Comparative genomics of methylated amine utilization by marine Roseobacter clade bacteria and development of functional gene markers (tmm, gmaS)

Environmental Microbiology

Volumn 14, Issue 9, 2012, Pages 2308-2322

  Chen, Yin ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINE; GAMMA GLUTAMYLMETHYLAMIDE SYNTHETASE; GAMMA-GLUTAMYLMETHYLAMIDE SYNTHETASE; LIGASE; MIXED FUNCTION OXIDASE; NITROGEN; SEA WATER;

ARTICLE; BACTERIAL GENOME; CLASSIFICATION; GENETIC MARKER; GENETICS; GENOMICS; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PHYLOGENY; POLYMERASE CHAIN REACTION; REPRODUCIBILITY; ROSEOBACTER; STANDARD;

AMINES; CARBON-NITROGEN LIGASES; GENETIC MARKERS; GENOME, BACTERIAL; GENOMICS; MIXED FUNCTION OXYGENASES; NITROGEN; OXIDATION-REDUCTION; PHYLOGENY; POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; ROSEOBACTER; SEAWATER; WATER MICROBIOLOGY;

BACTERIA (MICROORGANISMS); ROSEOBACTER;

EID: 84865717815     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2012.02765.x     Document Type: Article

References (71)

1. Anthony, C. (1982) The Biochemistry of Methylotrophs. London, UK: Academic Press.
2. Biebl, H., Allgaier, M., Lünsdorf, H., Pukall, R., Tindall, B.J., and Wagner-Däbler, I. (2005) Roseovarius mucosus sp. nov., a member of the Roseobacter clade with trace amounts of bacteriochlorophyll a. Int J Syst Evol Microbiol 55: 2377-2383.
3. Biers, E.J., Wang, K., Pennington, C., Belas, R., Chen, F., and Moran, M.A. (2008) Occurrence and expression of gene transfer agent genes in marine bacterioplankton. Appl Environ Microbiol 74: 2933-2939.
4. Boden, R., Kelly, D.P., Murrell, J.C., and Schäfer, H. (2010) Oxidation of dimethylsulfide to tetrathionate by Methylophaga thiooxidans sp. nov.: a new link in the sulfur cycle. Environ Microbiol 12: 2688-2699.
5. Boden, R., Murrell, J.C., and Schäfer, H. (2011) Dimethylsulfide is an energy source for the heterotrophic marine bacterium Sagittula stellata. FEMS Microbiol Lett 322: 188-193.
6. Boettcher, K.L., Geaghan, K.K., Maloy, A.P., and Barber, B.J. (2005) Roseovarius crassostreae sp. nov., a member of the Roseobacter clade and the apparent cause of juvenile oyster disease (JOD) in cultured Eastern oysters. Int J Syst Evol Microbiol 55: 1531-1537.
7. Bosch, G., Skovran, E., Xia, Q., Wang, T., Taub, F., Miller, J.A., etal. (2009) Comprehensive proteomics of Methylobacterium extorquens AM1 metabolism under single carbon and nonmethylotrophic conditions. Proteomics 8: 3494-3505.
8. Buchan, A., González, J.M., and Moran, M.A. (2005) Overview of the marine Roseobacter lineage. Appl Environ Microbiol 71: 5665-5677.
9. Capone, D.G., Bronk, D.A., Mulholland, M.R., and Carpenter, E.J. (eds) (2008) Nitrogen in the Marine Environment, 2nd edn. Amsterdam, the Netherland: Elsevier.
10. Chandler, S.R. (1983) The utilization of methylamine-nitrogen by the methazotrophic bacterium Pseudomonad P. PhD thesis. University of Reading, UK.
11. Chen, Y., Dumont, M.G., Cébron, A., and Murrell, J.C. (2007) Identification of active methanotrophs in a landfill soil through detection of expression of 16S rRNA and functional genes. Environ Microbiol 9: 2855-2869.
12. Chen, Y., Wu, L., Boden, R., Hillebrand, A., Kumaresan, D., Moussard, H., etal. (2009) Life without light: microbial diversity and evidence of sulfur- and ammonium-based chemolithotrophy in Movile Cave. ISME J 3: 1093-1104.
13. Chen, Y., McAleer, K.L., and Murrell, J.C. (2010a) Monomethylamine as a nitrogen source for a nonmethylotrophic bacterium, Agrobacterium tumefaciens. Appl Environ 76: 4102-4104.
