Vanadium K-edge XAS studies on the native and peroxo-forms of vanadium chloroperoxidase from Curvularia inaequalis

Coordination Chemistry Reviews

et al. 2015

124

In the environment, vanadium-dependent haloperoxidases (VHPO) are likely to play a key role in the production of biogenic organo-halogens. These enzymes contain vanadate as a prosthetic group, and catalyze, in the presence of hydrogen peroxide, the oxidation of halide ions (Cl -, Br -or I -). They are classified according to the most electronegative halide that they can oxidize. Since the first discovery of a vanadium bromoperoxidase in the brown alga Ascophyllum nodosum thirty years ago, structural and mechanistic studies have been mainly conducted on two types of VHPO, chloro-and bromoperoxidases, and more recently on a vanadium-dependent iodoperoxidase. In this review, we highlight the main progress obtained on the structure-function relation of these proteins, based on biochemistry, crystallography and X-ray absorption spectroscopy (XAS). The comparison of 3D protein structures of the different VHPO helped identify the residues that govern the molecular mechanisms of catalysis and specificity of VHPO. Vanadium K-edge XAS gave further important insight to understand the fine changes around the vanadium cofactor during the catalytic cycle. The combination of different structural approaches, at different scales of resolution, shed new light on biological vanadium coordination in the active site, and its importance for the catalytic cycle and halide specificity of vanadium haloperoxidases. Keywords (max 6)Vanadium-dependent haloperoxidase, vanadium coordination, crystallographic structure, structural evolution, oligomeric state, X-ray absorption spectroscopy on biological vanadium

Section: Vanadium Haloperoxidase Exafsmentioning

confidence: 99%

Section: Vanadium Haloperoxidase Exafsmentioning

confidence: 99%

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Vanadium haloperoxidases: From the discovery 30 years ago to X-ray crystallographic and V K-edge absorption spectroscopic studies

Leblanc

Vilter

Coordination Chemistry Reviews

et al. 2015

124

“…The first step of the catalytic cycle is the coordination of hydrogen peroxide to vanadate, leading to the formation of a stable peroxovanadate intermediate as shown by X-ray diffraction and X-ray absorption spectroscopy (17)(18)(19). The second step, i.e., the oxidation of the halide, is the determinant for the enzymatic specificity of VHPO but has yet to be elucidated.…”

mentioning

confidence: 99%

The Vanadium Iodoperoxidase from the Marine Flavobacteriaceae Species Zobellia galactanivorans Reveals Novel Molecular and Evolutionary Features of Halide Specificity in the Vanadium Haloperoxidase Enzyme Family

Rebuffet

Delage

et al. 2014

Appl Environ Microbiol

Vanadium haloperoxidases (VHPO) are key enzymes that oxidize halides and are involved in the biosynthesis of organo-halogens. Until now, only chloroperoxidases (VCPO) and bromoperoxidases (VBPO) have been characterized structurally, mainly from eukaryotic species. Three putative VHPO genes were predicted in the genome of the flavobacterium Zobellia galactanivorans, a marine bacterium associated with macroalgae. In a phylogenetic analysis, these putative bacterial VHPO were closely related to other VHPO from diverse bacterial phyla but clustered independently from eukaryotic algal VBPO and fungal VCPO. Two of these bacterial VHPO, heterogeneously produced in Escherichia coli, were found to be strictly specific for iodide oxidation. The crystal structure of one of these vanadium-dependent iodoperoxidases, Zg-VIPO1, was solved by multiwavelength anomalous diffraction at 1.8 Å, revealing a monomeric structure mainly folded into ␣-helices. This three-dimensional structure is relatively similar to those of VCPO of the fungus Curvularia inaequalis and of Streptomyces sp. and is superimposable onto the dimeric structure of algal VBPO. Surprisingly, the vanadate binding site of Zg-VIPO1 is strictly conserved with the fungal VCPO active site. Using site-directed mutagenesis, we showed that specific amino acids and the associated hydrogen bonding network around the vanadate center are essential for the catalytic properties and also the iodide specificity of Zg-VIPO1. Altogether, phylogeny and structure-function data support the finding that iodoperoxidase activities evolved independently in bacterial and algal lineages, and this sheds light on the evolution of the VHPO enzyme family. H alogenated compounds have various biological functions in nature, ranging from chemical defense to signaling. Indeed, halogenation (i.e., iodination, bromination, or chlorination) is an efficient strategy used to increase the biological activity of secondary metabolites and involves many different halogenating enzymes (1-4). Among them, vanadium-dependent haloperoxidases (VHPO) contain the bare metal oxide vanadate as a prosthetic group. In the presence of hydrogen peroxide, VHPO enzymes catalyze the oxidation of halides according to the reaction H 2 O 2 ϩ X Ϫ ϩ H ϩ ¡ H 2 O ϩ HOX, wherein X Ϫ represents a halide ion and may be Cl Ϫ , Br Ϫ , or I Ϫ (4). A variety of halocarbons can subsequently be generated if the appropriate nucleophilic acceptors are present. The nomenclature of vanadium-dependent haloperoxidases is based on the most electronegative halide they can oxidize: chloroperoxidases (VCPO) can catalyze the oxidation of three different halides, i.e., chloride, bromide and iodide; bromoperoxidases (VBPO) can oxidize only bromide and iodide; and iodoperoxidases (VIPO) are specific for iodide.The first VBPO was discovered 30 years ago, in the brown alga Ascophyllum nodosum (5). Since then, structural and mechanistic studies have focused on two types of eukaryotic VHPO, namely, VCPO from the pathogenic fungus Curvularia inaequalis (6) a...

“…During the catalytic cycle, the vanadate group reacts with the strong oxidant, hydrogen peroxide, and forms a peroxovanadate intermediate with the creation of an OÀ ÀO bond between an equatorial oxygen-hydrogen bond to lysine residues (O2) and the apical oxygen (O4) (Renirie et al, 2010) (Figure 10.7b). According to previous 17 O NMR studies (Casn y et al, 2000), H 2 O 2 binds to VO 4 in the "side-on" (g 2 ) mode.…”

Section: Fine Structure and Vanadate Coordination Into The Active Sitementioning

confidence: 99%

Halogenation and Vanadium Haloperoxidases

Outstanding Marine Molecules

Leblanc

2014

In marine organisms, vanadium haloperoxidases (VHPO) are involved in the production of halogenated metabolites, which feature a large panel of biological roles, such as signal molecules or antibiotics. VHPO-based halogenation processes are likely to play a role in the biogeochemical cycling of halogens because of the formation of volatile halocarbons, especially in marine coastal environments where large seaweed beds dominate. At the biochemical level, these enzymes present different specificities, and are classified according to the most electronegative halide that they can oxidize. In this chapter, a review is provided of all data obtained from biochemical, molecular characterization and structural studies on these haloperoxidases, since their discovery in a marine brown alga 30 years ago.