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Title: Toward a mechanistic and physiological understanding of a ferredoxin:disulfide reductase from the domains Archaea and Bacteria

Abstract

Disulfide reductases reduce other proteins and are critically important for cellular redox signaling and homeostasis. Methanosarcina acetivorans is a methane-producing microbe from the domain Archaea that produces a ferredoxin:disulfide reductase (FDR) for which the crystal structure has been reported, yet its biochemical mechanism and physiological substrates are unknown. FDR and the extensively characterized plant-type ferredoxin:thioredoxin reductase (FTR) belong to a distinct class of disulfide reductases that contain a unique active-site [4Fe-4S] cluster. The results reported in this paper support a mechanism for FDR similar to that reported for FTR with notable exceptions. Unlike FTR, FDR contains a rubredoxin [1Fe-0S] center postulated to mediate electron transfer from ferredoxin to the active-site [4Fe-4S] cluster. UV-Vis, EPR and Mӧssbauer spectroscopic data indicated that two-electron reduction of the active-site disulfide in FDR involves a one-electron-reduced [4Fe-4S] 1+ intermediate previously hypothesized for FTR. Our results support a role for an active-site tyrosine in FDR that occupies the equivalent position of an essential histidine in the active-site of FTR. Of note, one of seven Trxs encoded in the genome (Trx5) and methanoredoxin, a glutaredoxin-like enzyme from M. acetivorans, were reduced by FDR advancing the physiological understanding of FDRs role in the redox metabolism of methanoarchaea. Finally,more » bioinformatics analyses show FDR homologs are widespread in diverse microbes from the domain Bacteria.« less

Authors:
 [1];  [1]; ORCiD logo [2];  [3];  [4];  [5];  [6];  [6]; ORCiD logo [1]
  1. Pennsylvania State Univ., University Park, PA (United States). Dept. of Biochemistry and Molecular Biology
  2. Pennsylvania State Univ., University Park, PA (United States). Dept. of Chemistry
  3. Univ. of Arkansas, Fayetteville, AR (United States). Dept. of Biological Sciences; ImmunoVision, Inc., Springdale, AR (United States)
  4. Pennsylvania State Univ., University Park, PA (United States). Dept. of Biochemistry and Molecular Biology; Sardar Patel Renewable Energy, Gujarat (India). Research Inst.
  5. Univ. of Arkansas, Fayetteville, AR (United States). Dept. of Biological Sciences
  6. Pennsylvania State Univ., University Park, PA (United States). Dept. of Biochemistry and Molecular Biology, and Dept. of Chemistry
Publication Date:
Research Org.:
Pennsylvania State Univ., University Park, PA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1540311
Grant/Contract Number:  
FG02-95ER20198
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Biological Chemistry
Additional Journal Information:
Journal Volume: 293; Journal Issue: 24; Journal ID: ISSN 0021-9258
Publisher:
American Society for Biochemistry and Molecular Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biochemistry & molecular biology; archaea; stress; enzyme mechanism; disulfide; thioredoxin; Methanosarcina acetivorans; anaerobic; methanoarchaea; redox maintenance; ferredoxin; thioredoxin reductase

Citation Formats

Prakash, Divya, Walters, Karim A., Martinie, Ryan J., McCarver, Addison C., Kumar, Adepu K., Lessner, Daniel J., Krebs, Carsten, Golbeck, John H., and Ferry, James G. Toward a mechanistic and physiological understanding of a ferredoxin:disulfide reductase from the domains Archaea and Bacteria. United States: N. p., 2018. Web. doi:10.1074/jbc.ra118.002473.
Prakash, Divya, Walters, Karim A., Martinie, Ryan J., McCarver, Addison C., Kumar, Adepu K., Lessner, Daniel J., Krebs, Carsten, Golbeck, John H., & Ferry, James G. Toward a mechanistic and physiological understanding of a ferredoxin:disulfide reductase from the domains Archaea and Bacteria. United States. doi:10.1074/jbc.ra118.002473.
Prakash, Divya, Walters, Karim A., Martinie, Ryan J., McCarver, Addison C., Kumar, Adepu K., Lessner, Daniel J., Krebs, Carsten, Golbeck, John H., and Ferry, James G. Wed . "Toward a mechanistic and physiological understanding of a ferredoxin:disulfide reductase from the domains Archaea and Bacteria". United States. doi:10.1074/jbc.ra118.002473. https://www.osti.gov/servlets/purl/1540311.
@article{osti_1540311,
title = {Toward a mechanistic and physiological understanding of a ferredoxin:disulfide reductase from the domains Archaea and Bacteria},
author = {Prakash, Divya and Walters, Karim A. and Martinie, Ryan J. and McCarver, Addison C. and Kumar, Adepu K. and Lessner, Daniel J. and Krebs, Carsten and Golbeck, John H. and Ferry, James G.},
abstractNote = {Disulfide reductases reduce other proteins and are critically important for cellular redox signaling and homeostasis. Methanosarcina acetivorans is a methane-producing microbe from the domain Archaea that produces a ferredoxin:disulfide reductase (FDR) for which the crystal structure has been reported, yet its biochemical mechanism and physiological substrates are unknown. FDR and the extensively characterized plant-type ferredoxin:thioredoxin reductase (FTR) belong to a distinct class of disulfide reductases that contain a unique active-site [4Fe-4S] cluster. The results reported in this paper support a mechanism for FDR similar to that reported for FTR with notable exceptions. Unlike FTR, FDR contains a rubredoxin [1Fe-0S] center postulated to mediate electron transfer from ferredoxin to the active-site [4Fe-4S] cluster. UV-Vis, EPR and Mӧssbauer spectroscopic data indicated that two-electron reduction of the active-site disulfide in FDR involves a one-electron-reduced [4Fe-4S]1+ intermediate previously hypothesized for FTR. Our results support a role for an active-site tyrosine in FDR that occupies the equivalent position of an essential histidine in the active-site of FTR. Of note, one of seven Trxs encoded in the genome (Trx5) and methanoredoxin, a glutaredoxin-like enzyme from M. acetivorans, were reduced by FDR advancing the physiological understanding of FDRs role in the redox metabolism of methanoarchaea. Finally, bioinformatics analyses show FDR homologs are widespread in diverse microbes from the domain Bacteria.},
doi = {10.1074/jbc.ra118.002473},
journal = {Journal of Biological Chemistry},
number = 24,
volume = 293,
place = {United States},
year = {2018},
month = {5}
}

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