14. Chen, Y., Scanlan, J., Song, L., Crombie, A., Rahman, M.T., Schäfer, H., and Murrell, J.C. (2010b) Gamma-glutamylmethylamide is an essential intermediate for monomethylamine metabolism in Methylocella silvestris. Appl Environ Microbiol 76: 4530-4537.
15. 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: 17797-19976.
16. Chistoserdova, L. (2011) Modularity of methylotrophy, revisited. Environ Microbiol 13: 2603-2622.
17. Chistoserdova, L., Kalyuzhnaya, M.G., and Lidstrom, M.E. (2009) The expanding world of methylotrophic metabolism. Annu Rev Microbiol 63: 477-499.
18. Curson, A.R.J., Todd, J.D., Sullivan, M.J., and Johnston, A.W.B. (2011) Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes. Nat Rev Microbiol 9: 849-859.
19. Davidson, V.L., Husain, M., and Neher, J.W. (1986) Electron transfer flavoprotein from Methylophilus methylotrophus: properties, comparison with other electron transfer flavoproteins, and regulation of expression by carbon source. J Bacteriol 166: 812-817.
20. Dixon, J.L., Beale, R., and Nightingale, P.D. (2011) Microbial methanol uptake in northeast Atlantic waters. ISME J 5: 704-716.
21. Fitzsimons, M.F., Kahni-danon, B., and Dawitt, M. (2001) Distributions and adsorption of the methylamines in the inter-tidal sediments of an East Anglian estuary. Environ Exp Bot 46: 225-236.
22. 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.
23. Gibb, S.W., Mantoura, R.F.C., Liss, P.S., and Barlow, R.G. (1999) Distributions and biogeochemistries of methylamines and ammonium in the Arabian Sea. Deep Sea Res Part II Top Stud Oceanogr 46: 593-615.
24. Giovannoni, S., and Rappé, M. (2000) Evolution, diversity, and molecular ecology of marine prokaryotes. In Microbial Ecology of the Oceans. Kirchman, D.L. (ed.). New York, NY, USA: John Wiley & Sons, pp. 47-84.
25. Giovannoni, S., Hayakawa, D.H., Tripp, H.J., Stingl, U., Givan, S.A., Cho, J.C., etal. (2008) The small genome of an abundant coastal ocean methylotroph. Environ Microbiol 10: 1771-1782.
26. Goenrich, M., Bartoschek, S., Hagemeier, C.H., Griesinger, C., and Vorholt, J.A. (2002) A glutathione-dependent formaldehyde-activating enzyme (Gfa) from Paracoccus denitrificans detected and purified via two-dimensional proton exchange NMR spectroscopy. J Biol Chem 277: 3069-3072.
27. González, J.M., and Moran, M.A. (1997) Numerical dominance of a group of marine bacteria in the alpha-subclass of the class Proteobacteria in coastal seawater. Appl Environ Microbiol 63: 4237-4242.
28. Hatton, A.D., and Gibb, S.W. (1999) A technique for the determination of trimethylamine N-oxide in natural waters and biological media. Anal Chem 71: 4886-4891.
29. Holmes, A.J., Kelly, D.P., Baker, S.C., Thompson, A.S., De Marco, P., Kenna, E.M., and Murrell, J.C. (1997) Methylosulfonomonas methylovora gen. nov., sp. nov., and Marinosulfonomonas methylotropha gen. nov., sp. nov.: novel methylotrophs able to grow on methanesulfonic acid. Arch Microbiol 167: 46-53.
30. Janvier, M., Frehel, C., Grimont, F., and Gasser, F. (1985) Methylophaga marina gen. nov., sp. nov. and Methylophaga thalassica sp. nov., marine methylotrophs. Int J Syst Bacteriol 35: 131-139.
31. Janvier, M., Regnault, B., and Grimont, P. (2003) Development and use of fluorescent 16S rRNA-targeted probes for the specific detection of Methylophaga species by in situ hybridization in marine sediments. Res Microbiol 154: 483-490.
32. Kanagawa, T., Dazai, M., and Fukuoka, S. (1982) Degradation of O, O-dimethyl phosphorodithioate by Thiobacillus thioparus TK-1 and Pseudomonas AK-2. Agric Biol Chem 46: 2571-2578.
