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The two-component flavin-dependent monooxygenases belong to an emerging classof enzymes involved in oxidation reactions in a number of metabolic andbiosynthetic pathways in microorganisms. One component is a NAD(P)H:flavinoxidoreductase, which provides a reduced flavin to the second component, theproper monooxygenase. There, the reduced flavin activates molecular oxygen forsubstrate oxidation. Here, we study the flavin reductase ActVB and ActVA-ORF5gene product, both reported to be involved in the last step of biosynthesis ofthe natural antibiotic actinorhodin in Streptomyces coelicolor. For the firsttime we show that ActVA-ORF5 is a FMN-dependent monooxygenase that togetherwith the help of the flavin reductase ActVB catalyzes the oxidation reaction.The mechanism of the transfer of reduced FMN between ActVB and ActVA-ORF5 hasbeen investigated. Dissociation constant values for oxidized and reduced flavin(FMNox and FMNred) with regard to ActVB and ActVA-ORF5 have been determined.The data clearly demonstrate a thermodynamic transfer of FMNred from ActVB toActVA-ORF5 without involving a particular interaction between the two proteincomponents. In full agreement with these data, we propose a reaction mechanismin which FMNox binds to ActVB, where it is reduced, and the resulting FMNredmoves to ActVA-ORF5, where it reacts with O2 to generate a flavinperoxideintermediate. A direct spectroscopic evidence for the formation of such specieswithin ActVA-ORF5 is reported.

A two-component flavin-dependent monooxygenase involved in actinorhodin biosynthesis in Streptomyces coelicolor