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Phylogenetic analysis reveals the surprising diversity of an oxygenase class

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Abstract

As metalloenzymes capable of transforming a broad range of substrates with high stereo- and regiospecificity, the multicomponent Rieske oxygenases (ROs) have been studied in bacterial systems for applications in bioremediation and industrial biocatalysis. These studies include genetic and biochemical investigations, determination of enzyme structure, phylogenetic analysis, and enzyme classification. Although RO terminal oxygenase components (RO–Os) share a conserved domain structure, their sequences are highly divergent and present significant challenges for identification and classification. Herein, we present the first global phylogenetic analysis of a broad range of RO–Os from diverse taxonomic groups. We employed objective, structure-based criteria to significantly reduce the inclusion of erroneously aligned sequences in the analysis. Our findings reveal that RO biochemical studies to date have been largely concentrated in an unexpectedly narrow portion of the RO–O sequence landscape. Additionally, our analysis demonstrates the existence two distinct groups of RO–O sequences. Finally, the sequence diversity recognized in this study necessitates a new RO–O classification scheme. We therefore propose a P450-like naming system. Our results reveal a diversity of sequence and potential catalytic functionality that has been wholly unappreciated in the RO literature. This study also demonstrates that many commonly used bioinformatic tools may not be sufficient to analyze the vast amount of data available in current databases. These findings facilitate the expanded exploration of RO catalytic capabilities in both biological and technological contexts and increase the potential for practical exploitation of their activities.

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Abbreviations

BPDORHA1 :

Biphenyl dioxygenase from Rhodococcus jostii RHA1

CDART:

Conserved Domain Architecture Retrieval Tool

CDD:

Conserved Domain Database

CMO:

Choline monooxygenase

ETC:

Electron transport chain

KshAH37Rv :

3-Ketosteroid 9α-hydroxyxlase from Mycobacterium tuberculosis H37Rv

NCBI:

National Center for Biotechnology Information

NDO9816-4 :

Naphthalene dioxygenase from Pseudomonas sp. NCIB 9816-4

P450:

Cytochrome P450

PDB:

Protein Data Bank

RO:

Rieske oxygenase

RO–O:

Rieske oxygenase terminal oxygenase component

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Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, University of British Columbia, 2350 Health Sciences Mall, Vancouver, BC, V6T 1Z3, Canada

    Jenna K. Capyk & Lindsay D. Eltis

  2. Department of Microbiology and Immunology, University of British Columbia, 2350 Health Sciences Mall, Vancouver, BC, V6T 1Z3, Canada

    Lindsay D. Eltis

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  1. Jenna K. Capyk
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Correspondence to Lindsay D. Eltis.

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Capyk, J.K., Eltis, L.D. Phylogenetic analysis reveals the surprising diversity of an oxygenase class. J Biol Inorg Chem 17, 425–436 (2012). https://doi.org/10.1007/s00775-011-0865-9

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