sulfur, selenium) and the structure of [(CH3)4N]2[Fe4Se4(SC6H5)4]
journal, June 1978

Synthetic nickel-iron NiFe3Q4 cubane-type clusters (S = 3/2) by reductive rearrangement of linear [Fe3Q4(SEt)4]3- (Q = sulfur, selenium)
journal, October 1990

Tracing the ‘ninth sulfur’ of the nitrogenase cofactor via a semi-synthetic approach
journal, April 2018