Anaerobic metabolism of aromatic compounds

Annals of the New York Academy of Sciences

Volumn 1125, Issue , 2008, Pages 82-99

  Fuchs, Georg ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Anaerobes; Aromatic metabolism; Benzoate; Benzoyl CoA pathway; Benzoyl CoA reductase; Oxygenases; Phenol; Toluene

Indexed keywords

ACYL COENZYME A; ADENOSINE TRIPHOSPHATE; AROMATIC COMPOUND; BENZOYL COENZYME A REDUCTASE; OXIDOREDUCTASE; OXYGEN; OXYGENASE; UNCLASSIFIED DRUG;

AEROBE; ANAEROBIC METABOLISM; CONFERENCE PAPER; HYDROLYSIS; MOLECULE; NONHUMAN; PHOTOTROPH;

BACTERIA (MICROORGANISMS);

EID: 41349085209     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1196/annals.1419.010     Document Type: Conference Paper

References (103)

1. HAYAISHI, O. 1994. Tryptophan, oxygen, and sleep. Annu. Rev. Biochem. 63: 1-24.
2. DAGLEY, S. 1978. Pathway for the utilization of organic growth substrates. In The Bacteria, Vol. 6. L.N. Ornston & J.R. Sokatch, Eds.: 305-388. New York: Academic Press.
3. DAGLEY, S. 1986. Biochemistry of aromatic hydrocarbon degradation in pseudomonads. In The Bacteria, Vol. 10. J.R. Sokatch & L.N. Ornston, Eds.: 527-555. New York: Academic Press.
4. HARAYAMA, S., M. KOK & E.L. NEIDLE. 1992. Functional and evolutionary relationships among diverse oxygenases. Annu. Rev. Microbiol. 446: 565-601.
5. DAGLEY, S. 1971. Catabolism of aromatic compounds by microorganisms. Adv. Microbial. Physiol. 6: 1-76.
6. HARWOOD, C.S. & R.E. PARALES. 1996. The β-ketoadipate pathway and the biology of self identity. Annu. Rev. Microbiol. 50: 553-590.
7. OLIVERA, E.R., B. MINAMBERS, B. GARCIA, et al. 1998. Molecular characterization of the phenylacetic acid catabolic pathway in Pseudomonas putida U: the phenylacetyl-coenzyme A catabolon. Proc. Natl. Acad. Sci. USA. 95: 6419-6424.
8. FERRANDEZ, A., B. MINAMBERS, B. GARCIA, et al. 1998. Catabolism of phenylacetic acid in Escherichia coli. J. Biol. Chem. 273: 25974-25986.
9. DIAZ, E., A. FERRANDEZ, M.A. PRIETO & J.L. GARCIA. 2001. Biodegradation of aromatic compounds by Escherichia coli. Microbiol. Mol. Biol. Rev. 65: 523-569.
10. MOHAMED, M.E., W. ISMAIL, J. HEIDER & G. FUCHS. 2002. Aerobic metabolism of phenylacetic acids in Azoarcus evansii. Arch. Microbiol. 178: 180-192.
11. LUENGO, J.M., J.L. GARCÍA & E.R. OLIVERA. 2001. The phenylacetyl-CoA catabolon: a complex catabolic unit with broad biotechnological applications. Mol. Microbiol. 39: 1434-1442.
12. ROST, R., S. HAAS, E. HAMMER, et al. 2002. Molecular analysis of aerobic phenylacetate degradation in Azoarcus evansii. Mol. Genet. Genomics 267: 656-663.
13. ISMAIL, W., M.E. MOHAMED, B.L. WANNER, et al. 2003. Functional genomics by NMR spectroscopy: phenylacetate catabolism in Escherichia coli. Eur. J. Biochem. 270: 3047-3054.
14. BARTOLOME-MARTIN, D., E.V. MARTINEZ- GARCIA, J. MASCARAQUE, et al. 2004. Characterization of a second functional gene cluster for the catabolism of phenylacetic acid in Pseudomonas sp. Strain Y2. Gene 341: 167-179.
15. ZAAR, A., W. EISENREICH, A. BACHER & G. FUCHS. 2001. A novel pathway of aerobic benzoate catabolism in the bacteria Azoarcus evansii and Bacillus stearothermophilus. J. Biol. Chem. 276: 24997-25004.
16. ZAAR, A., J. GESCHER, W. EISENREICH, et al. 2004. New enzymes in aerobic benzoate metabolism in Azoarcus evansii. Benzoyl-CoA oxygenase. Mol. Microbiol. 54: 223-238.