33. Kasprzak, A.A., Papas, E.J., and Steenkamp, D.J. (1983) Identity of the subunits and the stoicheiometry of prosthetic groups in trimethylamine dehydrogenase and dimethylamine dehydrogenase. Biochem J 211: 535-541.
34. Kim, H.G., Doronina, N.V., Trotsenko, Y.A., and Kim, S.W. (2007) Methylophaga aminisulfidivorans sp. nov., a restricted facultatively methylotrophic marine bacterium. Int J Syst Evol Microbiol 57: 2096-2101.
35. 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, NY, USA: John Wiley & Sons, pp. 143-173.
36. Latypova, E., Yang, S., Wang, Y.S., Chavkin, T.A., Hackett, M., Schäfer, H., and Kalyuzhnaya, M.G. (2010) Genetics of the glutamate-mediated methylamine utilization pathway in the facultative methylotrophic beta-proteobacterium Methyloversatilis universalis FAM5. Mol Microbiol 75: 426-439.
37. Lee, C., and Olson, B.L. (1984) Dissolved, exchangeable and bound aliphatic amines in marine sediments: initial results. Org Geochem 6: 259-263.
38. Loginova, N.V., Shishkina, V.N., and Trotsenko, Y.A. (1976) Primary metabolic pathways of methylated amines in Hyphomicrobium vulgare. Microbiology 45: 34-39.
39. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., etal. (2004) arb: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
40. Markowitz, V.M., Chen, I.-M.A., Palaniappan, K., Chu, K., Szeto, E., Grechkin, Y., etal. (2010) The integrated microbial genomes system: an expanding comparative analysis resource. Nucleic Acids Res 38: D382-D390.
41. Marx, C.J., Laukel, M., Vorholt, J.A., and Lidstrom, M.E. (2003) Purification of the formate-tetrahydrofolate ligase from Methylobacterium extorquens AM1 and demonstration of its requirement for methylotrophic growth. J Bacteriol 185: 7169-7175.
42. Moussard, H., Stralis-Pavese, N., Bodrossy, L., Neufeld, J.D., and Murrell, J.C. (2009) Identification of active methylotrophic bacteria inhabiting surface sediment of a marine estuary. Environ Microbiol Rep 1: 424-433.
43. Neufeld, J.D., Schäfer, H., Cox, M.J., Boden, R., McDonald, I.R., and Murrell, J.C. (2007) Stable-isotope probing implicates Methylophaga spp. and novel Gammaproteobacteria in marine methanol and methylamine metabolism. ISME J 1: 480-491.
44. Neufeld, J.D., Boden, R., Moussard, H., Schäfer, H., and Murrell, J.C. (2008) Substrate-specific clades of active marine methylotrophs associated with a phytoplankton bloom in a temperate coastal environment. Appl Environ Microbiol 74: 7321-7328.
45. Newton, R.J., Griffin, L.E., Bowles, K.M., Meile, C., Gifford, S., Givens, C.E., etal. (2010) Genome characteristics of a generalist marine bacterial lineage. ISME J 4: 784-798.
46. Oren, A. (1990) Formation and breakdown of glycine betaine and trimethylamine in hypersaline environments. Antonie Van Leeuwenhoek 58: 291-298.
47. Pollock, R.J., and Hersh, L.B. (1971) N-methylglutamate synthetase: purification and properties of the enzyme. J Biol Chem 246: 4737-4743.
48. Reitzer, L. (2003) Nitrogen assimilation and global regulation in Escherichia coli. Annu Rev Microbiol 57: 155-176.
49. Rusch, D.B., Halpern, A.L., Sutton, G., Heidelberg, K.B., Williamson, S., Yooseph, S., etal. (2007) The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol 5: e77.
50. Schaefer, J.K., Goodwin, K.D., McDonald, I.R., Murrell, J.C., and Oremland, R.S. (2002) Leisingera methylohalidivorans gen. nov., sp. nov., a marine methylotroph that grows on methyl bromide. Int J Syst Evol Microbiol 52: 851-859.
51. Schäfer, H. (2007) Isolation of Methylophaga spp. from marine dimethylsulfide degrading enrichment cultures and identification of polypeptides induced during growth on dimethylsulfide. Appl Environ Microbiol 73: 2580-2591.
