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Turning points in the evolution of peroxidase-catalase superfamily: molecular phylogeny of hybrid heme peroxidases.

Zámocký M, Gasselhuber B, Furtmüller PG, Obinger C - Cell. Mol. Life Sci. (2014)

Bottom Line: In some ascomycetous hybrid-type B peroxidases, the peroxidase domain is fused to a carbohydrate binding (WSC) domain.Both here described hybrid-type peroxidase families represent important turning points in the complex evolution of the whole peroxidase-catalase superfamily.We present and discuss their phylogeny, sequence signatures and putative biological function.

View Article: PubMed Central - PubMed

Affiliation: Division of Biochemistry, Department of Chemistry, VIBT, Vienna Institute of BioTechnology, BOKU, University of Natural Resources and Life Sciences, Muthgasse 18, 1190, Vienna, Austria, marcel.zamocky@boku.ac.at.

ABSTRACT
Heme peroxidases and catalases are key enzymes of hydrogen peroxide metabolism and signaling. Here, the reconstruction of the molecular evolution of the peroxidase-catalase superfamily (annotated in pfam as PF00141) based on experimentally verified as well as numerous newly available genomic sequences is presented. The robust phylogenetic tree of this large enzyme superfamily was obtained from 490 full-length protein sequences. Besides already well-known families of heme b peroxidases arranged in three main structural classes, completely new (hybrid type) peroxidase families are described being located at the border of these classes as well as forming (so far missing) links between them. Hybrid-type A peroxidases represent a minor eukaryotic subfamily from Excavates, Stramenopiles and Rhizaria sharing enzymatic and structural features of ascorbate and cytochrome c peroxidases. Hybrid-type B peroxidases are shown to be spread exclusively among various fungi and evolved in parallel with peroxidases in land plants. In some ascomycetous hybrid-type B peroxidases, the peroxidase domain is fused to a carbohydrate binding (WSC) domain. Both here described hybrid-type peroxidase families represent important turning points in the complex evolution of the whole peroxidase-catalase superfamily. We present and discuss their phylogeny, sequence signatures and putative biological function.

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Selected parts of structural multiple sequence alignment of 48 members of the peroxidase–catalase superfamily. This alignment demonstrates both high conservation of the active site residues as well as some variability. a Region including residues at the distal heme side, b region of the large loop, c region including residues at the proximal heme side. Secondary structural elements taken from the 3D structure of KatG from Burkholderia pseudomallei (BpKatG, PDB code 1MWV) are depicted (h helix, e strand, t turn). Essential residues involved in catalysis are labeled as “*” and those residues that were involved in catalysis but later during the evolution mutated as “.” residues discussed in the text are labeled with arrows. Sequences with known 3D structures are in bold. Parameters for the alignment are described in the Sect. “Materials and methods”. Abbreviations of peroxidase names are taken from PeroxiBase
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Fig5: Selected parts of structural multiple sequence alignment of 48 members of the peroxidase–catalase superfamily. This alignment demonstrates both high conservation of the active site residues as well as some variability. a Region including residues at the distal heme side, b region of the large loop, c region including residues at the proximal heme side. Secondary structural elements taken from the 3D structure of KatG from Burkholderia pseudomallei (BpKatG, PDB code 1MWV) are depicted (h helix, e strand, t turn). Essential residues involved in catalysis are labeled as “*” and those residues that were involved in catalysis but later during the evolution mutated as “.” residues discussed in the text are labeled with arrows. Sequences with known 3D structures are in bold. Parameters for the alignment are described in the Sect. “Materials and methods”. Abbreviations of peroxidase names are taken from PeroxiBase

Mentions: The multiple structural sequence alignment depicted in Fig. 5 suggests that the bifunctional activity of KatGs [5] has been lost stepwise. This can be exemplified by inspection of two representative hybrid-type A peroxidases, namely EgrAPx-CcP and LmAPx-CcP (Fig. 5). The (pseudo-) catalase activity of KatGs is based on the presence of a redox active cofactor, a post-translationally formed Trp-Tyr-Met adduct in close proximity to the heme group (BpKatG numbering: Trp111-Tyr238-Met264, Fig. 3a) [33]. Tyrosine 238, which is essential for the H2O2-degrading activity of KatG [34, 35], is located on the KatG-typical large loop LL1 that also contributes to the architecture of the substrate channel [5]. Both hybrid-type A peroxidases, EgrAPx-CcP and LmApx-CcP, have lost this large loop including Tyr238 (Fig. 5b) as well as the C-terminal part of large loop LL2 (Fig. 5c). Thus, they are not able to form the covalent adduct [10]. In LmAPx-CcP Met264 is substituted by a leucine, whereas in all hybrid-type A peroxidases Trp111 is fully conserved together with the catalytic residues His112 and Arg108 (BpKatG numbering Fig. 5). The histidine–arginine pair is found in all (mono) functional peroxidases of the catalase–peroxidase superfamily and is important for the heterolytic cleavage of H2O2 in compound I formation [36]. The proximal heme architecture including the triad His279––Asp389––Trp330 (and the H-bonding network between these residues) of hybrid-type A peroxidases is still very similar to that of KatGs [37].Fig. 5


Turning points in the evolution of peroxidase-catalase superfamily: molecular phylogeny of hybrid heme peroxidases.