17. GESCHER, J., W. EISENREICH, J. WOERTH, et al. 2005. Aerobic benzoyl-coenzyme A catabolic pathway in Azoarcus evansii: studies on the non-oxygenolytic ring cleavage enzyme. Mol. Microbiol. 56: 1586-1600.
18. GESCHER, J., W. ISMAIL, E. OELGESCHLAEGER, et al. 2006. Aerobic benzoyl-coenzyme A (CoA) catabolic pathway in Azoarcus evansii: conversion of ring cleavage product by 3,4-dehydroadipyl-CoA semialdehyde dehydrogenase. J. Bacteriol. 188: 2919-2927.
19. BUDER, R. & G. FUCHS. 1989. 2-Aminobenzoyl CoA monooxygenase/reductase, a novel type of flavoenzyme. Purification and some properties of the enzyme. Eur. J. Biochem. 185: 629-635.
20. BUDER, R., K. ZIEGLER, G. FUCHS, et al. 1989. 2-Aminobenzoyl-CoA monooxygenase/reductase, a novel type of flavoenzyme. Studies on the stoichiometry and the course of the reaction. Eur. J. Biochem. 185: 637-643.
21. LANGKAU, B., S.GHISLA, R. BUDER & G. FUCHS. 1990. 2-Aminobenzoyl-CoA monooxygenase/reductase, a novel type of flavoenzyme. Identification of the reaction products. Eur. J. Biochem. 191: 365-371.
22. LANGKAU, B., P. VOCK, V. MASSEY, et al. 1995. 2-Aminobenzoyl-CoA monooxygenase/reductase. Evidence for two distinct loci catalyzing substrate monooxygenation and hydrogenation. Eur. J. Biochem. 230: 676-685.
23. HARTMANN, S., C.HULTSCHIG, W. EISENREICH, et al. 1999. NIH-shift in flavin dependent monooxygenation. Mechanistic studies with 2-aminobenzoyl-CoA monooxygenase/reductase. Proc. Natl. Acad. Sci. USA 96: 7831-7836.
24. SCHÜHLE, C., M. JAHN, S. GHISLA & G. FUCHS. 2001. Two similar gene clusters coding for the enzymes of a new type of aerobic 2-aminobenzoate (anthranilate)metabolism in the bacterium Azoarcus evansii. J. Bacteriol. 183: 5268-5278.
25. EVANS, W.C. 1977. Biochemistry of the bacterial catabolism of aromatic compounds in anaerobic environments. Nature 270: 17-22.
26. DUTTON, P.L. & W.C. EVANS. 1978. Metabolism of aromatic compounds by Rhodospirillaceae. In The Photosynthetic Bacteria. R.K. Clyton & W.R. Sistrom, Eds.: 719-726. New York: Plenum Press.
27. KAISER, J.P. & K.W. HANSELMANN. 1982. Aromatic chemicals through anaerobic microbial conversion of lignin monomers. Experientia 38: 167-175.
28. SLEAT, R. & J.P. ROBINSON. 1984. The bacteriology of anaerobic degradation of aromatic compounds. J. Appl. Bacteriol. 57: 381-394.
29. YOUNG, L.Y. 1984. Anaerobic degradation of aromatic compounds. In Microbial Degradation of Organic Compounds. D.T. Gibson, Ed.: 487-523. New York: Marcel Dekker.
30. GIBSON, D.T. & V. SUBRAMANIAN. 1984. Microbial degradation of aromatic compounds. In Microbial Degradation of Organic Compounds.D.T.Gibson, Ed.: 181-252. New York: Marcel Dekker.
31. BERRY, D.F., A.J. FRANCIS & J.M. BOLLAG. 1987. Microbial metabolism of homocyclic and heterocyclic aromatic compounds under anaerobic conditions.Microbiol. Rev. 51: 43-59.
32. EVANS, W.C. & G. FUCHS. 1988. Anaerobic degradation of aromatic compounds. Annu. Rev. Microbiol. 42: 289-317.
33. SCHINK, B. & A. TSCHECH. 1988. Fermentative degradation of aromatic compounds. In Microbial Metabolism and the Carbon Cycle. S.R. Hagedorn, R.S. Hanson & D.A.Kunz, Eds.: 213-226. Chur, Switzerland: Harwood Academic Publishers.
34. HEIDER, J. & G. FUCHS. 1997. Anaerobic metabolism of aromatic compounds. Eur. J. Biochem. 243: 577-596.
35. HEIDER, J. & G. FUCHS. 1997. Microbial anaerobic aromatic metabolism. Anaerobe 3: 1-22.
