Substrate specificities and electron paramagnetic resonance properties of benzylsuccinate synthases in anaerobic toluene and m-xylene metabolism

Archives of Microbiology

Volumn 181, Issue 2, 2004, Pages 155-162

  Verfürth, Knut ^a   Pierik, Antonio J ^b   Leutwein, Christina ^a   Zorn, Susanne ^a   Heider, Johann ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Anaerobic metabolism; Azoarcus; Benzylsuccinate synthase; Cresols; Electron paramagnetic spectroscopy; Glycyl radical enzyme; Substrate specificity; Thauera; Toluene; Xylenes

Indexed keywords

AROMATIC HYDROCARBON; BACTERIAL ENZYME; BENZYLSUCCINATE SYNTHASE; FUMARIC ACID; METHYL GROUP; SYNTHETASE; TOLUENE; UNCLASSIFIED DRUG; XYLENE;

ADDITION REACTION; ARTICLE; AZOARCUS; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; CATALYSIS; DEGRADATION; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME PURIFICATION; ENZYME SPECIFICITY; ISOMER; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; THAUERA AROMATICA;

ANAEROBIOSIS; AZOARCUS; BIODEGRADATION, ENVIRONMENTAL; CARBON-CARBON LYASES; CRESOLS; ELECTRON SPIN RESONANCE SPECTROSCOPY; SUBSTRATE SPECIFICITY; SUCCINATES; THAUERA; TOLUENE; XYLENES;

AZOARCUS; AZOARCUS SP.; BACTERIA (MICROORGANISMS); NEGIBACTERIA; THAUERA; THAUERA AROMATICA;

EID: 10744221011     PISSN: 03028933     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00203-003-0642-4     Document Type: Article

References (49)

