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

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.

doi:10.1074/jbc.ra118.002473

Cited by 10 publications

(34 citation statements)

References 36 publications

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“…Rubredoxins are small, soluble proteins that typically contain one iron atom (although zinc, cobalt, or nickel can substitute) coordinated to four cysteinyl residues (Sieker et al, 1994). RDs are found in various (mainly archeal and bacterial) proteins, for instance flavorubredoxins, ruberythrins, nigerythrins, protein kinase G, or the essential LapB protein of Escherichia coli (Gomes et al, 2002;Iyer et al, 2005;Zhao et al, 2007;Prince and Jia, 2015;Wittwer et al, 2016;Prakash et al, 2018), and typically participate in electron transfer reactions or in redox regulation. RubA has been initially implicated in the redox control of the biogenesis of iron-sulfur (Fe-S) clusters of PSI in the cyanobacterium Synechococcus sp PCC 7002 (hereafter Synechococcus; Shen et al, 2002aShen et al, , 2002bGolbeck and Shen, 2006).…”

Section: Introductionmentioning

confidence: 99%

A Photosynthesis-Specific Rubredoxin-Like Protein Is Required for Efficient Association of the D1 and D2 Proteins during the Initial Steps of Photosystem II Assembly

et al. 2019

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Oxygenic photosynthesis relies on accessory factors to promote the assembly and maintenance of the photosynthetic apparatus in the thylakoid membranes. The highly conserved membrane-bound rubredoxin-like protein RubA has previously been implicated in the accumulation of both PSI and PSII, but its mode of action remains unclear. Here, we show that RubA in the cyanobacterium Synechocystis sp PCC 6803 is required for photoautotrophic growth in fluctuating light and acts early in PSII biogenesis by promoting the formation of the heterodimeric D1/D2 reaction center complex, the site of primary photochemistry. We find that RubA, like the accessory factor Ycf48, is a component of the initial D1 assembly module as well as larger PSII assembly intermediates and that the redox-responsive rubredoxin-like domain is located on the cytoplasmic surface of PSII complexes. Fusion of RubA to Ycf48 still permits normal PSII assembly, suggesting a spatiotemporal proximity of both proteins during their action. RubA is also important for the accumulation of PSI, but this is an indirect effect stemming from the downregulation of light-dependent chlorophyll biosynthesis induced by PSII deficiency. Overall, our data support the involvement of RubA in the redox control of PSII biogenesis.

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Section: Introductionmentioning

confidence: 99%

A Photosynthesis-Specific Rubredoxin-Like Protein Is Required for Efficient Association of the D1 and D2 Proteins during the Initial Steps of Photosystem II Assembly

et al. 2019

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“…In the domain Bacteria , glutaredoxin is reduced by glutathione and diverse low-molecular-weight thiols (Holmgren, 1989; Van Laer et al, 2013). Prevailing evidence indicates that glutathione and glutaredoxins are unlikely participants in the oxidative stress response of methanogens (McCarver et al, 2017; Prakash et al, 2018). In Methanosarcina acetivorans , the annotated glutaredoxin enzyme (AAM05066.1, renamed methanoredoxin) utilizes coenzyme M and ferredoxin:disulfide reductase (Yenugudhati et al, 2015; Prakash et al, 2018).…”

Section: Resultsmentioning

confidence: 99%

“…Prevailing evidence indicates that glutathione and glutaredoxins are unlikely participants in the oxidative stress response of methanogens (McCarver et al, 2017; Prakash et al, 2018). In Methanosarcina acetivorans , the annotated glutaredoxin enzyme (AAM05066.1, renamed methanoredoxin) utilizes coenzyme M and ferredoxin:disulfide reductase (Yenugudhati et al, 2015; Prakash et al, 2018). A glutaredoxin homolog, which is more similar to glutaredoxin from the domain Bacteria (30% identity, 71% coverage to glutaredoxin under the accession number Q9HU55.1 from Pseudomonas aeruginosa PAO1), is also present in each genome of Methanohalophilus reported here.…”

