Formaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) in Methanosarcina barkeri: A possible function in ribose-5-phosphate biosynthesis

Archives of Microbiology

Volumn 184, Issue 1, 2005, Pages 41-48

  Goenrich, Meike ^a   Thauer, Rudolf K ^a   Yurimoto, Hiroya ^b   Kato, Nobuo ^b  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

C1 metabolism; Methanogenesis from formaldehyde; Methanogenic archaea; Methanosarcina mazei; Ribulose monophosphate pathway

Indexed keywords

BACTERIAL ENZYME; CELL EXTRACT; FORMALDEHYDE; FORMALDEHYDE ACTIVATING ENZYME; HEXULOSE PHOSPHATE SYNTHASE; METHANOPTERIN; RIBOSE 5 PHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; CATALYSIS; ENZYME ACTIVITY; ENZYME SYNTHESIS; ESCHERICHIA COLI; GENE EXPRESSION; METHANOGENESIS; METHANOSARCINA BARKERI; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; WESTERN BLOTTING;

ALDEHYDE-LYASES; AMINO ACID SEQUENCE; CARBON-NITROGEN LIGASES; FORMALDEHYDE; METHANOSARCINA BARKERI; MOLECULAR SEQUENCE DATA; RIBOSEMONOPHOSPHATES;

ARCHAEA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; METHANOSARCINA BARKERI; METHANOSARCINA MAZEI;

EID: 27744470399     PISSN: 03028933     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00203-005-0008-1     Document Type: Article

References (52)

