Identification and characterization of trimethylamine N-oxide (TMAO) demethylase and TMAO permease in Methylocella silvestris BL2

Environmental Microbiology

Volumn 16, Issue 10, 2014, Pages 3318-3330

  Zhu, Yijun ^a   Jameson, Eleanor ^a   Parslow, Rosemary A ^b   Lidbury, Ian ^a   Fu, Tiantian ^a   Dafforn, Timothy R ^b   Schäfer, Hendrik ^a   Chen, Yin ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

METHYLOCELLA SILVESTRIS;

CARRIER PROTEIN; LYASE; METHYLAMINE; TRIMETHYLAMINE-OXIDE ALDOLASE; TRIMETHYLOXAMINE;

ALPHAPROTEOBACTERIA; BACTERIAL GENE; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTAGENESIS; PHYSIOLOGY;

ALDEHYDE-LYASES; ALPHAPROTEOBACTERIA; ESCHERICHIA COLI; GENES, BACTERIAL; MEMBRANE TRANSPORT PROTEINS; METHYLAMINES; MUTAGENESIS;

EID: 84907817507     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12585     Document Type: Article

References (47)

1. Alberta, J.A., and Dawson, J.H. (1987) Purification to homogeneity and initial physical characterization of secondary amine monooxygenase. J Biol Chem 262: 11857-11863.
2. Anthony, C. (1982) The Biochemistry of Methylotrophs. London, UK: Academic Press.
3. Barrett, E.L., and Kwan, H.S. (1985) Bacterial reduction of trimethylamine oxide. Annu Rev Microbiol 39: 131-149.
4. Bhadbhade, B.J., Sarnaik, S.S., and Kanekar, P.P. (2002) Biomineralization of an organophosphorus pesticide, Monocrotophos, by soil bacteria. J Appl Microbiol 93: 224-234.
5. Cape, J.N., Cornell, S.E., Jickells, T.D., and Nemitz, E. (2011) Organic nitrogen in the atmosphere - where does it come from? A review of sources and methods. Atmos Res 102: 30-48.
6. Chen, Y., Crombie, A., Rahman, M.T., Dedysh, S.N., Liesack, W., Stott, M.B., etal. (2010a) Complete genome sequence of the aerobic facultative methanotroph Methylocella silvestris BL2. J Bacteriol 192: 3840-3841.
7. Chen, Y., Scanlan, J., Song, L., Crombie, A., Rahman, M.T., Schäfer, H., etal. (2010b) {gamma}-Glutamylmethylamide is an essential intermediate in the metabolism of methylamine by Methylocella silvestris. Appl Environ Microbiol 76: 4530-4537.
8. Chen, Y., Patel, N.A., Crombie, A., Scrivens, J.H., and Murrell, J.C. (2011) Bacterial flavin-containing monooxygenase is trimethylamine monooxygenase. Proc Natl Acad Sci USA 108: 17791-17796.
9. Dam, J., Velikovsky, C.A., Mariuzza, R.A., Urbanke, C., and Schuck, P. (2005) Sedimentation velocity analysis of heterogeneous protein-protein interactions: Lamm equation modeling and sedimentation coefficient distributions c(s). Biophys J 89: 619-634.
10. Dunfield, P.F., Khmelenina, V.N., Suzina, N.E., Trotsenko, Y.A., and Dedysh, S.N. (2003) Methylocella silvestris sp. nov., a novel methanotroph isolated from an acidic forest cambisol. Int J Syst Evol Microbiol 53: 1231-1239.
11. Fu, X.Y., Xue, C.H., Miao, B.C., Liang, J.N., Li, Z.J., and Cui, F.X. (2006) Purification and characterization of trimethylamine-N-oxide demethylase from jumbo squid (Dosidicus gigas). J Agric Food Chem 54: 968-972.
12. Galperin, M.Y., and Koonin, E.V. (2010) From complete genome sequence to 'complete' understanding? Trends Biotechnol 28: 398-406.
13. Ge, X., Wexler, A.S., and Clegg, S.L. (2011) Atmospheric amines - part I. A review. Atmos Environ 45: 524-546.
14. Gibb, S.W., and Hatton, A.D. (2004) The occurrence and distribution of trimethylamine-N-oxide in Antarctic coastal waters. Mar Chem 91: 65-75.
15. Kalyuzhnaya, M.G., De Marco, P., Bowerman, S., Pacheco, C.C., Lara, J.C., Lidstrom, M.E., etal. (2006) Methyloversatilis universalis gen. nov., sp. nov., a novel taxon within the Betaproteobacteria represented by three methylotrophic isolates. Int J Syst Evol Microbiol 56: 2517-2522.
16. Kamanavalli, C.M., and Ninnekar, H.Z. (2000) Biodegradation of propoxur by Pseudomonas species. World J Microb Biot 16: 329-331.
17. Kamiya, A., and Ose, Y. (1984) Study of odorous compounds produced by putrefaction of foods: 5. Fatty-acids, sulfur-compounds and amines. J Chromatogr 292: 383-391.
18. Kanamori, T., Kanou, N., Atomi, H., and Imanaka, T. (2004) Enzymatic characterization of a prokaryotic urea carboxylase. J Bacteriol 186: 2532-2539.
19. Kimura, M., Seki, N., and Kimura, I. (2000) Purification and characterization of trimethylamine-N-oxide demethylase from walleye pollack muscle. Fish Sci 66: 967-973.
20. King, G.M. (1988) Distributions and metabolism of quaternary amines in marine sediments. In Nitrogen Cycling in Coastal Marine Environments. Blackburn, T.H., and Sørensen, J. (eds). New York, USA: John Wiley & Sons, pp. 143-173.
