DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: A Ferredoxin Disulfide Reductase Delivers Electrons to the Methanosarcina barkeri Class III Ribonucleotide Reductase

Abstract

Two subtypes of class III anaerobic ribonucleotide reductases (RNRs) studied so far couple the reduction of ribonucleotides to the oxidation of formate, or the oxidation of NADPH via thioredoxin and thioredoxin reductase. Certain methanogenic archaea contain a phylogenetically distinct third subtype of class III RNR, with distinct active-site residues. Here we report the cloning and recombinant expression of the Methanosarcina barkeri class III RNR and show that the electrons required for ribonucleotide reduction can be delivered by a [4Fe-4S] protein ferredoxin disulfide reductase, and a conserved thioredoxin-like protein NrdH present in the RNR operon. The diversity of class III RNRs reflects the diversity of electron carriers used in anaerobic metabolism

Authors:
;  [1];  [2];  [2];  [1];
  1. Department of Chemistry, Boston University, 590 Commonwealth Avenue, Boston, Massachusetts 02215, United States
  2. Department of Biochemistry and Molecular Biology, Pennsylvania State University, University Park, Pennsylvania 16802, United States
Publication Date:
Research Org.:
Pennsylvania State Univ., University Park, PA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1234035
Alternate Identifier(s):
OSTI ID: 1438007
Grant/Contract Number:  
FG02-95ER20198 MOD16; FG02-95ER20198
Resource Type:
Published Article
Journal Name:
Biochemistry
Additional Journal Information:
Journal Name: Biochemistry Journal Volume: 54 Journal Issue: 47; Journal ID: ISSN 0006-2960
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Wei, Yifeng, Li, Bin, Prakash, Divya, Ferry, James G., Elliott, Sean J., and Stubbe, JoAnne. A Ferredoxin Disulfide Reductase Delivers Electrons to the Methanosarcina barkeri Class III Ribonucleotide Reductase. United States: N. p., 2015. Web. doi:10.1021/acs.biochem.5b01092.
Wei, Yifeng, Li, Bin, Prakash, Divya, Ferry, James G., Elliott, Sean J., & Stubbe, JoAnne. A Ferredoxin Disulfide Reductase Delivers Electrons to the Methanosarcina barkeri Class III Ribonucleotide Reductase. United States. https://doi.org/10.1021/acs.biochem.5b01092
Wei, Yifeng, Li, Bin, Prakash, Divya, Ferry, James G., Elliott, Sean J., and Stubbe, JoAnne. Thu . "A Ferredoxin Disulfide Reductase Delivers Electrons to the Methanosarcina barkeri Class III Ribonucleotide Reductase". United States. https://doi.org/10.1021/acs.biochem.5b01092.
@article{osti_1234035,
title = {A Ferredoxin Disulfide Reductase Delivers Electrons to the Methanosarcina barkeri Class III Ribonucleotide Reductase},
author = {Wei, Yifeng and Li, Bin and Prakash, Divya and Ferry, James G. and Elliott, Sean J. and Stubbe, JoAnne},
abstractNote = {Two subtypes of class III anaerobic ribonucleotide reductases (RNRs) studied so far couple the reduction of ribonucleotides to the oxidation of formate, or the oxidation of NADPH via thioredoxin and thioredoxin reductase. Certain methanogenic archaea contain a phylogenetically distinct third subtype of class III RNR, with distinct active-site residues. Here we report the cloning and recombinant expression of the Methanosarcina barkeri class III RNR and show that the electrons required for ribonucleotide reduction can be delivered by a [4Fe-4S] protein ferredoxin disulfide reductase, and a conserved thioredoxin-like protein NrdH present in the RNR operon. The diversity of class III RNRs reflects the diversity of electron carriers used in anaerobic metabolism},
doi = {10.1021/acs.biochem.5b01092},
journal = {Biochemistry},
number = 47,
volume = 54,
place = {United States},
year = {Thu Nov 19 00:00:00 EST 2015},
month = {Thu Nov 19 00:00:00 EST 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1021/acs.biochem.5b01092

Citation Metrics:
Cited by: 15 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Molecular characterization of the thioredoxin system from Methanosarcina acetivorans
journal, September 2014

  • McCarver, Addison C.; Lessner, Daniel J.
  • FEBS Journal, Vol. 281, Issue 20
  • DOI: 10.1111/febs.12964

Rheostat Re-Wired: Alternative Hypotheses for the Control of Thioredoxin Reduction Potentials
journal, April 2015


The Genome of M. acetivorans Reveals Extensive Metabolic and Physiological Diversity
journal, April 2002


The Zn center of the anaerobic ribonucleotide reductase from E. coli
journal, April 2009

  • Luttringer, Florence; Mulliez, Etienne; Dublet, Bernard
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 14, Issue 6
  • DOI: 10.1007/s00775-009-0505-9

Lipoamide Dehydrogenase, Glutathione Reductase, Thioredoxin Reductase, and Thioredoxin
journal, November 1967

