Phenylalanine catabolism in Archaeoglobus fulgidus VC-16

Archives of Microbiology

Volumn 195, Issue 12, 2013, Pages 781-797

  Parthasarathy, Anutthaman ^a,c   Kahnt, Jörg ^a   Chowdhury, Nilanjan Pal ^a,b   Buckel, Wolfgang ^a,b  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c Stanford University   (United States)

Author keywords

Archaeoglobus; Hyperthermophile; Phenylalanine

Indexed keywords

ACETYL COENZYME A SYNTHETASE; AROMATIC COMPOUND; ARYL PYRUVATE FERREDOXIN OXIDOREDUCTASE; BACTERIAL ENZYME; CAFFEIC ACID; FAMILY III COENZYME A TRANSFERASE; PHENYLALANINE; PHENYLALANINE 2 OXOGLUTARATE AMINOTRANSFERASE; PHENYLLACTATE DEHYDROGENASE; PHENYLPROPIONYL COENZYME A DEHYDROGENASE; RADICAL IRON SULFUR 3 PHENYLLACTYL COA DEHYDRATASE; SULFATE; TRYPTOPHAN; UNCLASSIFIED DRUG; ENZYME;

AMINO ACID METABOLISM; ARCHAEOGLOBUS FULGIDUS; ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; CATABOLISM; CLOSTRIDIUM; CONTROLLED STUDY; DECARBOXYLATION; FERMENTATION; NONHUMAN; PRIORITY JOURNAL; SULFATE REDUCER; CLASSIFICATION; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; OXIDATION REDUCTION REACTION; PHYLOGENY;

ARCHAEA; ARCHAEOGLOBUS; ARCHAEOGLOBUS FULGIDUS; ARCHAEOGLOBUS FULGIDUS DSM 4304; CLOSTRIDIA;

ARCHAEOGLOBUS FULGIDUS; ENZYMES; FERMENTATION; OXIDATION-REDUCTION; PHENYLALANINE; PHYLOGENY; SULFATES;

EID: 84890295793     PISSN: 03028933     EISSN: 1432072X     Source Type: Journal    
DOI: 10.1007/s00203-013-0925-3     Document Type: Article

References (81)