36. HARWOOD, C.S., G. BURCHHARDT, H. HERMANN & G. FUCHS. 1999. Anaerobic metabolism of aromatic compounds via the benzoyl-coenzyme A pathway. FEMS Microbiol. Rev. 22: 439-458.
37. BOLL, M., G. FUCHS & J. HEIDER. 2002. Anaerobic oxidation of aromatic compounds and hydrocarbons. Curr. Opin. Biol. Chem. 6: 604-611.
38. SCHINK, B., B. PHILIPP & J. MÜLLER. 2000. Anaerobic degradation of phenolic compounds. Naturwissenschaften 87: 12-23.
39. GIBSON, J. & C.S. HARWOOD. 2002. Metabolic diversity in aromatic compound utilization by anaerobic microbes. Annu. Rev. Microbiol. 56: 345-369.
40. BOLL, M., G. FUCHS & J. HEIDER. 2002. Anaerobic metabolism of aromatic compounds. Curr. Opin. Chem. Biol. 6: 604-611.
41. BOLL, M. & G. FUCHS. 2005. Unusual reactions involved in the anaerobic metabolism of phenolic compounds. Biol. Chem. 386: 989-997.
42. BOLL, M. 2005. Key enzymes in the anaerobic aromatic metabolism catalysing Birch-like reductions. Biochim. Biophys. Acta 1707: 34-50.
43. HARUKI, E. 1982. Organic syntheses with carbon dioxide. In Organic and Bio-organic Chemistry of Carbon Dioxide. S. Inoue & N. Yamazaki, Eds.: 5-78. New York: Halsted Press.
44. KOSUGI, Y., Y. IMAOKA, F. GOTOH, et al. 2003. Carboxylations of alkali metal phenoxides with carbon dioxide. Org. Biomol. Chem. 1: 817-821.
45. TSCHECH, A. & G. FUCHS. 1987. Anaerobic degradation of phenol by pure cultures of newly isolated denitrifying pseudomonads. Arch. Microbiol. 148: 213-217.
46. 2 and 4-hydroxybenzoate. Arch. Microbiol. 152: 594-599.
47. LACK, A. & G. FUCHS. 1994. Evidence that phenol phosphorylation to phenylphosphate is the first step in anaerobic phenol metabolism in a denitrifying Pseudomonas sp. Arch. Microbiol. 161: 132-139.
48. SCHMELING, S., A. NARMANDAKH, O. SCHMITT, et al. 2004. Phenylphosphate synthase: a new phosphotransferase catalyzing the first step in anaerobic phenol metabolism in Thauera aromatica. J. Bacteriol. 186: 8044-8057.
49. LACK, A. & G. FUCHS. 1992. Carboxylation of phenylphosphate by phenol carboxylase, an enzyme system of anaerobic phenol metabolism. J. Bacteriol. 174: 3629-3636.
50. 2: 4-hydroxybenzoate isotope exchange reaction. Eur. J. Biochem. 197: 473-479.
51. SCHÜHLE, K. & G. FUCHS. 2004. Phenylphosphate carboxylase: a new C-C lyase involved in anaerobic phenol metabolism in Thauera aromatica. J. Bacteriol. 186: 4556-4567.
52. BREINIG, S. & G. FUCHS. 2000. Genes involved in the anaerobic metabolism of phenol in the bacterium Thauera aromatica. J. Bacteriol. 182: 5849-5863.
53. NARMANDAKH, A., N. GAD'ON, F. DREPPER, et al. 2006. Phosphorylation of phenol by phenylphosphate synthase: role of histidine phosphate in catalysis. J. Bacteriol. 188: 7815-7822.
54. SHINODA, Y., Y. SAKAI, M. UE, et al. 2000. Isolation and characterization of a new denitrifying spirillum capable of anaerobic degradation of phenol. Appl. Environ. Microbiol. 66: 1286-1291.
55. SHINODA, Y., J. AKAGI, Y. UCHIHASHI, et al. 2005. Anaerobic degradation of aromatic compounds by Magnetospirillum strains: isolation and degradation genes. Biosci. Biotechnol. Biochem. 69: 1483-1491.
56. RABUS, R., M. KUBE, J. HEIDER, et al. 2005.The genome sequence of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Arch Microbiol. 183: 27-36.
57. HE, Z. & J. WIEGEL. 1995. Purification and characterization of an oxygen-sensitive 4-hydroxybenzoate decarboxylase from Clostridium hydroxybenzoicum. Eur. J. Biochem. 229: 77-82.