  • Williams, Charles H.; Zanetti, Giuliana; Arscott, L. David
  • Journal of Biological Chemistry, Vol. 242, Issue 22
  • DOI: 10.1016/S0021-9258(18)99415-9

Microbial Reefs in the Black Sea Fueled by Anaerobic Oxidation of Methane
journal, August 2002


Higher-level classification of the Archaea: evolution of methanogenesis and methanogens
journal, January 2005

  • Bapteste, Éric; Brochier, Céline; Boucher, Yan
  • Archaea, Vol. 1, Issue 5
  • DOI: 10.1155/2005/859728

The genome sequence of the psychrophilic archaeon, Methanococcoides burtonii: the role of genome evolution in cold adaptation
journal, April 2009

  • Allen, Michelle A.; Lauro, Federico M.; Williams, Timothy J.
  • The ISME Journal, Vol. 3, Issue 9
  • DOI: 10.1038/ismej.2009.45

Structural mechanism of allosteric substrate specificity regulation in a ribonucleotide reductase
journal, October 2004

  • Larsson, Karl-Magnus; Jordan, Albert; Eliasson, Rolf
  • Nature Structural & Molecular Biology, Vol. 11, Issue 11
  • DOI: 10.1038/nsmb838

Structural and Biochemical Characterization of a Ferredoxin:Thioredoxin Reductase-like Enzyme from Methanosarcina acetivorans
journal, May 2015


Direct Electrochemical Characterization of Archaeal Thioredoxins
journal, May 2007

  • Chobot, Sarah E.; Hernandez, Hector H.; Drennan, Catherine L.
  • Angewandte Chemie, Vol. 119, Issue 22
  • DOI: 10.1002/ange.200604620

Structural basis for allosteric regulation of human ribonucleotide reductase by nucleotide-induced oligomerization
journal, February 2011

  • Fairman, James Wesley; Wijerathna, Sanath Ranjan; Ahmad, Md Faiz
  • Nature Structural & Molecular Biology, Vol. 18, Issue 3
  • DOI: 10.1038/nsmb.2007

The Function and Properties of the Iron−Sulfur Center in Spinach Ferredoxin:Thioredoxin Reductase:  A New Biological Role for Iron−Sulfur Clusters
journal, January 1996

  • Staples, Christopher R.; Ameyibor, Emmanuel; Fu, Weiguang
  • Biochemistry, Vol. 35, Issue 35
  • DOI: 10.1021/bi961007p

Microscopic p K a Values of Escherichia coli Thioredoxin
journal, December 1997

  • Chivers, Peter T.; Prehoda, Kenneth E.; Volkman, Brian F.
  • Biochemistry, Vol. 36, Issue 48
  • DOI: 10.1021/bi970071j

Direct cloning of the trxB gene that encodes thioredoxin reductase.
journal, January 1985


The state of copper in stellacyanin and laccase from the lacquer tree Rhus vernicifera
journal, April 1970

  • Malmström, Bo G.; Reinhammar, Bengt; Vänngård, Tore
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 205, Issue 1
  • DOI: 10.1016/0005-2728(70)90060-5

The Free Radical of the Anaerobic Ribonucleotide Reductase from Escherichia coli Is at Glycine 681
journal, March 1996

  • Sun, Xueyin; Ollagnier, Sandrine; Schmidt, Peter P.
  • Journal of Biological Chemistry, Vol. 271, Issue 12
  • DOI: 10.1074/jbc.271.12.6827

Ferredoxin:thioredoxin reductase (FTR) links the regulation of oxygenic photosynthesis to deeply rooted bacteria
journal, December 2012


The Crystal Structure of Thermotoga maritima Class III Ribonucleotide Reductase Lacks a Radical Cysteine Pre-Positioned in the Active Site
journal, July 2015


Purification and properties of an F420-dependent NADP reductase from methanobacterium thermoautotrophicum
journal, December 1984


Activation of the Anaerobic Ribonucleotide Reductase by S-Adenosylmethionine
journal, September 2005

  • Gambarelli, Serge; Luttringer, Florence; Padovani, Dominique
  • ChemBioChem, Vol. 6, Issue 11
  • DOI: 10.1002/cbic.200500182

A model for the role of multiple cysteine residues involved in ribonucleotide reduction: amazing and still confusing
journal, October 1992

  • Mao, S. S.; Holler, T. P.; Yu, G. X.
  • Biochemistry, Vol. 31, Issue 40
  • DOI: 10.1021/bi00155a029

Ribonucleotide reductases in the twenty-first century
journal, March 1998


Coenzyme B12-Dependent Ribonucleotide Reductase: Evidence for the Participation of Five Cysteine Residues in Ribonucleotide Reduction
journal, October 1994

  • Booker, Squire; Licht, Stuart; Broderick, Joan
  • Biochemistry, Vol. 33, Issue 42
  • DOI: 10.1021/bi00208a019

Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase
journal, June 2010

  • Costa, K. C.; Wong, P. M.; Wang, T.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 24
  • DOI: 10.1073/pnas.1003653107

Enzymatic assembly of DNA molecules up to several hundred kilobases
journal, April 2009