1. Atlas RM (1993) Handbook of microbiological media. CRC Press, Boca Raton, USA. http://nar.oxfordjournals.org/content/40/W1/W573
2. Boc A, Philippe H, Makarenkov V (2010) Inferring and validating horizontal gene transfer events using bipartition dissimilarity. Syst Biol 59:195-211
3. Boll M, Fuchs G (1995) Benzoyl-coenzyme A reductase (dearomatizing), a key enzyme of anaerobic aromatic metabolism: ATP dependence of the reaction, purification and some properties of the enzyme from Thauera aromatica strain K172. Eur J Biochem 234:921-933
4. Buckel W (1980a) Analysis of the fermentation pathways of clostridia using double labelled glutamate. Arch Microbiol 127:167-169
5. Buckel W (1980b) The reversible dehydration of (R)-2-hydroxyglutarate to (E)-glutaconate. Eur J Biochem 106:439-447
6. Buckel W (2001) Sodium ion-translocating decarboxylases. Biochim Biophys Acta 1505:15-27
7. Buckel W, Barker HA (1974) Two pathways of glutamate fermentation by anaerobic bacteria. J Bacteriol 117:1248-1260
8. Buckel W, Keese R (1995) One-electron redox reactions of CoASH esters in anaerobic bacteria - a mechanistic proposal. Ang Chem Intl Ed Eng 34:1502-1505
9. Buckel W, Semmler R (1983) Purification, characterisation and reconstitution of glutaconyl-CoA decarboxylase, a biotin-dependent sodium pump from anaerobic bacteria. Eur J Biochem 136:427-434
10. + translocating ferredoxin reduction. Biochim Biophys Acta 1827:94-113
11. Buckel W, Zhang J, Friedrich P, Parthasarathy A, Li H, Djurdjevic I, Dobbek H, Martins BM (2011) Enzyme catalyzed radical dehydrations of hydroxy acids. Biochim Biophys Acta 1824:1278-1290
12. Bult CJ, White O, Olsen GJ, Zhou L, Fleischmann RD, Sutton GG, Blake JA, FitzGerald FM, Clayton RA, Gocayne JD, Kerlavage AR, Dougherty BA, Tomb J-F, Adams MD, Reich CI, Overbeek R, Kirkness EF, Weinstock KG, Merrick JM, Glodek A, Scott JL, Geoghagen NSM, Weidman JF, Fuhrmann JL, Nguyen D, Utterback TR, Kelley JM, Peterson JD, Sadow PW, Hanna MC, Cotton MD, Roberts KM, Hurst MA, Kaine BP, Borodovsky M, Klenk H-P, Fraser CM, Smith HO, Woese CR, Venter JC (1996) Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273:1058-1073
13. Çinkaya I (2002) Substrat induzierte Radikalbildung in dem Eisen-Schwefel-Flavoenzym 4-Hydroxybutyryl-CoA-Dehydratase aus Clostridium aminobutyricum. Dissertation, Philipps University, Marburg
14. 1H-NMR studies of osmolyte turnover. Biochim Biophys Acta 1427:193-204
15. Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454-458
16. Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:10881-10890
17. Dauwe B, Middelburg JJ (1998) Amino acids and hexosamines as indicators of organic matter degradation state in North Sea sediments. Limnol Oceanogr 43:782-798
18. Dickert S (2001) Fermentation von L-phenylalanin in Clostridium sporogenes: Charakterisierung der Phenyllactat-Dehydratase. Dissertation, Philipps University, Marburg
19. Dickert S, Pierik AJ, Linder D, Buckel W (2000) The involvement of coenzyme A esters in the dehydration of (R)-phenyllactate to (E)-cinnamate by Clostridium sporogenes. Eur J Biochem 267:3874-3884
20. Dickert S, Pierik AJ, Buckel W (2002) Molecular characterization of phenyllactate dehydratase and its initiator from Clostridium sporogenes. Mol Microbiol 44:49-60
21. Djurdjevic I, Zelder O, Buckel W (2010) Method for the production of glutaconate. International patent application WO/2010/081885
22. Djurdjevic I, Zelder O, Buckel W (2011) Production of glutaconic acid in a recombinant Escherichia coli strain. Appl Env Microbiol 77:320-322