Zámocký M, Gasselhuber B, Furtmüller PG, Obinger C - Cell. Mol. Life Sci. (2014)

Selected parts of structural multiple sequence alignment of 48 members of the peroxidase–catalase superfamily. This alignment demonstrates both high conservation of the active site residues as well as some variability. a Region including residues at the distal heme side, b region of the large loop, c region including residues at the proximal heme side. Secondary structural elements taken from the 3D structure of KatG from Burkholderia pseudomallei (BpKatG, PDB code 1MWV) are depicted (h helix, e strand, t turn). Essential residues involved in catalysis are labeled as “*” and those residues that were involved in catalysis but later during the evolution mutated as “.” residues discussed in the text are labeled with arrows. Sequences with known 3D structures are in bold. Parameters for the alignment are described in the Sect. “Materials and methods”. Abbreviations of peroxidase names are taken from PeroxiBase
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4232752&req=5

Fig5: Selected parts of structural multiple sequence alignment of 48 members of the peroxidase–catalase superfamily. This alignment demonstrates both high conservation of the active site residues as well as some variability. a Region including residues at the distal heme side, b region of the large loop, c region including residues at the proximal heme side. Secondary structural elements taken from the 3D structure of KatG from Burkholderia pseudomallei (BpKatG, PDB code 1MWV) are depicted (h helix, e strand, t turn). Essential residues involved in catalysis are labeled as “*” and those residues that were involved in catalysis but later during the evolution mutated as “.” residues discussed in the text are labeled with arrows. Sequences with known 3D structures are in bold. Parameters for the alignment are described in the Sect. “Materials and methods”. Abbreviations of peroxidase names are taken from PeroxiBase
Mentions: The multiple structural sequence alignment depicted in Fig. 5 suggests that the bifunctional activity of KatGs [5] has been lost stepwise. This can be exemplified by inspection of two representative hybrid-type A peroxidases, namely EgrAPx-CcP and LmAPx-CcP (Fig. 5). The (pseudo-) catalase activity of KatGs is based on the presence of a redox active cofactor, a post-translationally formed Trp-Tyr-Met adduct in close proximity to the heme group (BpKatG numbering: Trp111-Tyr238-Met264, Fig. 3a) [33]. Tyrosine 238, which is essential for the H2O2-degrading activity of KatG [34, 35], is located on the KatG-typical large loop LL1 that also contributes to the architecture of the substrate channel [5]. Both hybrid-type A peroxidases, EgrAPx-CcP and LmApx-CcP, have lost this large loop including Tyr238 (Fig. 5b) as well as the C-terminal part of large loop LL2 (Fig. 5c). Thus, they are not able to form the covalent adduct [10]. In LmAPx-CcP Met264 is substituted by a leucine, whereas in all hybrid-type A peroxidases Trp111 is fully conserved together with the catalytic residues His112 and Arg108 (BpKatG numbering Fig. 5). The histidine–arginine pair is found in all (mono) functional peroxidases of the catalase–peroxidase superfamily and is important for the heterolytic cleavage of H2O2 in compound I formation [36]. The proximal heme architecture including the triad His279––Asp389––Trp330 (and the H-bonding network between these residues) of hybrid-type A peroxidases is still very similar to that of KatGs [37].Fig. 5

Bottom Line: In some ascomycetous hybrid-type B peroxidases, the peroxidase domain is fused to a carbohydrate binding (WSC) domain.Both here described hybrid-type peroxidase families represent important turning points in the complex evolution of the whole peroxidase-catalase superfamily.We present and discuss their phylogeny, sequence signatures and putative biological function.

View Article: PubMed Central - PubMed

Affiliation: Division of Biochemistry, Department of Chemistry, VIBT, Vienna Institute of BioTechnology, BOKU, University of Natural Resources and Life Sciences, Muthgasse 18, 1190, Vienna, Austria, marcel.zamocky@boku.ac.at.

ABSTRACT
Heme peroxidases and catalases are key enzymes of hydrogen peroxide metabolism and signaling. Here, the reconstruction of the molecular evolution of the peroxidase-catalase superfamily (annotated in pfam as PF00141) based on experimentally verified as well as numerous newly available genomic sequences is presented. The robust phylogenetic tree of this large enzyme superfamily was obtained from 490 full-length protein sequences. Besides already well-known families of heme b peroxidases arranged in three main structural classes, completely new (hybrid type) peroxidase families are described being located at the border of these classes as well as forming (so far missing) links between them. Hybrid-type A peroxidases represent a minor eukaryotic subfamily from Excavates, Stramenopiles and Rhizaria sharing enzymatic and structural features of ascorbate and cytochrome c peroxidases. Hybrid-type B peroxidases are shown to be spread exclusively among various fungi and evolved in parallel with peroxidases in land plants. In some ascomycetous hybrid-type B peroxidases, the peroxidase domain is fused to a carbohydrate binding (WSC) domain. Both here described hybrid-type peroxidase families represent important turning points in the complex evolution of the whole peroxidase-catalase superfamily. We present and discuss their phylogeny, sequence signatures and putative biological function.

Show MeSH
Related in: MedlinePlus