21. Large, P.J. (1971) Non-oxidative demethylation of trimethylamine N-oxide by Pseudomonas aminovorans. FEBS Lett 18: 297-300.
22. Lidbury, I., Murrell, J.C., and Chen, Y. (2014) Trimethylamine N-oxide metabolism by abundant marine heterotrophic bacteria. Proc Natl Acad Sci USA 111: 2710-2715.
23. Marchler-Bauer, A., Zheng, C., Chitsaz, F., Derbyshire, M.K., Geer, L.Y., Geer, R.C., etal. (2013) CDD: conserved domains and protein three-dimensional strucure. Nucl Acids Res 41: D348-D352.
24. Marx, C.J., and Lidstrom, M.E. (2002) Broad-host-range cre-lox system for antibiotic marker recycling in gram-negative bacteria. Biotechniques 33: 1062-1067.
25. Mitch, W.A., Sharp, J.O., Trussell, R.R., Valentine, R.L., Alvarez-Cohen, L., and Sedlak, D.L. (2003) N-Nitrosodimethylamine (NDMA) as a drinking water contaminant: a review. Environ Eng Sci 20: 389-404.
26. Murphy, S.M., Sorooshian, A., Kroll, J.H., Ng, N.L., Chhabra, P., Tong, C., etal. (2007) Secondary aerosol formation from atmospheric reactions of aliphatic amines. Atmos Chem Phys 7: 2313-2337.
27. Myers, P.A., and Zatman, L.J. (1971) The metabolism of trimethylamine N-oxide by Bacillus PM6. Biochem J 121: 10P.
28. Okamura-Ikeda, K., Hosaka, H., Yoshimura, M., Yamashita, E., Toma, S., Nakagawa, A., etal. (2005) Crystal structure of human T-protein of glycine cleavage system at 2.0 A resolution and its implication for understanding non-ketotic hyperglycinemia. J Mol Biol 351: 1146-1159.
29. Parkin, K.L., and Hultin, H.O. (1986) Characterization of trimethylamine-N-oxide (TMAO) demethylase activity from fish muscle microsomes. J Biochem 100: 77-86.
30. Punta, M., Coggill, P.C., Eberhardt, R.Y., Mistry, J., Tate, J., Boursnell, C., etal. (2012) The Pfam protein families database. Nucleic Acids Res 40: D290-D301.
31. Quesenberry, M.S., and Lee, Y.C. (1996) A rapid formaldehyde assay using purpald reagent: application under periodation conditions. Anal Biochem 234: 50-55.
32. Raymond, J.A., and Plopper, G.E. (2002) A bacterial TMAO transporter. Comp Biochem Physiol B Biochem Mol Biol 133: 29-34.
33. Reisch, C.R., Moran, M.A., and Whitman, W.B. (2008) Dimethylsulfoniopropionate-dependent demethylase (DmdA) from Pelagibacter ubique and Silicibacter pomeroyi. J Bacteriol 190: 8018-8024.
34. Richards, S.E., Wang, Y., Claus, S.P., Lawler, D., Kochhar, S., Holmes, E., etal. (2013) Metabolic phenotype modulation by caloric restriction in a lifelong dog study. J Proteome Res 12: 3117-3127.
35. Saier, M.H. (2000) Families of transmembrane transporters selective for amino acids and their derivatives. Microbiology 146 (Pt 8): 1775-1795.
36. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys J 78: 1606-1619.
37. Schuller, D.J., Reisch, C.R., Moran, M.A., Whitman, W.B., and Lanzilotta, W.N. (2012) Structures of dimethylsulfoniopropionate-dependent demethylase from the marine organism Pelagibacter ubique. Protein Sci 21: 289-298.
38. Smith, J.L., Wishnok, J.S., and Deen, W.M. (1994) Metabolism and excretion of methylamines in rats. Toxicol Appl Pharmacol 125: 296-308.
39. Sun, J., Steindler, L., Thrash, J.C., Halsey, K.H., Smith, D.P., Carter, A.E., etal. (2011) One carbon metabolism in SAR11 pelagic marine bacteria. PLoS ONE 6: e23973.
40. Takeuchi, K., Hatanaka, A., Kimura, M., Seki, N., Kimura, I., Yamada, S., etal. (2003) Aspolin, a novel extremely aspartic acid-rich protein in fish muscle, promotes iron-mediated demethylation of trimethylamine-N-oxide. J Biol Chem 278: 47416-47422.
41. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
42. Topp, E., Hanson, R.S., Ringelberg, D.B., White, D.C., and Wheatcroft, R. (1993) Isolation and characterization of an N-methylcarbamate insecticide-degrading methylotrophic bacterium. Appl Environ Microbiol 59: 3339-3349.
43. Warren, C.R. (2013a) High diversity of small organic N observed in soil water. Soil Biol Biochem 57: 444-450.
44. Warren, C.R. (2013b) Quaternary ammonium compounds can be abundant in some soils and are taken up as intact molecules by plants. New Phytol 198: 476-485.
45. Yancey, P.H. (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208: 2819-2830.
46. Yu, Z., Zhang, Q., Kraus, T.E.C., Dahlgren, R.A., Anastasio, C., and Zasoski, R.J. (2002) Contribution of amino compounds to dissolved organic nitrogen in forest soils. Biogeochemistry 61: 173-198.
47. Zhang, A.Q., Mitchell, S.C., Ayesh, R., and Smith, R.L. (1992) Determination of trimethylamine and related aliphatic-amines in human urine by headspace gas-chromatography. J Chromatogr 584: 141-145.