23. D'Ordine RL, Tonge PJ, Carey PR, Anderson VE (1994) Electronic rearrangement induced by substrate analog binding to the enoyl-CoA hydratase active site: evidence for substrate activation. Biochemistry 33:12635-12643
24. Gerhardt A, Çinkaya I, Linder D, Huisman G, Buckel W (2000) Fermentation of 4-aminobutyrate by Clostridium aminobutyricum: cloning of two genes involved in the formation and dehydration of 4-hydroxybutyryl-CoA. Arch Microbiol 174:189-199
25. Ghisla S, Thorpe C (2004) Acyl-CoA dehydrogenases. A mechanistic overview. Eur J Biochem 271:494-508
26. Gokarn RR, Selifonova OV, Jessen HJ, Gort SJ, Selmer T, Buckel W (2004) 3-Hydroxypropionic acid and other organic compounds. US Patent Application 20040076982, Cargill Incorporated, Minneapolis, MN, USA
27. Graupner M, Xu H, White RH (unpublished) In: Roberts MF (2005) Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst Open Access J 1:5
28. Grein F, Ramos AR, Venceslau SS, Pereira IAC (2013) Unifying concepts in anaerobic respiration: Insights from dissimilatorysulfur metabolism. Biochim Biophys Acta 1827:145-160
29. Habicht KS, Salling L, Thamdrup B, Canfield DE (2005) Effect of low sulfate concentrations on lactate oxidation and isotope fractionation during sulfate reduction by Archaeoglobus fulgidus Strain Z. Appl Env Microbiol 71:3770-3777
30. Hans M, Sievers J, Müller U, Bill E, Vorholt JA, Linder D, Buckel W (1999) 2-Hydroxyglutaryl-CoA dehydratase from Clostridium symbiosum. Eur J Biochem 265:404-414
31. Hartzell PL, Reed DW (2006) The genus Archaeoglobus. Prokaryotes 3:82-100
32. Havir EA, Hanson KR (1970) l-phenylalanine ammonia-lyase (potato tubers). Methods Enzymol 17A:575-581
33. Heider J (2001) A new family of CoA-transferases. FEBS Lett 509:345-349
34. Hemmi H, Takahashi Y, Shibuya K, Nakayama T, Nishino T (2005) Menaquinone-specific prenyl reductase from the hyperthermophilic archaeon Archaeoglobus fulgidus. J Bacteriol 187:1937-1944
35. Herrmann G, Selmer T, Jessen HJ, Gokarn RR, Selifonova O, Gort SJ, Buckel W (2005) Two beta-alanyl-CoA:ammonia lyases in Clostridium propionicum. FEBS J 272:813-821
36. Herrmann G, Jayamani E, Mai G, Buckel W (2008) Energy conservation via electron-transferring flavoprotein in anaerobic bacteria. J Bacteriol 190:784-791
37. Hetzel M, Brock M, Selmer T, Pierik AJ, Golding BT, Buckel W (2003) Acryloyl-CoA reductase from Clostridium propionicum, an enzyme complex of propionyl-CoA dehydrogenase and electron-transferring flavoprotein. Eur J Biochem 270:902-910
38. Hodgins DS (1971) Yeast phenylalanine ammonia-lyase. Purification, properties, and the identification of catalytically essential dehydroalanine. J Biol Chem 246:2977-2985
39. Holmes DE, Risso C, Smith JA, Lovely DE (2011) Anaerobic oxidation of benzene by the hyperthermophilic archaeon Ferroglobus placidus. Appl Env Microbiol 17:5926-5933
40. Hufnagel P, Rabus R (2006) Mass spectrometric identification of proteins in complex post-genomic projects. Soluble proteins of the metabolically versatile, denitrifying 'Aromatoleum' sp. strain EbN1. J Mol Microbiol Biotech 11:53-81
41. Jayamani E (2008) A unique way of energy conservation in glutamate fermenting clostridia. Dissertation, Philipps Universität, Marburg
42. Kandasamy V, Vaidyanathan H, Djurdjevic I, Jayamani E, Ramachandran KB, Buckel W, Jayaraman G, Ramalingam S (2013) Engineering Escherichia coli with acrylate pathway genes for propionic acid synthesis and its impact on mixed-acid fermentation. Appl Microbiol Biotechnol 97:1191-1200
43. Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511-518
44. Kawaguchi A, Yoshimura T, Okuda S (1981) A new method for the preparation of acyl-CoA thioesters. J Biochem 89:337-339