58. HUANG, J., Z. HE & J. WIEGEL. 1999. Cloning, characterization, and expression of a novel gene encoding a 4-hydroxybenzoate decarboxylase from Clostridium hydroxybenzoicum. J. Bacteriol. 181: 5119-5122.
59. CAVIN, J.F., V. DARTOIS & C. DIVIES. 1998. Gene cloning, transcriptional analysis, purification, and characterization of phenolic acid decarboxylase from Bacillus subtilis. Appl. Environ. Microbiol. 64: 1466-1471.
60. CHOW, K.T., M.K. POPE & J. DAVIES. 1999. Characterization of a vanillic acid non-oxidative decarboxylation gene cluster from Streptomyces sp. D7. Microbiology 145: 2393-2403.
61. 2-limited conditions. J. Bacteriol. 172: 212-217.
62. ZHANG, X. & J. WIEGEL. 1994. Reversible conversion of 4-hydroxybenzoate and phenol by Clostridium hydroxybenzoicum. Appl. Environ. Microbiol. 60: 4182-4185.
63. 13C-4 benzoate, an intermediate step in the anaerobic degradation of chlorophenols. FEMS Microbiol. Lett. 67: 63-66.
64. ZHANG, X. & J. WIEGEL. 1990. Sequential anaerobic degradation of 2,4-dichlorophenol in freshwater sediments. Appl. Environ. Microbiol. 56: 1119-1127.
65. ZHANG, X. & J. WIEGEL. 1992. The anaerobic degradation of 3-chloro-4-hydroxybenzoate in freshwater sediment proceeds via either chlorophenol or hydroxybenzoate to phenol and subsequently to benzoate. Appl. Environ. Microbiol. 58: 3580-3585.
66. SHARAK GENTHNER, B.R., G.T. TOWNSEND & P.J. CHAPMAN. 1990. Effect of fluorinated analogues of phenol and hydroxybenzoates on the anaerobic transformation of phenol to benzoate. Biodegradation 1: 65-74.
67. BIEGERT, T., U. ALTENSCHMIDT, C. ECKERSKORN & G. FUCHS. 1993. Enzymes of anaerobic metabolism of phenolic compounds. 4-Hydroxybenzoate-CoA ligase from a denitrifying Pseudomonas species. Eur. J. Biochem. 213: 555-561.
68. GIBSON, J., M. DISPENSA, G.C. FOGG, et al. 1994. 4-Hydroxybenzoate-coenzyme A ligase from Rhodopseudomonas palustris: purification, gene sequence, and role in anaerobic degradation. J. Bacteriol. 176: 634-41.
69. LAEMPE, D., M. JAHN, K. BREESE, et al. 2001. Anaerobic metabolism of 3-hydroxybenzoate by the denitrifying bacterium Thauera aromatica. J. Bacteriol. 183: 968-979.
70. MÖBITZ, H. & M. BOLL. 2002. A Birch-like mechanism in enzymatic benzoyl-CoA reduction - A kinetic study of substrate analogues combined with an ab initio model. Biochemistry 41: 1752-1758.
71. BRACKMANN, R. & G. FUCHS. 1993. Enzymes of anaerobic metabolism of phenolic compounds - 4-Hydroxybenzoyl-CoA reductase (dehydroxylating) from a denitrifying Pseudomonas species. Eur. J. Biochem. 213: 563-571.
72. BOLL, M., G. FUCHS, C. MEIER, et al. 2001. Redox centers of 4-hydroxybenzoyl-CoA reductase, a member of the xanthine oxidase family of molybdenum-containing enzymes. J. Biol. Chem. 276: 47853-47862.
73. BREESE, K. & G. FUCHS. 1998. 4-Hydroxybenzoyl-CoA reductase (dehydroxylating) from the denitrifying bacterium Thauera aromatica. Prosthetic groups, electron donor, and genes of amember of the molybdenum-flavin-iron-sulfur proteins. Eur. J. Biochem. 251: 916-923.
74. GIBSON, J., M. DISPENSA & C.S. HARWOOD. 1997. 4-Hydroxybenzoyl-CoA reductase (dehydroxylating) is required for anaerobic degradation of 4-hydroxybenzoate by Rhodopseudomonas palustris and shares features with molybdenum-containing hydroxylases. J. Bacteriol. 179: 634-642.