  • Gibson, Daniel G.; Young, Lei; Chuang, Ray-Yuan
  • Nature Methods, Vol. 6, Issue 5, p. 343-345
  • DOI: 10.1038/nmeth.1318

Purine biosynthesis in the domain Archaea without folates or modified folates
journal, May 1997


DNA building blocks: keeping control of manufacture
journal, September 2011

  • Hofer, Anders; Crona, Mikael; Logan, Derek T.
  • Critical Reviews in Biochemistry and Molecular Biology, Vol. 47, Issue 1
  • DOI: 10.3109/10409238.2011.630372

A radical-chemical route to acetyl-CoA: the anaerobically induced pyruvate formate-lyase system of Escherichia coli
journal, August 1990


Naturally occurring 5-deazaflavin coenzymes: biological redox roles
journal, June 1986


Enzymology of one-carbon metabolism in methanogenic pathways
journal, January 1999


Ribonucleotide Reductases
journal, June 2006


Measurement of Thioredoxin and Thioredoxin Reductase
journal, May 2005


The class III ribonucleotide reductase from Neisseria bacilliformis can utilize thioredoxin as a reductant
journal, August 2014

  • Wei, Y.; Funk, M. A.; Rosado, L. A.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 36
  • DOI: 10.1073/pnas.1414396111

Formate is the hydrogen donor for the anaerobic ribonucleotide reductase from Escherichia coli.
journal, September 1995

  • Mulliez, E.; Ollagnier, S.; Fontecave, M.
  • Proceedings of the National Academy of Sciences, Vol. 92, Issue 19
  • DOI: 10.1073/pnas.92.19.8759

Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage
journal, July 2013

  • Haroon, Mohamed F.; Hu, Shihu; Shi, Ying
  • Nature, Vol. 500, Issue 7464
  • DOI: 10.1038/nature12375

A Chemically Competent Thiosulfuranyl Radical on the Escherichia coli Class III Ribonucleotide Reductase
journal, June 2014

  • Wei, Yifeng; Mathies, Guinevere; Yokoyama, Kenichi
  • Journal of the American Chemical Society, Vol. 136, Issue 25
  • DOI: 10.1021/ja5030194

Thiyl Radicals in Ribonucleotide Reductases
journal, January 1996


Molecular Mechanisms of Thioredoxin and Glutaredoxin as Hydrogen Donors for Mammalian S Phase Ribonucleotide Reductase
journal, March 2009

  • Avval, Farnaz Zahedi; Holmgren, Arne
  • Journal of Biological Chemistry, Vol. 284, Issue 13
  • DOI: 10.1074/jbc.M809338200

Cloning, sequencing, and expression of the adenosylcobalamin-dependent ribonucleotide reductase from Lactobacillus leichmannii.
journal, September 1993

  • Booker, S.; Stubbe, J.
  • Proceedings of the National Academy of Sciences, Vol. 90, Issue 18
  • DOI: 10.1073/pnas.90.18.8352

A rapid assay for CDP reductase activity in mammalian cell extracts
journal, March 1970


Mimicking the active site of protein disulfide-isomerase by substitution of proline 34 in Escherichia coli thioredoxin
journal, May 1991


High-field EPR detection of a disulfide radical anion in the reduction of cytidine 5'-diphosphate by the E441Q R1 mutant of Escherichia coli ribonucleotide reductase
journal, August 1999

  • Lawrence, C. C.; Bennati, M.; Obias, H. V.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 16
  • DOI: 10.1073/pnas.96.16.8979

Characterization of Escherichia coli NrdH : A GLUTAREDOXIN-LIKE PROTEIN WITH A THIOREDOXIN-LIKE ACTIVITY PROFILE
journal, July 1997

  • Jordan, Albert; Åslund, Fredrik; Pontis, Elisabet
  • Journal of Biological Chemistry, Vol. 272, Issue 29
  • DOI: 10.1074/jbc.272.29.18044

A Continuous, Spectrophotometric Activity Assay for Nitrogenase Using the Reductant Titanium(III) Citrate
journal, September 1994


Methanogenic archaea: ecologically relevant differences in energy conservation
journal, June 2008

  • Thauer, Rudolf K.; Kaster, Anne-Kristin; Seedorf, Henning
  • Nature Reviews Microbiology, Vol. 6, Issue 8
  • DOI: 10.1038/nrmicro1931

SOAS: A free program to analyze electrochemical data and other one-dimensional signals
journal, September 2009


Structural Insight into KCNQ (Kv7) Channel Assembly and Channelopathy
journal, March 2007


Complete Genome Sequence of Methanosaeta concilii, a Specialist in Aceticlastic Methanogenesis
journal, May 2011

  • Barber, R. D.; Zhang, L.; Harnack, M.
  • Journal of Bacteriology, Vol. 193, Issue 14
  • DOI: 10.1128/JB.05031-11

Physiological functions of thioredoxin and thioredoxin reductase: Thioredoxin and thioredoxin reductase
journal, October 2000


Methanotrophic archaea possessing diverging methane-oxidizing and electron-transporting pathways
journal, December 2013