45. Kim J, Hetzel M, Boiangiu CD, Buckel W (2004) Dehydration of (R)-2-hydroxyacyl-CoA to enoyl-CoA in the fermentation of alpha-amino acids by anaerobic bacteria. FEMS Microbiol Rev 28:455-468
46. Kim J, Darley DJ, Buckel W, Pierik AJ (2008) An allylic ketyl radical intermediate in clostridial amino-acid fermentation. Nature 452:239-242
47. Klees AG, Linder D, Buckel W (1992) 2-Hydroxyglutaryl-CoA dehydratase from Fusobacterium nucleatum (subsp. nucleatum): an iron-sulfur flavoprotein. Arch Microbiol 158:294-301
48. Klenk H-P, 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, Peterson S, Reich CI, McNeil LK, Badger JH, Glodek A, Zhou L, Overbeek R, Gocayne JD, Weidman JF, McDonald L, Utterback T, Cotton MD, Spriggs T, Artiach P, Kaine BP, Sykes SM, Sadow PW, D'Andrea KP, Bowman C, Fujii C, Garland SC, Mason TM, Olsen GJ, Fraser CM, Smith HO, Woese CR, Venter JC (1997) The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 390:364-370
49. Knauer SH, Buckel W, Dobbek H (2011) Structural basis for reductive radical formation and electron recycling in (R)-2-hydroxyisocaproyl-CoA dehydratase. J Am Chem Soc 133:4342-4347
50. Knauer SH, Buckel W, Dobbek H (2012) On the ATP-dependent activation of the radical enzyme (R)-2-hydroxyisocaproyl-CoA dehydratase. Biochemistry 51:6609-6622
51. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
52. Lee C (1988) Amino acid and amine biogeochemistry in marine particulate material and sediments. In: Blackburn TH, Sørensen J (eds) Nitrogen cycling in coastal marine environments. Wiley, New York, pp 125-141
53. Lehman TC, Thorpe C (1990) Alternate electron acceptors for medium-chain acyl-CoA dehydrogenase: use of ferricenium salts. Biochemistry 29:10594-10602
54. Li F, Hinderberger J, Seedorf H, Zhang J, Buckel W, Thauer RK (2008) Coupled ferredoxin and crotonyl Coenzyme A (CoA) Reduction with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex from Clostridium kluyveri. J Bacteriol 190:843-850
55. Lim S, Springstead JR, Yu M, Bartkowski W, Schröder I, Monbouquette HG (2004) A thermostable shikimate 5-dehydrogenase from the archaeon Archaeoglobus fulgidus. FEMS Microbiol Lett 238:101-106
56. Lim S, Springstead JR, Yu M, Bartkowski W, Schröder I, Monbouquette HG (2009) Characterization of a key trifunctional enzyme for aromatic amino acid biosynthesis in Archaeoglobus fulgidus. Extremophiles 13:191-198
57. MacKellar WJ, Wiederanders RS, Tallman DE (1978) Indirect determination of sulfate ion by spectrophotometric titration of excess barium (II) ion with ethylenediaminetetraacetate. Anal Chem 50:160-163
58. Mai X, Adams MWW (1994) Indolepyruvate ferredoxin oxidoreductase from the hyperthermophilic archaeon Pyrococcus furiosus: a new enzyme involved in peptide fermentation. J Biol Chem 269:16726-16732
59. +-dependent (R)-2-hydroxyglutarate dehydrogenase from Acidaminococcus fermentans. FEBS J 272:269-281
60. 2- from equilibrium reactions with flavodoxins, methyl viologen and hydrogen plus hydrogenase. Eur J Biochem 85:535-547
61. Mehta PK, Hale TI, Christen P (1989) Evolutionary relationships among aminotransferases: tyrosine aminotransferase, histidinol-phosphate aminotransferase, and aspartate aminotransferase are homologous proteins. Eur J Biochem 186:249-253
62. Möllering H, Wahlefeld, AW, Michal G (1974) Visualisierung NAD(P)-abhängiger Reaktionen. In: Bergmeyer HU (ed) Methoden der enzymatischen Analyse. Verlag Chemie, Weinheim/Bergstrasse, Germany, pp 145-153
63. Musfeldt M, Schönheit P (2002) Novel type of ADP-forming acetyl coenzyme A synthetase in hyperthermophilic archaea: heterologous expression and characterization of isoenzymes from the sulfate reducer, Archaeoglobus fulgidus and the methanogen Methanococcus jannaschii. J Bacteriol 184:636-644
