Structure of the Dissimilatory Sulfite Reductase from the Hyperthermophilic Archaeon Archaeoglobus fulgidus

Schiffer, Alexander; Parey, Kristian; Warkentin, Eberhard; Diederichs, Kay; Huber, Harald; Stetter, Karl O.; Kroneck, Peter M. H.

doi:10.1016/j.jmb.2008.04.027

Cited by 77 publications

(105 citation statements)

References 62 publications

(59 reference statements)

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“…To the best of our knowledge, this is the first time a covalent link is observed involving a heme meso carbon and a cysteine residue. The A. fulgidus dSiR, which was purified anaerobically, does not include DsrC (31). We recently obtained crystals from anaerobically purified Dvir, which still showed the presence of the cross-link.…”

Section: Discussionmentioning

confidence: 99%

“…In the A. fulgidus dSiR, the substrate binding site of the DsrA siroheme is also blocked by a tryptophan residue that is sitting right above the iron. In addition, there is an extended loop that blocks access to this heme, which was proposed to have a structural role (31). This loop is absent from Dvir, but in its place, there is an extended loop from the DsrA ferredoxin domain (Gly-257A to Asp-275A) that also shields access to the sirohydrochlorin.…”

Section: The Crystal Structure Of D Vulgaris Dsir Bound To Dsrcmentioning

confidence: 99%

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The Crystal Structure of Desulfovibrio vulgaris Dissimilatory Sulfite Reductase Bound to DsrC Provides Novel Insights into the Mechanism of Sulfate Respiration

Oliveira

Vonrhein

Matías

et al. 2008

Journal of Biological Chemistry

159

226

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Sulfate reduction is one of the earliest types of energy metabolism used by ancestral organisms to sustain life. Despite extensive studies, many questions remain about the way respiratory sulfate reduction is associated with energy conservation. A crucial enzyme in this process is the dissimilatory sulfite reductase (dSiR), which contains a unique siroheme-[4Fe4S] coupled cofactor. Here, we report the structure of desulfoviridin from Desulfovibrio vulgaris, in which the dSiR DsrAB (sulfite reductase) subunits are bound to the DsrC protein. with its conserved C-terminal cysteine reaching the distal side of the siroheme. We propose a novel mechanism for the process of sulfite reduction involving DsrAB, DsrC, and the DsrMKJOP membrane complex (a membrane complex with putative disulfide/thiol reductase activity), in which two of the six electrons for reduction of sulfite derive from the membrane quinone pool. These results show that DsrC is involved in sulfite reduction, which changes the mechanism of sulfate respiration. This has important implications for models used to date ancient sulfur metabolism based on sulfur isotope fractionations.The dissimilatory reduction of sulfur compounds is one of the earliest energy metabolisms detected on earth, at ϳ3.5 billion years ago (1, 2). At the end of the Archean (ϳ2.7 billion years ago), the advent of oxygenic photosynthesis led to a gradual increase in the levels of atmospheric oxygen, which in turn caused an increasing flux of sulfate to the oceans from weathering of sulfide minerals on land (3). As a consequence of this process, reduction of sulfate became a dominant biological process in the oceans, resulting in sulfidic anoxic conditions from about 2.5 to 0.6 billion years ago (3, 4). During this extended period, sulfate-reducing prokaryotes were main players in marine habitats where most evolutionary processes were taking place. Today, these organisms are still major contributors to the biological carbon and sulfur cycles, and their activities have important environmental and economic consequences.A key enzyme in sulfur-based energy metabolism is the dissimilatory sulfite reductase (dSiR), 3 which is present in organisms that reduce sulfate, sulfite, and other sulfur compounds. This enzyme is also found in some phototrophic and chemotrophic sulfur oxidizers, where it is proposed to operate in the reverse direction (reverse sulfite reductase, rSiR). The dSiR is minimally composed of two subunits, DsrA and DsrB, in an ϳ200-kDa ␣ 2 ␤ 2 arrangement. The dsrA and dsrB genes are paralogous and most likely arose from a very early gene duplication event that preceded the separation of the archaea and bacteria domains (5-8), in agreement with a very early onset of biological sulfite reduction. The dSiR belongs to a family of proteins that also include the assimilatory sulfite (aSiR) and nitrite (aNiR) reductases, the monomeric low molecular mass aSiRs, and other dSiRs like asrC and Fsr (9 -11). This family has in common a characteristic cofactor assembly that includes an iro...

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Section: Discussionmentioning

confidence: 99%

Section: The Crystal Structure Of D Vulgaris Dsir Bound To Dsrcmentioning

confidence: 99%

The Crystal Structure of Desulfovibrio vulgaris Dissimilatory Sulfite Reductase Bound to DsrC Provides Novel Insights into the Mechanism of Sulfate Respiration

Oliveira

Vonrhein

Matías

et al. 2008

Journal of Biological Chemistry

159

226

View full text Add to dashboard Cite

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“…Both have similar conformations but are less distorted than the cofactor on the assimilatory sulphite reductase from E. coli. 145 Similarly, non-planar macrocycles have also been implied in nitrite reductases. For example, the structure of oxidized cyt cd 1 (nitrite reductase) from Thiosphaera pantotropha showed a covalently bound, hexacoordinated (HIS, HIS) type c cytochrome and a planar, hexacoordinated (TYR, HIS) heme d 1 .…”

Section: Heme D 1 and Sirohemementioning

confidence: 99%

Conformational control of cofactors in nature – the influence of protein-induced macrocycle distortion on the biological function of tetrapyrroles