1. Acharya P, Goenrich M, Hagemeier CH, Demmer U, Vorholt JA, Thauer RK, Ermler U (2005) How an enzyme binds the C1-carrier tetrahydromethanopterin: Structure of the tetrahydromethanopterin dependent formaldehyde-activating enzyme (Fae) from Methylobacterium extorquens AM1. J Biol Chem 280:13712-13719
2. Adeosun EK, Smith TJ, Hoberg AM, Velarde G, Ford R, Dalton H (2004) Formaldehyde dehydrogenase preparations from Methylococcus capsulatus (Bath) comprise methanol dehydrogenase and methylene tetrahydromethanopterin dehydrogenase. Microbiology 150:707-713
3. Arfman N, Bystrykh L, Govorukhina NI, Dijkhuizen L (1990) 3-Hexulose-6-phosphate synthase from thermotolerant methylotroph Bacillus C1. Methods Enzymol 188:391-397
4. Bauer M, Lombardot T, Teeling H, Ward NL, Amann RI, Glockner FO (2004) Archaea-like genes for C1-transfer enzymes in Planctomycetes: phylogenetic implications of their unexpected presence in this phylum. J Mol Evol 59:571-586
5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
6. Breitung J, Börner G, Scholz S, Linder D, Stetter KO, Thauer RK (1992) Salt dependence, kinetic properties and catalytic mechanism of N-formylmethanofuran:tetrahydromethanopterin formyltransferase from the extreme thermophile Methanopyrus kandleri. Eur J Biochem 210:971-981
7. Brockamp HP, Steigel A, Kula MR (1993) Stereochemistry of Aldol Reactions with 3-Hexulose Phosphate Synthase. Liebigs Ann Chem, pp 621-624
8. Buchenau B, Thauer RK (2004) Tetrahydrofolate-specific enzymes in Methanosarcina barkeri and growth dependence of this methanogenic archaeon on folic acid or p-aminobenzoic acid. Arch Microbiol 182:313-325
9. Bult CJ, White O, Olsen GJ, Zhou L, Fleischmann RD, Sutton GG, Blake JA, FitzGerald LM, Clayton RA, Gocayne JD, Kerlavage AR, Dougherty BA, Tomb JF, Adams MD, Reich CI, Overbeek R, Kirkness EF, Weinstock KG, Merrick JM, Glodek A, Scott JL, Geoghagen NS, Venter JC (1996) Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273:1058-1073
10. Chistoserdova L, Vorholt JA, Thauer RK, Lidstrom ME (1998) C1 transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic Archaea. Science 281:99-102
11. Chistoserdova L, Gomelsky L, Vorholt JA, Gomelsky M, Tsygankov YD, Lidstrom ME (2000) Analysis of two formaldehyde oxidation pathways in Methylobacillus flagellatus KT, a ribulose monophosphate cycle methylotroph. Microbiology 146:233-238
12. Chistoserdova L, Jenkins C, Kalyuzhnaya MG, Marx CJ, Lapidus A, Vorholt JA, Staley JT, Lidstrom ME (2004) The enigmatic planctomycetes may hold a key to the origins of methanogenesis and methylotrophy. Mol Biol Evol 21:1234-1241
13. Daussmann T, Aivasidis A, Wandrey C (1997) Purification and characterization of an alcohol:N,N-dimethyl-4-nitrosoaniline oxidoreductase from the methanogen Methanosarcina barkeri DSM 804 strain Fusaro. Eur J Biochem 248:889-896
14. Deppenmeier U, Johann A, Hartsch T, Merkl R, Schmitz RA, Martinez-Arias R, Henne A, Wiezer A, Baumer S, Jacobi C, Bruggemann H, Lienard T, Christmann A, Bomeke M, Steckel S, Bhattacharyya A, Lykidis A, Overbeek R, Klenk HP, Gunsalus RP, Fritz HJ, Gottschalk G (2002) The genome of Methanosarcina mazei: evidence for lateral gene transfer between bacteria and archaea. J Mol Microbiol Biotechnol 4:453-461
15. Ferenci T, Strøm T, Quayle JR (1974) Purification and properties of 3-hexulose phosphate synthase and phospho-3-hexuloisomerase from Methylococcus capsulatus. Biochem J 144:477-486
16. Galagan JE, Nusbaum C, Roy A, Endrizzi MG, MacDonald P, FitzHugh W, Calvo S, Engels R, Smirnov S, Atnoor D, Brown A, Allen N, Naylor J, Stange-Thomann N, DeArellano K, Johnson R, Linton L, McEwan P, McKernan K, Talamas J, Tirrell A, Ye WJ, Zimmer A, Barber RD, Cann I, Birren B (2002) The genome of M. acetivorans reveals extensive metabolic and physiological diversity. Genome Res 12:532-542
