Catalytic Activity of the Archetype from Group 4 of the FTR-like Ferredoxin:Thioredoxin Reductase Family Is Regulated by Unique S=7/2 and S=1/2 [4Fe-4S] Clusters

被引:0
作者
Prakash, Divya [1 ]
Xiong, Jin [2 ]
Chauhan, Shikha S. [1 ]
Walters, Karim A. [3 ]
Kruse, Hannah [1 ]
Yennawar, Neela [4 ]
Golbeck, John H. [3 ,5 ]
Guo, Yisong [2 ]
Ferry, James G. [3 ]
机构
[1] Southern Illinois Univ, Sch Chem & Biomol Sci, Carbondale, IL 62901 USA
[2] Carnegie Mellon Univ, Dept Chem, Pittsburgh, PA 15213 USA
[3] Penn State Univ, Dept Biochem & Mol Biol, University Pk, PA 16802 USA
[4] Penn State Univ, Huck Inst Life Sci, University Pk, PA 16802 USA
[5] Penn State Univ, Dept Chem, University Pk, PA 16802 USA
基金
美国国家卫生研究院;
关键词
FERREDOXIN-THIOREDOXIN REDUCTASE; METHANOSARCINA-ACETIVORANS; FUNDAMENTAL PROCESSES; DISULFIDE REDUCTION; ENZYME; SITE; PROTEINS; SYSTEM; PURIFICATION; CHLOROPLAST;
D O I
10.1021/acs.biochem.3c00651
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Thioredoxin reductases (TrxR) activate thioredoxins (Trx) that regulate the activity of diverse target proteins essential to prokaryotic and eukaryotic life. However, very little is understood of TrxR/Trx systems and redox control in methanogenic microbes from the domain Archaea (methanogens), for which genomes are abundant with annotations for ferredoxin:thioredoxin reductases [Fdx/thioredoxin reductase (FTR)] from group 4 of the widespread FTR-like family. Only two from the FTR-like family are characterized: the plant-type FTR from group 1 and FDR from group 6. Herein, the group 4 archetype (AFTR) from Methanosarcina acetivorans was characterized to advance understanding of the family and TrxR/Trx systems in methanogens. The modeled structure of AFTR, together with EPR and Mossbauer spectroscopies, supports a catalytic mechanism similar to plant-type FTR and FDR, albeit with important exceptions. EPR spectroscopy of reduced AFTR identified a transient [4Fe-4S](1+) cluster exhibiting a mixture of S = 7/2 and typical S = 1/2 signals, although rare for proteins containing [4Fe-4S] clusters, it is most likely the on-pathway intermediate in the disulfide reduction. Furthermore, an active site histidine equivalent to residues essential for the activity of plant-type FTR and FDR was found dispensable for AFTR. Finally, a unique thioredoxin system was reconstituted from AFTR, ferredoxin, and Trx2 from M. acetivorans, for which specialized target proteins were identified that are essential for growth and other diverse metabolisms.
引用
收藏
页码:1588 / 1598
页数:11
相关论文
共 48 条
  • [1] RESOLUTION OF COMPONENT PROTEINS IN AN ENZYME COMPLEX FROM METHANOSARCINA-THERMOPHILA CATALYZING THE SYNTHESIS OR CLEAVAGE OF ACETYL-COA
    ABBANAT, DR
    FERRY, JG
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1991, 88 (08) : 3272 - 3276
  • [2] A complete ferredoxin/thioredoxin system regulates fundamental processes in amyloplasts
    Balmer, Y
    Vensel, WH
    Cai, N
    Manieri, W
    Schürmann, P
    Hurkman, WJ
    Buchanan, BB
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2006, 103 (08) : 2988 - 2993
  • [3] Ferredoxin:thioredoxin reductase (FTR) links the regulation of oxygenic photosynthesis to deeply rooted bacteria
    Balsera, Monica
    Uberegui, Estefania
    Susanti, Dwi
    Schmitz, Ruth A.
    Mukhopadhyay, Biswarup
    Schuermann, Peter
    Buchanan, Bob B.
    [J]. PLANTA, 2013, 237 (02) : 619 - 635
  • [4] Redox-dependent acetyl transfer partial reaction of the acetyl-CoA decarbonylase/synthase complex: Kinetics and mechanism
    Bhaskar, B
    DeMoll, E
    Grahame, DA
    [J]. BIOCHEMISTRY, 1998, 37 (41) : 14491 - 14499
  • [5] Benzoyl-CoA reductase (dearomatizing), a key enzyme of anaerobic aromatic metabolism - A study of adenosinetriphosphatase activity, ATP stoichiometry of the reaction and EPR properties of the enzyme
    Boll, M
    Albracht, SSP
    Fuchs, G
    [J]. EUROPEAN JOURNAL OF BIOCHEMISTRY, 1997, 244 (03): : 840 - 851
  • [6] Ferredoxin-linked flavoenzyme defines a family of pyridine nucleotide-independent thioredoxin reductases
    Buey, Ruben M.
    Fernandez-Justel, David
    de Pereda, Jose M.
    Revuelta, Jose L.
    Schurmann, Peter
    Buchanan, Bob B.
    Balsera, Monica
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2018, 115 (51) : 12967 - 12972
  • [7] Mossbauer, Electron Paramagnetic Resonance, and Theoretical Studies of a Carbene-Based All-Ferrous Fe4S4 Cluster: Electronic Origin and Structural Identification of the Unique Spectroscopic Site
    Chakrabarti, Mrinmoy
    Deng, Liang
    Holm, R. H.
    Munck, Eckard
    Bominaar, Emile L.
    [J]. INORGANIC CHEMISTRY, 2009, 48 (07) : 2735 - 2747
  • [8] Structural snapshots along the reaction pathway of ferredoxin-thioredoxin reductase
    Dai, Shaodong
    Friemann, Rosmarie
    Glauser, Dominique A.
    Bourquin, Florence
    Manieri, Wanda
    Schuermann, Peter
    Eklund, Hans
    [J]. NATURE, 2007, 448 (7149) : 92 - 102
  • [9] Glutathione analogs in prokaryotes
    Fahey, Robert C.
    [J]. BIOCHIMICA ET BIOPHYSICA ACTA-GENERAL SUBJECTS, 2013, 1830 (05): : 3182 - 3198
  • [10] Methanosarcina acetivorans: A Model for Mechanistic Understanding of Aceticlastic and Reverse Methanogenesis
    Ferry, James G.
    [J]. FRONTIERS IN MICROBIOLOGY, 2020, 11