52. Schäfer, H., McDonald, I.R., Nightingale, P.D., and Murrell, J.C. (2005) Evidence for the presence of a CmuA methyltransferase pathway in novel marine methyl halide-oxidizing bacteria. Environ Microbiol 7: 839-852.
53. Selje, N., Simon, M., and Brinkhoff, T. (2004) A newly discovered Roseobacter cluster in temperate and polar oceans. Nature 427: 445-448.
54. Sohm, J.A., Webb, E.A., and Capone, D.G. (2011) Emerging patterns of marine nitrogen fixation. Nat Rev Microbiol 9: 499-508.
55. Somerville, C.C., Knight, I.T., Straube, W.L., and Colwell, R.R. (1989) Simple, rapid method for direct isolation of nucleic acids from aquatic environments. Appl Environ Microbiol 55: 548-554.
56. Sorokin, D.Y., Tourova, T.P., and Muyzer, G. (2005) Citreicella thiooxidans gen. nov., sp. nov., a novel lithoheterotrophic sulfur-oxidizing bacterium from the Black Sea. Syst Appl Microbiol 28: 679-687.
57. 1 utilization pathway in Methylobacterium chloromethanicum CM4. J Bacteriol 184: 3476-3484.
58. Sun, F., Wang, B., Liu, X., Lai, Q., Du, Y., Li, G., etal. (2010) Leisingera nanhaiensis sp. nov., isolated from marine sediment. Int J Syst Evol Microbiol 60: 275-280.
59. 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.
60. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007) mega4: molecular evolutionary genetics analysis (mega) software version 4.0. Mol Biol Evol 24: 1596-1599.
61. Uchino, Y., Hirata, A., Yokota, A., and Sugiyama, J. (1998) Reclassification of marine Agrobacterium species: proposals of Stappia stellulata gen. nov., comb. nov., Stappia aggregata sp. nov., nom. rev., Ruegeria atlantica gen. nov., comb. nov., Ruegeria gelatinovora comb. nov., Ruegeria algicola comb. nov., and Ahrensia kieliense gen. nov., sp. nov., nom. rev. J Gen Appl Microbiol 44: 201-210.
62. Vandecandelaere, I., Segaert, E., Mollica, A., Faimali, M., and Vandamme, P. (2008) Leisingera aquimarina sp. nov., isolated from a marine electroactive biofilm, and emended descriptions of Leisingera methylohalidivorans Schaefer etal. 2002, Phaeobacter daeponensis Yoon etal. 2007 and Phaeobacter inhibens Martens etal. 2006. Int J Syst Evol Microbiol 58: 2788-2793.
63. Vorholt, J.A., Marc, C.J., Lidstrom, M.E., and Thauer, R.K. (2000) Novel formaldehyde-activating enzyme in Methylobacterium extorquens AM1 required for growth on methanol. J Bacteriol 182: 6645-6650.
64. Wagner-Döbler, I., and Biebl, H. (2006) Environmental biology of the marine Roseobacter lineage. Annu Rev Microbiol 60: 255-280.
65. Wang, X.C., and Lee, C. (1994) Sources and distribution of aliphatic amines in salt marsh sediment. Org Geochem 22: 1005-1201.
66. 1 oxidation pathway in Methanosarcina barkeri: new insights into Mtr/Mer bypass pathway. J Bacteriol 190: 1928-1936.
67. Welsh, D.T. (2000) Ecological significance of compatible solute accumulation by microorganisms: from single cells to global climate. FEMS Microbiol Rev 24: 263-290.
68. Wilson, S.M., Gleisten, M.P., and Donohue, T.J. (2008) Identification of proteins involved in formaldehyde metabolism by Rhodobacter sphaeroides. Microbiology 154: 296-305.
69. Yang, C.C., Packman, L.C., and Scrutton, N.S. (1995) The primary structure of Hyphomicrobium X dimethylamine dehydrogenase: relationship to trimethylamine dehydrogenase and implications for substrate recognition. Eur J Biochem 232: 264-271.
70. Yuan, J., Lai, Q., Wang, B., Sun, F., Liu, X., Du, Y., etal. (2009) Oceanicola pacificus sp. nov., isolated from a deep-sea pyrene-degrading consortium. Int J Syst Evol Microbiol 59: 1158-1161.
71. Zehr, J.P., and Kudela, R.M. (2011) Nitrogen cycle of the open ocean: from genes to ecosystems. Annu Rev Mar Sci 3: 197-225.