17. Goenrich M, Bursy J, Hubner E, Linder D, Schwartz AC, Vorholt JA (2002) Purification and characterization of the methylene tetrahydromethanopterin dehydrogenase MtdB and the methylene tetrahydrofolate dehydrogenase FolD from Hyphomicrobium zavarzinii ZV580. Arch Microbiol 177:299-303
18. Hendrickson EL, Kaul R, Zhou Y, Bovee D, Chapman P, Chung J, Conway de Macario E, Dodsworth JA, Gillett W, Graham DE, Hackett M, Haydock AK, Kang A, Land ML, Levy R, Lie TJ, Major TA, Moore BC, Porat I, Palmeiri A, Rouse G, Saenphimmachak C, Soll D, Van Dien S, Wang T, Whitman WB, Xia Q, Zhang Y, Larimer FW, Olson MV, Leigh JA (2004) Complete genome sequence of the genetically tractable hydrogenotrophic methanogen Methanococcus maripaludis. J Bacteriol 186:6956-6969
19. Ishikawa K, Matsui I, Payan F, Cambillau C, Ishida H, Kawarabayasi Y, Kikuchi H, Roussel A (2002) A hyperthermostable D-ribose-5-phosphate isomerase from Pyrococcus horikoshii characterization and three-dimensional structure. Structure (Camb) 10:877-886
20. Johnson KA, Chen L, Yang H, Roberts MF, Stec B (2001) Crystal structure and catalytic mechanism of the MJ0109 gene product: a bifunctional enzyme with inositol monophosphatase and fructose 1,6-bisphosphatase activities. Biochemistry 40:618-630
21. 2. Eur J Biochem 184:223-232
22. 4. Eur J Biochem 186:309-316
23. Karrasch M, Börner G, Enßle M, Thauer RK (1989) Formylmethanofuran dehydrogenase from methanogenic bacteria, a molybdoenzyme. FEBS Lett 253:226-230
24. Kato N (1990) 3-Hexulose-6-phosphate synthase from Mycobacterium gastri MB19. Methods Enzymol 188:397-401
25. Kato N, Ohashi H, Tani Y, Ogata K (1978) 3-Hexulosephosphate synthase from Methylomonas aminofaciens 77a. Purification, properties and kinetics. Biochim Biophys Acta 523:236-244
26. Klenk HP, Clayton RA, Tomb JF, White O, Nelson KE, Ketchum KA, Dodson RJ, Gwinn M, Hickey EK, Peterson JD, Richardson DL, Kerlavage AR, Graham DE, Kyrpides NC, Fleischmann RD, Quackenbush J, Lee NH, Sutton GG, Gill S, Kirkness EF, Dougherty BA, McKenney K, Adams MD, Loftus B, Venter JC (1997) The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 390:364-370
27. Larimer FW, Jung C-H, Chen Y-R, Hartman FC (2002) Heterologous overexpression of pentose-5-phosphate isomerase and pentose-5-phosphate 3-epimerase from Methanococcus jannaschii. Microb Comb Genomics 3:80
28. Lorentzen E, Siebers B, Hensel R, Pohl E (2004) Structure, function and evolution of the Archaeal class I fructose-1,6-bisphosphate aldolase. Biochem Soc Trans 32:259-263
29. Maden BEH (2000) Tetrahydrofolate and tetrahydromethanopterin compared: functionally distinct carriers in C-1 metabolism. Biochem J 350:609-629
30. Mahlmann A, Deppenmeier U, Gottschalk G (1989) Methanofuran-B is required for Co2 formation from formaldehyde by Methanosarcina barkeri. FEMS Microbiol Lett 61:115-120
31. Martinez-Cruz LA, Dreyer MK, Boisvert DC, Yokota H, Martinez-Chantar ML, Kim R, Kim SH (2002) Crystal structure of MJ1247 protein from M. jannaschii at 2.0 A resolution infers a molecular function of 3-hexulose-6-phosphate isomerase. Structure (Camb) 10:195-204
32. Marx CJ, Chistoserdova L, Lidstrom ME (2003) Formaldehyde-detoxifying role of the tetrahydromethanopterin-linked pathway in Methylobacterium extorquens AM1. J Bacteriol 185:7160-7168
33. Marx CJ, Miller JA, Chistoserdova L, Lidstrom ME (2004) Multiple formaldehyde oxidation/detoxification pathways in Burkholderia fungorum LB400. J Bacteriol 186:2173-2178
34. Müller V, Winner C, Gottschalk G (1988) Electron-transport driven sodium extrusion during methanogenesis from formaldehyde and molecular hydrogen by Methanosarcina barkeri. Eur J Biochem 178:519-525
35. Orita I, Yurimoto H, Hirai R, Kawarabayasi Y, Sakai Y, Kato N (2005) The archaeon Pyrococcus horikoshiipossesses a bifunctional enzyme for formaldehyde fixation via the ribulose monophosphate pathway. J Bacteriol 187:3636-3642