64. Nelson KE, Clayton RA, Gill SR, Gwinn ML, Dodson RJ, Haft DH, Hickey EK, Peterson JD, Nelson WC, Ketchum KA, McDonald L, Utterback TR, Malek JA, Linher KD, Garrett MM, Stewart AM, Cotton MD, Pratt MS, Phillips CA, Richardson D, Heidelberg J, Sutton GG, Fleischmann RD, Eisen JA, White O, Salzberg SL, Smith HO, Venter JC, Fraser CM (1999) Evidence for lateral gene transfer between archaea and bacteria from genome sequence of Thermotoga maritima. Nature 399:323-329
65. Onuffer JJ, Kirsch JF (1995) Redesign of the substrate specificity of Escherichia coli aspartate aminotransferase to that of Escherichia coli tyrosine aminotransferase by homology modeling and site-directed mutagenesis. Protein Sci 4:1750-1757
66. Parthasarathy A, Buckel W, Smith DM (2010) On the thermodynamic equilibrium between (R)-2-hydroxyacyl-CoA and 2-enoyl-CoA. FEBS J 277:1738-1746
67. Parthasarathy A, Pierik AJ, Kahnt J, Zelder O, Buckel W (2011) Substrate specificity of 2-hydroxyglutaryl-CoA dehydratase from Clostridium symbiosum: towards a bio-based production of adipic acid. Biochemistry 50:3540-3550
68. Phillips NW (1984) Role of different microbes and substrates as potential food suppliers of specific essential nutrients to marine detritivores. Bull Mar Sci 35:283-298
69. Riddles PW, Blakeley RL, Zerner B (1979) Ellman's reagent: 5,5′-dithiobis(2-nitrobenzoic acid)-a reexamination. Anal Biochem 94:75-81
70. Schröder I, Vadas A, Johnson E, Lim S, Monbouquette HG (2004) A novel archaeal alanine dehydrogenase homologous to ornithine cyclodeaminase and mu-crystallin. J Bacteriol 186:7680-7689
71. Simon EJ, Shemin D (1953) The preparation of S-succinyl Coenzyme A. J Am Chem Soc 75:2520-2520
72. Steen IH, Hvoslef H, Lien T, Birkeland N-K (2001) Isocitrate dehydrogenase, malate dehydrogenase, and glutamate dehydrogenase from Archaeoglobus fulgidus. Methods Enzymol 331:13-26
73. Stenmark P, Gurmu D, Nordlund P (2004) Crystal structure of CaiB, a Type-III CoA transferase in carnitine metabolism. Biochemistry 43:13996-14003
74. Stetter KO (1988) Archaeoglobus fulgidus gen. nov., sp. nov.: a new taxon of extremely thermophilic Archaebacteria. Syst Appl Microbiol 10:172-173
75. Stetter KO, Lauerer G, Thomm M, Neuner A (1987) Isolation of extremely thermophilic sulfate reducers: evidence for a novel branch of archaebacteria. Science 236:822-824
76. Stetter KO, Fiala G, Huber G, Huber R, Segerer A (1990) Hyperthermophilic microorganisms. FEMS Microbiol Rev 75:117-124
77. Tamannaei A (2003) Untersuchungen zum Katalysemechanismus der 2-Hydroxyglutaryl-CoA-Dehydratase aus Fusobacterium nucleatum. Diploma thesis, Philipps-Universität, Marburg
78. Thamer W, Cirpus I, Hans M, Pierik AJ, Selmer T, Bill E, Linder D, Buckel W (2003) A two [4Fe-4S]-cluster-containing ferredoxin as an alternative electron donor for 2-hydroxyglutaryl-CoA dehydratase from Acidaminococcus fermentans. Arch Microbiol 179:197-204
79. Wöhlbrand L, Jacob JH, Kube M, Mussmann M, Jarling R, Beck A, Amann R, Wilkes H, Reinhardt R, Rabus R (2013) Complete genome, catabolic sub-proteomes and key metabolites of Desulfobacula toluolica ol2, a marine, aromatic compound degrading, sulphate-reducing bacterium. Environ Microbiol 15:1334-1355
80. Zhao K, Chai X, Marmorstein R (2003) Structure of a Sir2 Substrate, Alba, reveals a mechanism for deacetylation-induced enhancement of DNA binding. J Biol Chem 278:26071-26077
81. Ziegenhorn J, Senn M, Bücher T (1976) Molar absorptivities of beta-NADH and beta-NADPH. Clin Chem 22:151-160