The 380 kb pCMU01 Plasmid Encodes Chloromethane Utilization Genes and Redundant Genes for Vitamin B12- and Tetrahydrofolate-Dependent Chloromethane Metabolism in Methylobacterium extorquens CM4: A Proteomic and Bioinformatics Study

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Roselli, Sandro ^a   Nadalig, Thierry ^a   Vuilleumier, Stéphane ^a   Bringel, Françoise ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CORRINOID; CYANOCOBALAMIN; METHANOL; METHYL CHLORIDE; OXIDOREDUCTASE; PAAE LIKE OXIDOREDUCTASE; PROTEIN ACS; PROTEIN METF; PROTEIN PNTAA; TETRAHYDROFOLIC ACID; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL METABOLISM; BACTERIAL STRAIN; BIOINFORMATICS; BIOSYNTHESIS; CHLOROMETHANE UTILIZATION; CMUA GENE; CMUB GENE; COBH2 GENE; CONTROLLED STUDY; DEHALOGENATION; EPISOME; FOLATE METABOLISM; GENE CLUSTER; GENE DUPLICATION; GENETIC IDENTIFICATION; GENOMICS; METHYLOBACTERIUM EXTORQUENS; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PAAE LIKE OXIDOREDUCTASE GENE; PLASMID; PROTEIN ANALYSIS; PROTEOMICS; PURU GENE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; TRANSPORT KINETICS; VITAMIN METABOLISM;

COMPUTATIONAL BIOLOGY; GENES, BACTERIAL; METABOLIC NETWORKS AND PATHWAYS; METHYL CHLORIDE; METHYLOBACTERIUM EXTORQUENS; MULTIGENE FAMILY; PLASMIDS; PROTEOMICS; STRESS, PHYSIOLOGICAL; TETRAHYDROFOLATES; VITAMIN B 12;

BACTERIA (MICROORGANISMS); METHYLOBACTERIUM EXTORQUENS;

EID: 84876043915     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056598     Document Type: Article

References (73)

1. Clerbaux C, Cunnold DM, Anderson J, Engel A, Fraser PJ, et al. (2007) Halogenated long-lived compounds, scientific assessment of ozone depletion: 2006. Global Ozone Research and Monitoring Project 10, Report No. 50. World Meteorological Organization, Geneva.
2. Nadalig T, Farhan Ul Haque M, Roselli S, Schaller H, Bringel F, et al. (2011) Detection and isolation of chloromethane-degrading bacteria from the Arabidopsis thaliana phyllosphere, and characterization of chloromethane utilization genes. FEMS Microbiol Ecol 77: 438-448.
3. Schäfer H, Miller LG, Oremland RS, Murrell JC, (2007) Bacterial cycling of methyl halides. Adv Appl Microbiol 61: 307-346.
4. Vuilleumier S, Nadalig T, Ul Haque MF, Magdelenat G, Lajus A, et al. (2011) Complete genome sequence of the chloromethane-degrading Hyphomicrobium sp. strain MC1. J Bacteriol 193: 5035-5036.
5. Marx CJ, Bringel F, Chistoserdova L, Moulin L, Farhan Ul Haque M, et al. (2012) Complete genome sequences of six strains of the genus Methylobacterium. J Bacteriol 194: 4746-4748.
6. Studer A, McAnulla C, Büchele R, Leisinger T, Vuilleumier S, (2002) Chloromethane-induced genes define a third C1 utilization pathway in Methylobacterium chloromethanicum CM4. J Bacteriol 184: 3476-3484.
7. Vannelli T, Studer A, Kertesz M, Leisinger T, (1998) Chloromethane metabolism by Methylobacterium sp. strain CM4. Appl Environ Microbiol 64: 1933-1936.
8. Studer A, Vuilleumier S, Leisinger T, (1999) Properties of the methylcobalamin: H4folate methyltransferase involved in chloromethane utilization by Methylobacterium sp. strain CM4. Eur J Biochem 264: 242-249.
9. Studer A, Stupperich E, Vuilleumier S, Leisinger T, (2001) Chloromethane: tetrahydrofolate methyl transfer by two proteins from Methylobacterium chloromethanicum strain CM4. Eur J Biochem 268: 2931-2938.
10. Vannelli T, Messmer M, Studer A, Vuilleumier S, Leisinger T, (1999) A corrinoid-dependent catabolic pathway for growth of a Methylobacterium strain with chloromethane. Proc Natl Acad Sci USA 96: 4615-4620.