36. Quayle JR, Ferenci T (1978) Evolutionary aspects of autotrophy. Microbiol Rev 42:251-273
37. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York
38. Slesarev AI, Mezhevaya KV, Makarova KS, Polushin NN, Shcherbinina OV, Shakhova VV, Belova GI, Aravind L, Natale DA, Rogozin IB, Tatusov RL, Wolf YI, Stetter KO, Malykh AG, Koonin EV, Kozyavkin SA (2002) The complete genome of hyperthermophile Methanopyrus kandleri AV19 and monophyly of archaeal methanogens. Proc Natl Acad Sci USA 99:4644-4649
39. Smith DR, Doucette-Stamm LA, Deloughery C, Lee H, Dubois J, Aldredge T, Bashirzadeh R, Blakely D, Cook R, Gilbert K, Harrison D, Hoang L, Keagle P, Lumm W, Pothier B, Qiu D, Spadafora R, Vicaire R, Wang Y, Wierzbowski J, Gibson R, Jiwani N, Caruso A, Bush D, Reeve JN (1997) Complete genome sequence of Methanobacterium thermoautotrophicum Δ: functional analysis and comparative genomics. J Bacteriol 179:7135-7155
40. Soderberg T (2004) Biosynthesis of ribose-5-phosphate and erythrose-4-phosphate in archaea: a phylogenetic analysis of archaeal genomes. Archea 1:published online at http://archaea.ws
41. Stec B, Yang H, Johnson KA, Chen L, Roberts MF (2000) MJ0109 is an enzyme that is both an inositol monophosphatase and the 'missing' archaeal fructose-1,6-bisphosphatase. Nat Struct Biol 7:1046-1050
42. Taylor EJ, Smith NL, Colby J, Charnock SJ, Black GW (2004) The gene encoding the ribulose monophosphate pathway enzyme, 3-hexulose-6-phosphate synthase, from Aminomonas aminovorus C2A1 is adjacent to coding sequences that exhibit similarity to histidine biosynthesis enzymes. Antonie Van Leeuwenhoek 86:167-172
43. Thauer RK (1998) Biochemistry of methanogenesis: a tribute to Marjory Stephenson. Microbiology 144:2377-2406
44. Thauer RK, Kunow J (1995) Sulfate reducing Archaea. In: Clark N (ed) Biotechnology handbook. Plenum Publishing Company Ltd, London, pp 33-48
45. Verhees CH, Kengen SWM, Tuininga JE, Schut GJ, Adams MWW, De Vos WM, Van der Oost J (2003) The unique features of glycolytic pathways in archaea. Biochem J 375:231-246
46. Vorholt JA (2002) Cofactor-dependent pathways of formaldehyde oxidation in methylotrophic bacteria. Arch Microbiol 178:239-249
47. 2O in Ferroglobus placidus. Arch Microbiol 167:19-23
48. Vorholt JA, Chistoserdova L, Stolyar SM, Thauer RK, Lidstrom ME (1999) Distribution of tetrahydromethanopterin-dependent enzymes in methylotrophic bacteria and phylogeny of methenyl tetrahydromethanopterin cyclohydrolases. J Bacteriol 181:5750-5757
49. Vorholt JA, Marx CJ, Lidstrom ME, Thauer RK (2000) Novel formaldehyde-activating enzyme in Methylobacterium extorquens AM1 required for growth on methanol. J Bacteriol 182:6645-6650
50. Ward N, Larsen O, Sakwa J, Bruseth L, Khouri H, Durkin AS, Dimitrov G, Jiang LX, Scanlan D, Kang KH, Lewis M, Nelson KE, Methe B, Wu M, Heidelberg JF, Paulsen IT, Fouts D, Ravel J, Tettelin H, Ren QH, Read T, DeBoy RT, Seshadri R, Salzberg SL, Jensen HB, Birkeland NK, Nelson WC, Dodson RJ, Grindhaug SH, Holt I, Eidhammer I, Jonasen I, Vanaken S, Utterback T, Feldblyum TV, Fraser CM, Lillehaug JR, Eisen JA (2004) Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). Plos Biol 2:1616-1628
51. Yanase H, Ikeyama K, Mitsui R, Ra S, Kita K, Sakai Y, Kato N (1996) Cloning and sequence analysis of the gene encoding 3-hexulose-6-phosphate synthase from the methylotrophic bacterium, Methylomonas aminofaciens 77a, and its expression in Escherichia coli. FEMS Microbiol Lett 135:201-205
52. Yurimoto H, Hirai R, Yasueda H, Mitsui R, Sakai Y, Kato N (2002) The ribulose monophosphate pathway operon encoding formaldehyde fixation in a thermotolerant methylotroph, Bacillus brevis S1. FEMS Microbiol Lett 214:189-193