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Bacterial flavin-containing monooxygenase is trimethylamine monooxygenase

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Chen, Yin, Patel, Nisha A., Crombie, Andrew, Scrivens, James H. and Murrell, J. C. (J. Colin). (2011) Bacterial flavin-containing monooxygenase is trimethylamine monooxygenase. Proceedings of the National Academy of Sciences, Vol.108 (No.43). pp. 17791-17796. ISSN 0027-8424

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Official URL: http://dx.doi.org/10.1073/pnas.1112928108

Abstract

Flavin-containing monooxygenases (FMOs) are one of the most important monooxygenase systems in Eukaryotes and have many important physiological functions. FMOs have also been found in bacteria; however, their physiological function is not known. Here, we report the identification and characterization of trimethylamine (TMA) monooxygenase, termed tmm, from Methylocella silvestris, using a combination of proteomic, biochemical and genetic approaches. This bacterial FMO contains the FMO sequence motif (FXGXXXHXXXF/Y) and typical flavin adenine dinucleotide and nicotinamide adenine dinucleotide phosphate-binding domains. The enzyme was highly expressed in TMA-grown M. silvestris and absent during growth on methanol. The gene, tmm, was expressed in Escherichia coli and the purified recombinant protein had high TMA monooxygenase activity. Mutagenesis of this gene abolished the ability of M. silvestris to grow on TMA as a sole carbon and energy source. Close homologs of tmm occur in many Alphaproteobacteria, in particular Rhodobacteraceae (marine “Roseobacter” clade, MRC) and the marine SAR11 clade (Pelagibacter ubique). We showed that the ability for MRC to use TMA as sole carbon and/or nitrogen source is directly linked to the presence of tmm in their genomes and purified Tmm of MRC and SAR11 from recombinant E. coli showed TMA monooxygenase activities. The tmm gene is very abundant in the metagenomes of the Global Ocean Sampling Expedition and we estimate that 20% of the bacteria in the surface ocean contain tmm. Taken together, our results suggest that TMA monooxygenase, a bacterial FMO, plays an important, yet overlooked, role in the global carbon and nitrogen cycles.

Item Type: Journal Article
Subjects: Q Science > QR Microbiology
Divisions: Faculty of Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH): Monooxygenases -- Physiological effect, Methanotrophs -- Physiology
Journal or Publication Title: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
ISSN: 0027-8424
Date: 25 October 2011
Volume: Vol.108
Number: No.43
Page Range: pp. 17791-17796
Identification Number: 10.1073/pnas.1112928108
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Restricted or Subscription Access
Funder: Natural Environment Research Council (Great Britain) (NERC)
Grant number: NE/H016236/1 (NERC), NE/E016855/1 (NERC)
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URI: http://wrap.warwick.ac.uk/id/eprint/38876

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