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One-Component Styrene Monooxygenases: An Evolutionary View on a Rare Class of Flavoproteins

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Abstract

Styrene monooxygenases (SMOs) are catalysts for the enantioselective epoxidation of terminal alkenes. Most representatives comprise a reductase and a monooxygenase which are encoded by separate genes (styA, styB). Only six presumed self-sufficient one-component SMOs (styA2B) have previously been submitted to databases, and one has so far been characterized. StyA2B can be supported by another epoxidase (StyA1) encoded by styA1, a gene in direct neighborhood of styA2B. The present report describes the identification of a further styA1/styA2B-like SMO, which was detected in Rhodococcus opacus MR11. Based on the initially available sequences of styA2B-type SMOs, primers directed at conserved sequences were designed and a 7,012-bp genomic fragment from strain MR11 was obtained after PCRs and subsequent genome walking. Six open reading frames (ORFs) were detected and compared to genomic fragments of strains comprising either two- or one-component SMOs. Among the proteins encoded by the ORFs, the monooxygenase StyA1/StyA2B showed the highest divergence on amino acid level when comparing proteins from different sources. That finding, a rare distribution of styA2B genes among bacteria, and the general observation of evolution from simple to complex systems indicate that one-component SMOs evolved from two-component ancestors. Analysis of gene products from styA/styB- and styA1/styA2B-like SMOs revealed that a fusion of styA/styB to styA2B might have happened at least twice among microorganisms. This points to a convergent evolution of one-component SMOs.

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Acknowledgments

The work was supported by a predoctoral fellowship from the Deutsche Bundesstiftung Umwelt (DBU). We are grateful to M. Sadowsky and J. Ferguson (University of Minnesota, USA) for providing the Arthrobacter strain TC1 as well as to J. Ishikawa (National Institute of Infectious Diseases, Japan) for providing a plasmid harboring a genomic fragment of the Nocardia strain IFM 10152.

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Correspondence to Dirk Tischler.

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Dedicated to the memory of Dr. Rakesh Jain

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Tischler, D., Gröning, J.A.D., Kaschabek, S.R. et al. One-Component Styrene Monooxygenases: An Evolutionary View on a Rare Class of Flavoproteins. Appl Biochem Biotechnol 167, 931–944 (2012). https://doi.org/10.1007/s12010-012-9659-y

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