11. Vuilleumier S, Chistoserdova L, Lee M-C, Bringel F, Lajus A, et al. (2009) Methylobacterium genome sequences: a reference blueprint to investigate microbial metabolism of C1 compounds from natural and industrial sources. PLoS ONE 4: e5584.
12. Chistoserdova L, (2011) Modularity of methylotrophy, revisited. Environ Microbiol 13: 2603-2622.
13. Scott AI, Roessner CA, (2002) Biosynthesis of cobalamin (vitamin B12). Biochem Soc Trans 30: 613-620.
14. Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS, (2003) Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes. J Biol Chem 278: 41148-41159.
15. Yi S, Seth EC, Men Y-J, Stabler SP, Allen RH, et al. (2012) Versatility in corrinoid salvaging and remodeling pathways supports corrinoid-dependent metabolism in Dehalococcoides mccartyi. Appl Environ Microbiol 78: 7745-7752.
16. Muller EEL, Hourcade E, Louhichi-Jelail Y, Hammann P, Vuilleumier S, et al. (2011) Functional genomics of dichloromethane utilization in Methylobacterium extorquens DM4. Environ Microbiol 13: 2518-2535.
17. Smejkalová H, Erb TJ, Fuchs G, (2010) Methanol assimilation in Methylobacterium extorquens AM1: demonstration of all enzymes and their regulation. PLoS ONE 5: e13001.
18. Vallenet D, Engelen S, Mornico D, Cruveiller S, Fleury L, et al. (2009) MicroScope: a platform for microbial genome annotation and comparative genomics. Database (Oxford) 2009: bap021.
19. Gossett JM, (1987) Measurement of Henry's law constants for C1 and C2 chlorinated hydrocarbons. Environ Sci Technol 21: 202-208.
20. Benjamini Y, Hochberg Y, (2000) On the adaptive control of the false discovery rate in multiple testing with independent statistics. J Educ Behav Stat 25: 60-83.
21. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, et al. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41.
22. Sluis MK, Larsen RA, Krum JG, Anderson R, Metcalf WW, et al. (2002) Biochemical, molecular, and genetic analyses of the acetone carboxylases from Xanthobacter autotrophicus strain Py2 and Rhodobacter capsulatus strain B10. J Bacteriol 184: 2969-2977.
23. Petersen J, Brinkmann H, Pradella S, (2009) Diversity and evolution of repABC type plasmids in Rhodobacterales. Environ Microbiol 11: 2627-2638.
24. Cevallos MA, Porta H, Izquierdo J, Tun-Garrido C, García-de-los-Santos A, et al. (2002) Rhizobium etli CFN42 contains at least three plasmids of the repABC family: a structural and evolutionary analysis. Plasmid 48: 104-116.
25. Pinto UM, Pappas KM, Winans SC, (2012) The ABCs of plasmid replication and segregation. Nat Rev Microbiol 10: 755-765.
26. Morgan RD, Bhatia TK, Lovasco L, Davis TB, (2008) MmeI: a minimal Type II restriction-modification system that only modifies one DNA strand for host protection. Nucleic Acids Res 36: 6558-6570.
27. Goldberg M, Pribyl T, Juhnke S, Nies DH, (1999) Energetics and topology of CzcA, a cation/proton antiporter of the resistance-nodulation-cell division protein family. J Biol Chem 274: 26065-26070.
28. Cadieux N, Bradbeer C, Reeger-Schneider E, Köster W, Mohanty AK, et al. (2002) Identification of the periplasmic cobalamin-binding protein BtuF of Escherichia coli. J Bacteriol 184: 706-717.
29. Vitreschak AG, Rodionov DA, Mironov AA, Gelfand MS, (2003) Regulation of the vitamin B12 metabolism and transport in bacteria by a conserved RNA structural element. RNA 9: 1084-1097.
30. Lequette Y, Odberg-Ferragut C, Bohin J-P, Lacroix J-M, (2004) Identification of mdoD, an mdoG paralog which encodes a twin-arginine-dependent periplasmic protein that controls osmoregulated periplasmic glucan backbone structures. J Bacteriol 186: 3695-3702.
31. Touzé T, Goude R, Georgeault S, Blanco C, Bonnassie S, (2004) Erwinia chrysanthemi O antigen is required for betaine osmoprotection in high-salt media. J Bacteriol 186: 5547-5550.
32. Li C, Ichikawa JK, Ravetto JJ, Kuo HC, Fu JC, et al. (1994) A new gene involved in stationary-phase survival located at 59 minutes on the Escherichia coli chromosome. J Bacteriol 176: 6015-6022.
