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Title: A Reduced F 420 -Dependent Nitrite Reductase in an Anaerobic Methanotrophic Archaeon

Journal Article · · Journal of Bacteriology
DOI:https://doi.org/10.1128/jb.00078-22· OSTI ID:1874394
 [1];  [2]; ORCiD logo [3];  [4];  [2];  [4];  [3];  [5];
  1. Genetics, Bioinformatics, and Computational Biology Ph.D. Program, Virginia Tech, Blacksburg, Virginia, USA, Department of Biochemistry, Virginia Tech, Blacksburg, Virginia, USA
  2. Department of Biochemistry, Virginia Tech, Blacksburg, Virginia, USA
  3. Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California, USA
  4. Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA
  5. Department of Biochemistry, Virginia Tech, Blacksburg, Virginia, USA, Virginia Tech Carilion School of Medicine, Virginia Tech, Blacksburg, Virginia, USA

Anaerobic methanotrophic archaea (ANME), which oxidize methane in marine sediments through syntrophic associations with sulfate-reducing bacteria, carry homologs of coenzyme F420-dependent sulfite reductase (Fsr) of Methanocaldococcus jannaschii, a hyperthermophilic methanogen from deep-sea hydrothermal vents. M. jannaschii Fsr (MjFsr) and ANME-Fsr belong to two phylogenetically distinct groups, FsrI and FsrII, respectively. MjFsrI reduces sulfite to sulfide with reduced F420 (F420H2), protecting methyl coenzyme M reductase (Mcr), an essential enzyme for methanogens, from sulfite inhibition. However, the function of FsrIIs in ANME, which also rely on Mcr and live in sulfidic environments, is unknown. We have determined the catalytic properties of FsrII from a member of ANME-2c. Since ANME remain to be isolated, we expressed ANME2c-FsrII in a closely related methanogen, Methanosarcina acetivorans. Purified recombinant FsrII contained siroheme, indicating that the methanogen, which lacks a native sulfite reductase, produced this coenzyme. Unexpectedly, FsrII could not reduce sulfite or thiosulfate with F420H2. Instead, it acted as an F420H2-dependent nitrite reductase (FNiR) with physiologically relevant Km values (nitrite, 5 μM; F420H2, 14 μM). From kinetic, thermodynamic, and structural analyses, we hypothesize that in FNiR, F420H2-derived electrons are delivered at the oxyanion reduction site at a redox potential that is suitable for reducing nitrite (E0' [standard potential], +440 mV) but not sulfite (E0', –116 mV). These findings and the known nitrite sensitivity of Mcr suggest that FNiR may protect nondenitrifying ANME from nitrite toxicity. Remarkably, by reorganizing the reductant processing system, Fsr transforms two analogous oxyanions in two distinct archaeal lineages with different physiologies and ecologies.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Aeronautics and Space Administration (NASA); Virginia Tech Agricultural Experiment Station Hatch Program; Gordon and Betty Moore Foundation
Grant/Contract Number:
SC0020373; AC05-00OR22725; NNX13AI05G; VA-160021; 9324
OSTI ID:
1874394
Alternate ID(s):
OSTI ID: 1883771
Journal Information:
Journal of Bacteriology, Journal Name: Journal of Bacteriology Vol. 204 Journal Issue: 7; ISSN 0021-9193
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

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