Section: Resultsmentioning

confidence: 99%

Comparative Genomics of the Genus Methanohalophilus, Including a Newly Isolated Strain From Kebrit Deep in the Red Sea

et al. 2019

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Halophilic methanogens play an important role in the carbon cycle in hypersaline environments, but are under-represented in culture collections. In this study, we describe a novel Methanohalophilus strain that was isolated from the sulfide-rich brine-seawater interface of Kebrit Deep in the Red Sea. Based on physiological and phylogenomic features, strain RSK, which is the first methanogenic archaeon to be isolated from a deep hypersaline anoxic brine lake of the Red Sea, represents a novel species of this genus. In order to compare the genetic traits underpinning the adaptations of this genus in diverse hypersaline environments, we sequenced the genome of strain RSK and compared it with genomes of previously isolated and well characterized species in this genus ( Methanohalophilus mahii , Methanohalophilus halophilus , Methanohalophilus portucalensis , and Methanohalophilus euhalobius ). These analyses revealed a highly conserved genomic core of greater than 93% of annotated genes (1490 genes) containing pathways for methylotrophic methanogenesis, osmoprotection through salt-out strategy, and oxidative stress response, among others. Despite the high degree of genomic conservation, species-specific differences in sulfur and glycogen metabolisms, viral resistance, amino acid, and peptide uptake machineries were also evident. Thus, while Methanohalophilus species are found in diverse extreme environments, each genotype also possesses adaptive traits that are likely relevant in their respective hypersaline habitats.

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“…Their respective homologs in M. acetivorans (MaTrx5 and MaTrx1) failed to display insulin disulfide reductase activity and are of unknown function [ 7 ]. Recently, a ferredoxin:disulfide reductase (FDR) has been demonstrated to reduce MaTrx5 [ 29 ]. FDRs are Fe-S enzymes present in a number of archaea and bacteria that are related to the plant-type ferredoxin:thioredoxin reductase catalytic subunit (FTRc) [ 30 ].…”

Section: Resultsmentioning

confidence: 99%

“…FDRs are Fe-S enzymes present in a number of archaea and bacteria that are related to the plant-type ferredoxin:thioredoxin reductase catalytic subunit (FTRc) [ 30 ]. Apparently, the NTR and FDR systems are both functional in Methanosarcina [ 29 , 31 , 32 ].…”

Section: Resultsmentioning

confidence: 99%

Crystal Structure of the Apo-Form of NADPH-Dependent Thioredoxin Reductase from a Methane-Producing Archaeon

et al. 2018

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The redox regulation of proteins via reversible dithiol/disulfide exchange reactions involves the thioredoxin system, which is composed of a reductant, a thioredoxin reductase (TR), and thioredoxin (Trx). In the pyridine nucleotide-dependent Trx reduction pathway, reducing equivalents, typically from reduced nicotinamide adenine dinucleotide phosphate (NADPH), are transferred from NADPH-TR (NTR) to Trx and, in turn, to target proteins, thus resulting in the reversible modification of the structural and functional properties of the targets. NTR enzymes contain three functional sites: an NADPH binding pocket, a non-covalently bound flavin cofactor, and a redox-active disulfide in the form of CxxC. With the aim of increasing our knowledge of the thioredoxin system in archaea, we here report the high-resolution crystal structure of NTR from the methane-generating organism Methanosarcina mazei strain Gö1 (MmNTR) at 2.6 Å resolution. Based on the crystals presently described, MmNTR assumes an overall fold that is nearly identical to the archetypal fold of authentic NTRs; however, surprisingly, we observed no electron density for flavin adenine dinucleotide (FAD) despite the well-defined and conserved FAD-binding cavity in the folded module. Remarkably, the dimers of the apo-protein within the crystal were different from those observed by small angle X-ray scattering (SAXS) for the holo-protein, suggesting that the binding of the flavin cofactor does not require major protein structural rearrangements. Rather, binding results in the stabilization of essential parts of the structure, such as those involved in dimer stabilization. Altogether, this structure represents the example of an apo-form of an NTR that yields important insight into the effects of the cofactor on protein folding.

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

Cited by 10 publications

References 36 publications

A Photosynthesis-Specific Rubredoxin-Like Protein Is Required for Efficient Association of the D1 and D2 Proteins during the Initial Steps of Photosystem II Assembly

A Photosynthesis-Specific Rubredoxin-Like Protein Is Required for Efficient Association of the D1 and D2 Proteins during the Initial Steps of Photosystem II Assembly

Comparative Genomics of the Genus Methanohalophilus, Including a Newly Isolated Strain From Kebrit Deep in the Red Sea

Crystal Structure of the Apo-Form of NADPH-Dependent Thioredoxin Reductase from a Methane-Producing Archaeon

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