1. Achong GR, Rodriguez AM, Spormann AM (2001) Benzylsuccinate synthase of Azoarcus sp. strain T: cloning, sequencing, transcriptional organization, and its role in anaerobic toluene and m-xylene mineralization. J Bacteriol 183:6763-6770
2. Anders A, Kaetzke A, Kämpfer P, Ludwig W, Fuchs G (1995) Taxonomic position of aromatic degrading denitrifying pseudomonad strains K172 and KB740 and their description as new members of the genera Thauera, T. aromatica sp. nov., and Azoarcus, A. evansii sp. nov., respectively, members of the beta subclass of Proteobacteria. Int J Syst Bacteriol 45:327-333
3. Annweiler E, Materna A, Safinowski M, Kappler A, Richnow HH, Michaelis W, Meckenstock RU (2000) Anaerobic degradation of 2-methylnaphthalene by a sulfate-reducing enrichment culture. Appl Environ Microbiol 66:5329-5333
4. Becker A, Fritz-Wolf K, Kabsch W, Knappe J, Schultz S, Wagner AFV (1999) Structure and mechanism of the glycyl radical enzyme pyruvate formate-lyase. Nat Struct Biol 6:969-975
5. Beller HR, Spormann AM (1997a) Anaerobic activation of toluene and o-xylene by addition to fumarate in denitrifying strain T. J Bacteriol 179:670-676
6. Beller HR, Spormann AM (1997b) Benzylsuccinate formation as a means of anaerobic toluene activation by sulfate-reducing strain PRTOL1. Appl Environ Microbiol 63:3729-3731
7. Beller HR, Spormann AM (1998) Analysis of the novel benzylsuccinate synthase reaction for anaerobic toluene activation based on structural studies of the product. J Bacteriol 180:5454-5457
8. Beller HR, Spormann AM (1999) Substrate range of benzylsuccinate synthase from Azoarcus sp. strain T. FEMS Microbiol Lett 178:147-153
9. Beller HR, Edwards EA (2000) Anaerobic toluene activation by benzylsuccinate synthase in a highly enriched methanogenic culture. Appl Environ Microbiol 67:5503-5509
10. Biegert T, Fuchs G, Heider J (1996) Evidence that oxidation of toluene in the denitrifying bacterium Thauera aromatica is initiated by formation of benzylsuccinate from toluene and fumarate. Eur J Biochem 238:661-668
11. 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
12. Brudvig GW (1995) Electron paramagnetic resonance spectroscopy. Methods Enzymol 246:536-554
13. Coschigano PW, Wehrman TS, Young LY (1998) Identification and analysis of genes involved in anaerobic toluene metabolism by strain T1: putative role of a glycine free radical. Appl Environ Microbiol 64:1650-1656
14. Dolfing J, Zeyer J, Binder-Eicher P, Schwarzenbach RP (1990) Isolation and characterisation of a bacterium that mineralises toluene in the absence of molecular oxygen. Arch Microbiol 154:336-341
15. Duboc-Toia C, Hassan AK, Mulliez E, Ollagnier-de Choudens S, Fontecave M, Leutwein C, Heider J (2003) Very high field EPR studies of glycyl radical enzymes. J Amer Chem Soc 125:38-39
16. Heider J, Spormann AM, Beller HR, Widdel F (1999) Anaerobic bacterial metabolism of hydrocarbons. FEMS Microbiol Rev 22:459-473
17. Hermuth K, Leuthner B, Heider J (2002) Operon structure and expression of the genes for benzylsuccinate synthase in Thauera aromatica strain K172. Arch Microbiol 177:132-138
18. Kane SR, Beller HR, Legier TC, Anderson RT (2002) Biochemical and genetic evidence of benzylsuccinate synthase in toluene-degrading, ferric iron-reducing Geobacter metallireducens. Biodegradation 13:149-154
19. Knappe J, Sawers G (1990) A radical-chemical route to acetyl-CoA: the anaerobically induced pyruvate formate-lyase system of Escherichia coli. FEMS Micobiol Rev 75:383-398
20. Kniemeyer O, Fischer T, Wilkes H, Glockner FO, Widdel F (2003) Anaerobic degradation of ethylbenzene by a new type of sulfate-reducing bacterium. Appl Environ Microbiol 69:760-768
21. Krieger CJ, Beller HR, Reinhard M, Spormann AM (1999) Initial reactions in anaerobic oxidation of m-xylene by the denitrifying bacterium Azoarcus sp. strain T. J Bacteriol 181:6403-6410
22. Krieger CJ, Roseboom W, Albracht SPJ, Spormann AM (2001) A stable organic free radical in anaerobic benzylsuccinate synthase of Azoarcus sp. strain T. J Biol Chem 276:12924-12927
23. Kube M, Heider J, Hufnagel P, Kühner S, Beck A, Reinhardt R, Rabus R (2004) Genes involved in the anaerobic degradation of toluene in a denitrifying bacterium, strain EbN1. Arch Microbiol (in press)
24. Leuthner B, Leutwein C, Schulz H, Hörth P, Haehnel W, Schiltz E, Schägger H, Heider J (1998) Biochemical and genetic characterisation of benzylsuccinate synthase from Thauera aromatica: a new glycyl radical enzyme catalysing the first step in anaerobic toluene metabolism. Mol Microbiol 28:615-628
25. Leuthner B, Heider J (2000) Anaerobic toluene catabolism of Thauera aromatica: the bbs operon codes for the enzymes of β-oxidation of the intermediate benzylsuccinate. J Bacteriol 182:272-277