2015

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Tetrapyrrole-containing proteins are one of the most fundamental classes of enzymes in nature and it remains an open question to give a chemical rationale for the multitude of biological reactions that can be catalyzed by these pigmentprotein complexes. There are many fundamental processes where the same (i.e., chemically identical) porphyrin cofactor is involved in chemically quite distinct reactions. For example, heme is the active cofactor for oxygen transport and storage (hemoglobin, myoglobin) and for the incorporation of molecular oxygen in organic substrates (cytochrome P 450 ). It is involved in the terminal oxidation (cytochrome c oxidase) and the metabolism of H 2 O 2 (catalases and peroxidases) and catalyzes various electron transfer reactions in cytochromes. Likewise, in photosynthesis the same chlorophyll cofactor may function as a reaction center pigment (charge separation) or as an accessory pigment (exciton transfer) in light harvesting complexes (e.g., chlorophyll a). Whilst differences in the apoprotein sequences alone cannot explain the often drastic differences in physicochemical properties encountered for the same cofactor in diverse protein complexes, a critical factor for all biological functions must be the close structural interplay between bound cofactors and the respective apoprotein in addition to factors such as hydrogen bonding or electronic effects. Here, we explore how nature can use the same chemical molecule as a cofactor for chemically distinct reactions using the concept of conformational flexibility of tetrapyrroles. The multifaceted roles of tetrapyrroles are discussed in the context of the current knowledge on distorted porphyrins. Contemporary analytical methods now allow a more quantitative look at cofactors in protein complexes and the development of the field is illustrated by case studies on hemeproteins and photosynthetic complexes. Specific tetrapyrrole conformations are now used to prepare bioengineered designer proteins with specific catalytic or photochemical properties.

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“…22 To investigate the role of Met175 as the main affinity-regulating residue in the aNiRs, we determined the crystal structures of three Nii3-M175 variants (Nii3-M175G, Nii3-M175E, and Nii3-M175K).…”

Section: Geometries Of the Siroheme And The [4fe-4s] Cluster Of Nii3-wtmentioning

confidence: 99%

“…In this study, we determined the crystal structures of tobacco aNiRs from leaf (Nii3) and root (Nii4). 18 The Nii3 structure was determined to a higher resolution than the previously solved aNiR, assimilatory sulfite reductase (aSiR) and dissimilatory sulfite reductase (dSiR) structures, 15,[19][20][21][22][23][24][25] and therefore precise geometries for the [4Fe-4S] cluster and siroheme could be determined. In addition, based on the detailed structures and on kinetic parameters, comparisons among wild-type Nii3 (Nii3-WT), Nii4-WT, and their variants (Nii3-M175G, Nii3-M175E, Nii3-M175K, Nii3-Q448K, and Nii4-K449Q) showed that the hydrophobicity of the Met175 side-chain was important for the efficient activity of aNiR and revealed that Gln448 of Nii3 and Lys449 of Nii4 play a role in enzyme efficiency (k cat / K m ).…”

Section: Introductionmentioning

confidence: 99%

Structure–function relationship of assimilatory nitrite reductases from the leaf and root of tobacco based on high‐resolution structures

et al. 2012

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Tobacco expresses four isomers of assimilatory nitrite reductase (aNiR), leaf-type (Nii1 and Nii3), and root-type (Nii2 and Nii4). The high-resolution crystal structures of Nii3 and Nii4, determined at 1.25 and 2.3 Å resolutions, respectively, revealed that both proteins had very similar structures. The Nii3 structure provided detailed geometries for the [4Fe-4S] cluster and the siroheme prosthetic groups. We have generated two types of Nii3 variants: one set focuses on residue Met175 (Nii3-M175G, Nii3-M175E, and Nii3-M175K), a residue that is located on the substrate entrance pathway; the second set targets residue Gln448 (Nii3-Q448K), a residue near the prosthetic groups. Comparison of the structures and kinetics of the Nii3 wild-type (Nii3-WT) and the Met175 variants showed that the hydrophobic side-chain of Met175 facilitated enzyme efficiency (k cat /K m ). The Nii4-WT has Lys449 at the equivalent position of Gln448 in Nii3-WT. The enzyme activity assay revealed that the turnover number (k cat ) and Michaelis constant (K m ) of Nii4-WT were lower than those of Nii3-WT. However, the k cat /K m of Nii4-WT was about 1.4 times higher than that of Nii3-WT. A comparison of the kinetics of the Nii3-Q448K and Nii4-K449Q variants revealed that the change in k cat /K m was brought about by the difference in Residue 448 (defined as Gln448 in Nii3 and Lys449 in Nii4). By combining detailed crystal structures with enzyme kinetics, we have proposed that Nii3 is the low-affinity and Nii4 is the high-affinity aNiR.

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Structure of the Dissimilatory Sulfite Reductase from the Hyperthermophilic Archaeon Archaeoglobus fulgidus

Cited by 77 publications

References 62 publications

The Crystal Structure of Desulfovibrio vulgaris Dissimilatory Sulfite Reductase Bound to DsrC Provides Novel Insights into the Mechanism of Sulfate Respiration

The Crystal Structure of Desulfovibrio vulgaris Dissimilatory Sulfite Reductase Bound to DsrC Provides Novel Insights into the Mechanism of Sulfate Respiration

Conformational control of cofactors in nature – the influence of protein-induced macrocycle distortion on the biological function of tetrapyrroles

Structure–function relationship of assimilatory nitrite reductases from the leaf and root of tobacco based on high‐resolution structures

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