Novel Acetone Metabolism in a Propane-utilizing Bacterium, Gordonia Sp. Strain TY-5

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 2006 Oct 31

PMID 17071761

Citations 36

Authors

Tetsuya Kotani

Hiroya Yurimoto

Nobuo Kato

Yasuyoshi Sakai

Affiliations

Soon will be listed here.

Abstract

In the propane-utilizing bacterium Gordonia sp. strain TY-5, propane was shown to be oxidized to 2-propanol and then further oxidized to acetone. In this study, the subsequent metabolism of acetone was studied. Acetone-induced proteins were found in extracts of cells induced by acetone, and a gene cluster designated acmAB was cloned on the basis of the N-terminal amino acid sequences of acetone-induced proteins. The acmA and acmB genes encode a Baeyer-Villiger monooxygenase (BVMO) and esterase, respectively. The BVMO encoded by acmA was purified from acetone-induced cells of Gordonia sp. strain TY-5 and characterized. The BVMO exhibited NADPH-dependent oxidation activity for linear ketones (C3 to C10) and cyclic ketones (C4 to C8). Escherichia coli expressing the acmA gene oxidized acetone to methyl acetate, and E. coli expressing the acmB gene hydrolyzed methyl acetate. Northern blot analyses revealed that polycistronic transcription of the acmAB gene cluster was induced by propane, 2-propanol, and acetone. These results indicate that the acmAB gene products play an important role in the metabolism of acetone derived from propane oxidation and clarify the propane metabolism pathway of strain TY-5 (propane --> 2-propanol --> acetone --> methyl acetate --> acetic acid + methanol). This paper provides the first evidence for BVMO-dependent acetone metabolism.

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References

Eppink M, Schreuder H, van Berkel W . Identification of a novel conserved sequence motif in flavoprotein hydroxylases with a putative dual function in FAD/NAD(P)H binding. Protein Sci. 1998; 6(11):2454-8. PMC: 2143585. DOI: 10.1002/pro.5560061119. View

Trower M, Buckland R, Griffin M . Characterization of an FMN-containing cyclohexanone monooxygenase from a cyclohexane-grown Xanthobacter sp. Eur J Biochem. 1989; 181(1):199-206. DOI: 10.1111/j.1432-1033.1989.tb14711.x. View

Allen J, Forney F, Markovetz A . Microbial subterminal oxidation of alkanes and alk-1-enes. Lipids. 1971; 6(7):448-52. DOI: 10.1007/BF02531227. View

Willetts A . Structural studies and synthetic applications of Baeyer-Villiger monooxygenases. Trends Biotechnol. 1997; 15(2):55-62. DOI: 10.1016/S0167-7799(97)84204-7. View

Watkinson R, Morgan P . Physiology of aliphatic hydrocarbon-degrading microorganisms. Biodegradation. 1990; 1(2-3):79-92. DOI: 10.1007/BF00058828. View

Kotani T, Yamamoto T, Yurimoto H, Sakai Y, Kato N . Propane monooxygenase and NAD+-dependent secondary alcohol dehydrogenase in propane metabolism by Gordonia sp. strain TY-5. J Bacteriol. 2003; 185(24):7120-8. PMC: 296251. DOI: 10.1128/JB.185.24.7120-7128.2003. View

Lukins H, FOSTER J . METHYL KETONE METABOLISM IN HYDROCARBON-UTILIZING MYCOBACTERIA. J Bacteriol. 1963; 85:1074-87. PMC: 278287. DOI: 10.1128/jb.85.5.1074-1087.1963. View

Morii S, Sawamoto S, Yamauchi Y, Miyamoto M, Iwami M, ITAGAKI E . Steroid monooxygenase of Rhodococcus rhodochrous: sequencing of the genomic DNA, and hyperexpression, purification, and characterization of the recombinant enzyme. J Biochem. 1999; 126(3):624-31. DOI: 10.1093/oxfordjournals.jbchem.a022494. View

Donoghue N, Norris D, Trudgill P . The purification and properties of cyclohexanone oxygenase from Nocardia globerula CL1 and Acinetobacter NCIB 9871. Eur J Biochem. 1976; 63(1):175-92. DOI: 10.1111/j.1432-1033.1976.tb10220.x. View

10.

Britton L, Markovetz A . A novel ketone monooxygenase from Pseudomonas cepacia. Purification and properties. J Biol Chem. 1977; 252(23):8561-6. View

11.

Brzostowicz P, Walters D, Jackson R, Halsey K, Ni H, Rouviere P . Proposed involvement of a soluble methane monooxygenase homologue in the cyclohexane-dependent growth of a new Brachymonas species. Environ Microbiol. 2005; 7(2):179-90. DOI: 10.1111/j.1462-2920.2004.00681.x. View

12.

Sakai Y, Ishikawa J, Fukasaka S, Yurimoto H, Mitsui R, Yanase H . A new carboxylesterase from Brevibacterium linens IFO 12171 responsible for the conversion of 1,4-butanediol diacrylate to 4-hydroxybutyl acrylate: purification, characterization, gene cloning, and gene expression in Escherichia coli. Biosci Biotechnol Biochem. 1999; 63(4):688-97. DOI: 10.1271/bbb.63.688. View

13.

Hasegawa Y, Nakai Y, Tokuyama T, Iwaki H . Purification and characterization of cyclohexanone 1,2-monooxygenase from Exophiala jeanselmei strain KUFI-6N. Biosci Biotechnol Biochem. 2001; 64(12):2696-8. DOI: 10.1271/bbb.64.2696. View

14.

Molinas S, Altabe S, Opperdoes F, Rider M, Michels P, Uttaro A . The multifunctional isopropyl alcohol dehydrogenase of Phytomonas sp. could be the result of a horizontal gene transfer from a bacterium to the trypanosomatid lineage. J Biol Chem. 2003; 278(38):36169-75. DOI: 10.1074/jbc.M305666200. View

15.

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

16.

Clark D, Ensign S . Evidence for an inducible nucleotide-dependent acetone carboxylase in Rhodococcus rhodochrous B276. J Bacteriol. 1999; 181(9):2752-8. PMC: 93715. DOI: 10.1128/JB.181.9.2752-2758.1999. View

17.

Vestal J, Perry J . Divergent metabolic pathways for propane and propionate utilization by a soil isolate. J Bacteriol. 1969; 99(1):216-21. PMC: 249990. DOI: 10.1128/jb.99.1.216-221.1969. View

18.

Sluis M, Ensign S . Purification and characterization of acetone carboxylase from Xanthobacter strain Py2. Proc Natl Acad Sci U S A. 1997; 94(16):8456-61. PMC: 22955. DOI: 10.1073/pnas.94.16.8456. View

19.

Bondoc F, Bao Z, Hu W, Gonzalez F, Wang Y, Yang C . Acetone catabolism by cytochrome P450 2E1: studies with CYP2E1-null mice. Biochem Pharmacol. 1999; 58(3):461-3. DOI: 10.1016/s0006-2952(99)00111-2. View

20.

Bradford M . A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72:248-54. DOI: 10.1016/0003-2697(76)90527-3. View