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Aromatic-ring-hydroxylating dioxygenases

Aromatic-ring-hydroxylating dioxygenases (ARHD) incorporate two atoms of dioxygen (O<sub>2</sub>) into their substrates in the dihydroxylation reaction. The product is (substituted) cis-1,2-dihydroxycyclohexadiene, which is subsequently converted to (substituted) benzene glycol by a cis-diol dehydrogenase.

A large family of multicomponent mononuclear (non-heme) iron oxygenases has been identified. Components of bacterial aromatic-ring dioxygenases constitute two different functional classes: hydroxylase components and electron transfer components. Hydroxylase components are either (αβ)<sub>n</sub> or (α)<sub>n</sub> oligomers. Two prosthetic groups, a Rieske-type [Fe<sub>2</sub>S<sub>2</sub>] center and a mononuclear iron, are associated with the α-subunit in the (αβ)<sub>n</sub>-type enzymes. Electron transfer components are composed of flavoprotein (NADH:ferredoxin oxidoreductase) and Rieske-type [Fe<sub>2</sub>S<sub>2</sub>] ferredoxin. In benzoate and toluate 1,2-dioxygenase systems, a single protein containing reductase and Rieske-type ferredoxin domains transfers the electrons from NADH to the hydroxylase component. In the phthalate 4,5-dioxygenase system, phthalate dioxygenase reductase (PDR) has the same function. PDR is a single protein comprising FMN-binding reductase and plant-type ferredoxin domains. Thus, the electron transfer in ARHD systems can be summarised as:

Biochemical classification

benzene 1,2-dioxygenase

benzene + NADH + H<sup>+</sup> + O<sub>2</sub> = cis-cyclohexa-3,5-diene-1,2-diol + NAD<sup>+</sup>

phthalate 4,5-dioxygenase

phthalate + NADH + H<sup>+</sup> + O<sub>2</sub> = cis-4,5-dihydroxycyclohexa-1(6),2-diene-1,2-dicarboxylate + NAD<sup>+</sup>

4-sulfobenzoate 3,4-dioxygenase

4-sulfobenzoate + NADH + H<sup>+</sup> + O<sub>2</sub> = 3,4-dihydroxybenzoate + sulfite + NAD<sup>+</sup>

4-chlorophenylacetate 3,4-dioxygenase

4-chlorophenylacetate + NADH + H<sup>+</sup> + O<sub>2</sub> = 3,4-dihydroxyphenylacetate + chloride + NAD<sup>+</sup>

benzoate 1,2-dioxygenase

benzoate + NADH + H<sup>+</sup> + O<sub>2</sub> = 1,2-dihydroxycyclohexa-3,5-diene-1-carboxylate + NAD<sup>+</sup>

toluene dioxygenase

toluene + NADH + H<sup>+</sup> + O<sub>2</sub> = (1S,2R)-3-methylcyclohexa-3,5-diene-1,2-diol + NAD<sup>+</sup>

naphthalene 1,2-dioxygenase

naphthalene + NADH + H<sup>+</sup> + O<sub>2</sub> = (1R,2S)-1,2-dihydronaphthalene-1,2-diol + NAD<sup>+</sup>

terephthalate 1,2-dioxygenase

terephthalate + NADH + H<sup>+</sup> + O<sub>2</sub> = (1R,6S)-dihydroxycyclohexa-2,4-diene-1,4-dicarboxylate + NAD<sup>+</sup>

biphenyl 2,3-dioxygenase

biphenyl + NADH + H<sup>+</sup> + O<sub>2</sub> = (1S,2R)-3-phenylcyclohexa-3,5-diene-1,2-diol + NAD<sup>+</sup>

Structure

The crystal structure of the hydroxylase component of naphthalene 1,2-dioxygenase from Pseudomonas has been determined. The protein is an (αβ)<sub>3</sub> hexamer. The β-subunit belongs to the α+β class. It has no prosthetic groups and its role in catalysis is unknown. The α-subunit can be divided into two domains: a Rieske domain that contains the [Fe<sub>2</sub>S<sub>2</sub>] center and the catalytic domain that contains the active site mononuclear iron. The Rieske domain (residues 38-158) consists of four β-sheets. The overall fold is very similar to that of the soluble fragment of the Rieske protein from bovine heart mitochondrial cytochrome bc<sub>1</sub> complex. In the [Fe<sub>2</sub>S<sub>2</sub>] center, Fe1 is coordinated by two cysteine residues (Cys-81 and Cys-101) while Fe2 is coordinated by N<sup>δ</sup> atoms of two histidine residues (His-83 and His-104). The catalytic domain belongs to the α+β class and is dominated by a nine-stranded antiparallel β-sheet. The iron of the active site is located at the bottom of a narrow channel, approximately 15 Å from the protein surface. The mononuclear iron is coordinated by His-208, His-213, Asp-362 (bidentate) and a water molecule. The geometry can be described as a distorted octahedral with one ligand missing. The structure of the hexamer suggests cooperativity between adjacent α-subunits, where electrons from the [Fe<sub>2</sub>S<sub>2</sub>] center in one α-subunit (A) are transferred to the mononuclear iron in the adjacent α-subunit (B) through Asp<sub>B</sub>-205, which is hydrogen-bonded to His<sub>A</sub>-104 of the Rieske center and His<sub>B</sub>-208 of the active site.

References

External links

  • - structure of naphthalene 1,2-dioxygenase from Pseudomonas putida
  • - structure of biphenyl 2,3-dioxygenase from Rhodococcus sp. strain RHA1
  • - InterPro entry for Bacterial ring hydroxylating dioxygenase, alpha subunit