26. Leutwein C, Heider J (1999) Anaerobic toluene catabolic pathway in denitrifying Thauera aromatica: activation and β-oxidation of the first intermediate, (R)-(+)-benzylsuccinate. Microbiology 145:3265-3271
27. Leutwein C, Heider J (2001) Succinyl-CoA: (R)-benzylsuccinate CoA-transferase: an enzyme of the anaerobic toluene catabolic pathway in denitrifying bacteria. J Bacteriol 183:4288-4295
28. Leutwein C, Heider J (2002) (R)-Benzylsuccinyl-CoA dehydrogenase from Thauera aromatica: a new acyl-CoA dehydrogenase involved in anaerobic toluene catabolism. Arch Microbiol 178:517-524
29. Logan DT, Andersson J, Sjöberg B-M, Nordlund P (1999) A glycyl radical site in the crystal structure of a class III ribonucleotide reductase. Science 283:1499-1504
30. Meckenstock RU (1999) Fermentative toluene degradation in anaerobic defined syntrophic cocultures. FEMS Microbiol Lett 177:67-73
31. Meckenstock RU, Annweiler E, Michaelis W, Richnow HH, Schink B (2000) Anaerobic naphthalene degradation by a sulfate-reducing enrichment culture. Appl Environ Microbiol 66:2743-2747
32. Müller JA, Galushko AS, Kappler A, Schink B (1999) Anaerobic degradation of m-cresol by Desulfobacterium cetonicum is initiated by formation of 3-hydroxybenzylsuccinate. Arch Microbiol 172:287-294
33. Müller JA, Galushko AS, Kappler A, Schink B (2001) Initiation of anaerobic degradation of p-cresol by formation of 4-hydroxybenzylsuccinate in Desulfobacterium cetonicum. J Bacteriol 183:752-757
34. Mulliez E, Fontecave M, Gaillard J, Reichard P (1993) An iron-sulfur center and a free radical in the active anaerobic ribonucleotide reductase of Escherichia coli. J Biol Chem 268:2296-2299
35. Parast CV, Wong KK, Lewisch SA, Kozarich JW, Peisach J, Magliozzo RS (1995) Hydrogen exchange of the glycyl radical of pyruvate formate-lyase is catalysed by cysteine 419. Biochemistry 34:2393-2399
36. Rabus R, Heider J (1998) Initial reactions of anaerobic metabolism of alkylbenzenes in denitrifying and sulfate-reducing bacteria. Arch Microbiol 170:377-384
37. Rabus R, Wilkes H, Behrends A, Armstroff A, Fischer T, Pierik AJ, Widdel F (2001) Anaerobic initial reaction of n-alkanes in a denitrifying bacterium: evidence for (1-methylpentyl)succinate as initial product and for involvement of an organic radical in n-hexane metabolism. J Bacteriol 183:1707-1715
38. Raynaud C, Sarcabal P, Meynial-Salles I, Croux C, Soucaille P (2003) Molecular characterisation of the 1,3-propanediol (1,3-PD) operon of Clostridium butyricum. Proc Natl Acad Sci USA 100:5010-5015
39. Reddy SG, Wong KK, Parast CV, Peisach J, Magliozzo RS, Kozarich JW (1998) Dioxygen inactivation of pyruvate formate-lyase: EPR-evidence for the formation of protein-based sulfinyl-and peroxyl-radicals. Biochemistry 37:558-563
40. Selmer T, Andrei P (2001) p-Hydroxyphenylacetate decarboxylase from Clostridium difficile. A novel glycyl radical enzyme catalysing the formation of p-cresol. Eur J Biochem 268:1363-1372
41. Seyfried B, Glod G, Schocher R, Tschech A, Zeyer J (1994) Initial reactions in the anaerobic oxidation of toluene and m-xylene by denitrifying bacteria. Appl Environ Microbiol 157:4047-4052
42. Sun X, Ollagnier S, Schmidt PP, Atta M, Mulliez E, Lepape L, Eliasson R, Gräslund A, Fontecave M, Reichard P, Sjöberg B-M (1996) The free radical of the anaerobic ribonucleotide reductase from Escherichia coli is at glycine 681. J Biol Chem 271:6827-6831
43. Torrents E, Girbe Buist AL, Eliasson R, Kok J, Gibert I, Gräslund A, Reichard P (2000) The anaerobic (class III) ribonucleotide reductase from Lactococcus lactis: catalytic properties and allosteric regulation of the pure enzyme system. J Biol Chem 275:2463-2471
44. Tschech A, Fuchs G (1987) Anaerobic degradation of phenol by pure cultures of newly isolated denitrifying pseudomonads. Arch Microbiol 148:213-217
45. Unkrig V, Neugebauer FA, Knappe J (1989) The free radical of pyruvate formate-lyase. Characterisation by EPR spectroscopy and involvement in catalysis as studied with the substrate-analogue hypophosphite. Eur J Biochem 184:723-728
46. Wagner AFV, Frey M, Neugebauer FA, Schäfer W, Knappe J (1992) The free radical in pyruvate formate lyase is located on glycine-734. Proc Natl Acad Sci USA 89:996-1000
47. Weil JA, Bolton JR, Wertz JE (1994) Electron paramagnetic resonance: elementary theory and practical applications. Wiley, New York
48. Young P, Andersson J, Sahlin M, Sjoberg B-M (1996) Bacteriophage T4 anaerobic ribonucleotide reductase contains a stable glycyl radical at position 580. J Biol Chem 271:20770-20775
49. Zengler K, Heider J, Rosselló-Mora R, Widdel F (1999) Phototrophic utilisation of toluene under anoxic conditions by a new strain of Blastochloris viridis. Arch Microbiol 172:204-212