33. Streit WR, Phillips DA, (1997) A biotin-regulated locus, bioS, in a possible survival operon of Rhizobium meliloti. Mol Plant Microbe Interact 10: 933-937.
34. Barynin VV, Whittaker MM, Antonyuk SV, Lamzin VS, Harrison PM, et al. (2001) Crystal structure of manganese catalase from Lactobacillus plantarum. Structure 9: 725-738.
35. Jang S, Imlay JA (2010) Hydrogen peroxide inactivates the Escherichia coli Isc iron-sulphur assembly system, and OxyR induces the Suf system to compensate. Mol Microbiol 78: 1448-.
36. Ranquet C, Ollagnier-de-Choudens S, Loiseau L, Barras F, Fontecave M, (2007) Cobalt stress in Escherichia coli. The effect on the iron-sulfur proteins. J Biol Chem 282: 30442-30451.
37. Kiley PJ, Beinert H, (2003) The role of Fe-S proteins in sensing and regulation in bacteria. Curr Opin Microbiol 6: 181-185.
38. Kikuchi G, Motokawa Y, Yoshida T, Hiraga K, (2008) Glycine cleavage system: reaction mechanism, physiological significance, and hyperglycinemia. Proc Jpn Acad, Ser B, Phys Biol Sci 84: 246-263.
39. Kalyuzhnaya MG, Lidstrom ME, (2005) QscR-mediated transcriptional activation of serine cycle genes in Methylobacterium extorquens AM1. J Bacteriol 187: 7511-7517.
40. Kalyuzhnaya MG, Lidstrom ME, (2003) QscR, a LysR-type transcriptional regulator and CbbR homolog, is involved in regulation of the serine cycle genes in Methylobacterium extorquens AM1. J Bacteriol 185: 1229-1235.
41. Doronina NV, Sokolov AP, Trotsenko YA, (1996) Isolation and initial characterization of aerobic chloromethane-utilizing bacteria. FEMS Microbiology Letters 142: 179-183.
42. Warner KL, Larkin MJ, Harper DB, Murrell JC, McDonald IR, (2005) Analysis of genes involved in methyl halide degradation in Aminobacter lissarensis CC495. FEMS Microbiol Lett 251: 45-51.
43. Jarrett JT, Hoover DM, Ludwig ML, Matthews RG, (1998) The mechanism of adenosylmethionine-dependent activation of methionine synthase: a rapid kinetic analysis of intermediates in reductive methylation of Cob(II)alamin enzyme. Biochemistry 37: 12649-12658.
44. Ferguson T, Soares JA, Lienard T, Gottschalk G, Krzycki JA, (2009) RamA, a protein required for reductive activation of corrinoid-dependent methylamine methyltransferase reactions in methanogenic archaea. J Biol Chem 284: 2285-2295.
45. Cotton NP, White SA, Peake SJ, McSweeney S, Jackson JB, (2001) The crystal structure of an asymmetric complex of the two nucleotide binding components of proton-translocating transhydrogenase. Structure 9: 165-176.
46. Okubo Y, Skovran E, Guo X, Sivam D, Lidstrom ME, (2007) Implementation of microarrays for Methylobacterium extorquens AM1. OMICS 11: 325-340.
47. Laukel M, Rossignol M, Borderies G, Völker U, Vorholt JA, (2004) Comparison of the proteome of Methylobacterium extorquens AM1 grown under methylotrophic and nonmethylotrophic conditions. Proteomics 4: 1247-1264.
48. Matthews RG, Sheppard C, Goulding C, (1998) Methylenetetrahydrofolate reductase and methionine synthase: biochemistry and molecular biology. Eur J Pediatr 157Suppl 2: S54-59.
49. Lee HY, Na KB, Koo HM, Kim YS, (2001) Identification of active site residues in Bradyrhizobium japonicum acetyl-CoA synthetase. J Biochem 130: 807-813.
50. Peyraud R, Kiefer P, Christen P, Portais J-C, Vorholt JA, (2012) Co-consumption of methanol and succinate by Methylobacterium extorquens AM1. PLoS ONE 7: e48271.
51. Pollich M, Klug G, (1995) Identification and sequence analysis of genes involved in late steps in cobalamin (vitamin B12) synthesis in Rhodobacter capsulatus. J Bacteriol 177: 4481-4487.
52. Campbell GRO, Taga ME, Mistry K, Lloret J, Anderson PJ, et al. (2006) Sinorhizobium meliloti bluB is necessary for production of 5,6-dimethylbenzimidazole, the lower ligand of B12. Proc Natl Acad Sci USA 103: 4634-4639.
53. Gray MJ, Escalante-Semerena JC, (2007) Single-enzyme conversion of FMNH2 to 5,6-dimethylbenzimidazole, the lower ligand of B12. Proc Natl Acad Sci USA 104: 2921-2926.
54. Taga ME, Larsen NA, Howard-Jones AR, Walsh CT, Walker GC, (2007) BluB cannibalizes flavin to form the lower ligand of vitamin B12. Nature 446: 449-453.
55. Zhang Y, Rodionov DA, Gelfand MS, Gladyshev VN, (2009) Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization. BMC Genomics 10: 78.
56. Bratlie MS, Johansen J, Sherman BT, Huang DW, Lempicki RA, et al. (2010) Gene duplications in prokaryotes can be associated with environmental adaptation. BMC Genomics 11: 588.
57. Vévodová J, Graham RM, Raux E, Schubert HL, Roper DI, et al. (2004) Structure/function studies on a S-adenosyl-L-methionine-dependent uroporphyrinogen III C methyltransferase (SUMT), a key regulatory enzyme of tetrapyrrole biosynthesis. J Mol Biol 344: 419-433.
58. Warren MJ, Roessner CA, Santander PJ, Scott AI, (1990) The Escherichia coli cysG gene encodes S-adenosylmethionine-dependent uroporphyrinogen III methylase. Biochem J 265: 725-729.
59. Haydock SF, Mironenko T, Ghoorahoo HI, Leadlay PF, (2004) The putative elaiophylin biosynthetic gene cluster in Streptomyces sp. DSM4137 is adjacent to genes encoding adenosylcobalamin-dependent methylmalonyl CoA mutase and to genes for synthesis of cobalamin. J Biotechnol 113: 55-68.
60. Roessner CA, Williams HJ, Scott AI, (2005) Genetically engineered production of 1-desmethylcobyrinic acid, 1-desmethylcobyrinic acid a,c-diamide, and cobyrinic acid a,c-diamide in Escherichia coli implies a role for CbiD in C-1 methylation in the anaerobic pathway to cobalamin. J Biol Chem 280: 16748-16753.
61. Alber BE, (2011) Biotechnological potential of the ethylmalonyl-CoA pathway. Appl Microbiol Biotechnol 89: 17-25.
62. McCutcheon JP, McDonald BR, Moran NA, (2009) Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc Natl Acad Sci USA 106: 15394-15399.
63. Morita H, Toh H, Fukuda S, Horikawa H, Oshima K, et al. (2008) Comparative genome analysis of Lactobacillus reuteri and Lactobacillus fermentum reveal a genomic island for reuterin and cobalamin production. DNA Res 15: 151-161.
64. Daniel R, Bobik TA, Gottschalk G, (1998) Biochemistry of coenzyme B12-dependent glycerol and diol dehydratases and organization of the encoding genes. FEMS Microbiol Rev 22: 553-566.
65. Bosi E, Fani R, Fondi M, (2011) The mosaicism of plasmids revealed by atypical genes detection and analysis. BMC Genomics 12: 403.
66. Muller EEL, Bringel F, Vuilleumier S, (2011) Dichloromethane-degrading bacteria in the genomic age. Res Microbiol 162: 869-876.
67. Peyraud R, Kiefer P, Christen P, Massou S, Portais J-C, et al. (2009) Demonstration of the ethylmalonyl-CoA pathway by using 13C metabolomics. Proc Natl Acad Sci USA 106: 4846-4851.
68. Halsey KH, Carter AE, Giovannoni SJ, (2012) Synergistic metabolism of a broad range of C1 compounds in the marine methylotrophic bacterium HTCC2181. Environ Microbiol 14: 630-640.
69. Niegowski D, Eshaghi S, (2007) The CorA family: structure and function revisited. Cell Mol Life Sci 64: 2564-2574.
70. Chou H-H, Berthet J, Marx CJ, (2009) Fast growth increases the selective advantage of a mutation arising recurrently during evolution under metal limitation. PLoS Genet 5: e1000652.
71. Borodina E, McDonald IR, Murrell JC, (2004) Chloromethane-dependent expression of the cmu gene cluster of Hyphomicrobium chloromethanicum. Appl Environ Microbiol 70: 4177-4186.
72. Maden BE, (2000) Tetrahydrofolate and tetrahydromethanopterin compared: functionally distinct carriers in C1 metabolism. Biochem J 350 Pt 3: 609-629.
73. Vorholt JA, (2002) Cofactor-dependent pathways of formaldehyde oxidation in methylotrophic bacteria. Arch Microbiol 178: 239-249.