75. UNCIULEAC, M., E. WARKENTIN, C.C. PAGE, et al. 2004. Structure of a xanthine oxidase-related 4-hydroxybenzoyl-CoA reductase with an additional [4Fe-4S] cluster and an inverted electron flow. Structure 12: 2249-2256.
76. HILLE, R. 2005. Molybdenum-containing hydroxylases. Arch. Biochem. Biophys. 433: 107-116.
77. BOLL, M., B. SCHINK, A. MESSERSCHMIDT & P.M. KRONECK. 2005. Novel bacterial molybdenum and tungsten enzymes: three-dimensional structure, spectroscopy, and reaction mechanism. Biol. Chem. 386: 999-1006.
78. BUCKEL, W. & R. KEESE. 1995. One electron reactions of CoASH esters in anaerobic bacteria. Angew. Chem. Int. Ed. Engl. 34: 1502-1506.
79. BOLL, M., G. FUCHS, G. TILLEY, et al. 2000. Unusual spectroscopic and electrochemical properties of the 2[4Fe-4S] ferredoxin of Thauera aromatica. Biochemistry 39: 4929-4938.
80. HEIDER, J. 2007. Adding handles to unhandy substrates: anaerobic hydrocarbon activation mechanisms. Curr. Opin. Chem. Biol. 11: 188-194.
81. BIEGERT, T., G. FUCHS & J. HEIDER. 1996. Evidence that anaerobic 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.
82. BELLER, H.R. & A.M. SPORMANN. 1997. Anaerobic activation of toluene and o-xylene by addition of fumarate in denitrifying strain T. J. Bacteriol. 179: 670-676.
83. LEUTHNER, B., C. LEUTWEIN, H. SCHULZ, et al. 1998. Biochemical and genetic characterization of benzylsuccinate synthase from Thauera aromatica: a new glycyl radical enzyme catalyzing the first step in anaerobic toluene metabolism. Mol. Microbiol. 28: 615-628.
84. KRIEGER, C.J., W. ROSEBOOM, S.P. ALBRACHT & A.M. SPORMANN. 2001. A stable organic free radical in anaerobic benzylsuccinate synthase of Azoarcus sp. strain T. J. Biol. Chem. 276: 12924-12927.
85. HEIDER, J., A.M. SPORMANN, H.R. BELLER & F. WIDDEL. 1999. Anaerobic bacterial metabolism of hydrocarbons. FEMS Microbiol. Rev. 22: 459-473.
86. SPORMANN, A.M. & F.WIDDEL. 2000. Metabolism of alkylbenzenes, alkanes, and other hydrocarbons in anaerobic bacteria. Biodegradation 11: 85-105.
87. WIDDEL, F. & R. RABUS. 2001. Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr. Opin. Biotechnol. 12: 259-276.
88. KOCH, J. & G. FUCHS. 1992. Enzymatic reduction of benzoyl-CoA to alicyclic compounds, a key reaction in anaerobic aromatic metabolism. Eur. J. Biochem. 205: 195-202.
89. KOCH, J., W. EISENREICH, A. BACHER & G. FUCHS. 1993. Products of enzymatic reduction of benzoyl-CoA, a key reaction in anaerobic aromatic metabolism. Eur. J. Biochem. 211: 649-661.
90. BOLL, M. & G. FUCHS. 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.
91. BOLL, M., S.J.P. ALBRACHT & G. FUCHS. 1997. Benzoyl-CoA reductase (dearomatizing), a key enzyme of anaerobic aromatic metabolism. A study of adenosinephosphate activity, ATP stoichiometry of the reaction and EPR properties of the enzyme. Eur. J. Biochem. 244: 840-851
92. EGLAND, P.G., D.A. PELLETIER, M. DISPENSA, et al. 1997. A cluster of bacterial genes for anaerobic benzene ring biodegradation. Proc. Natl. Acad. Sci. USA 94: 6484-6489.
93. BREESE, K., M. BOLL, J. ALT- MÖRBE, et al. 1998. Genes coding for the benzoyl-CoA pathway of anaerobic aromatic metabolism in the bacterium Thauera aromatica. Eur. J. Biochem. 256: 148-154.
94. BOLL, M., D. LAEMPE, W. EISENREICH, et al. 2000. Non-aromatic products from anoxic conversion of benzoyl-CoA with benzoyl-CoA reductase and cyclohexa-1,5-diene-1-carbonyl-CoA hydratase. J. Biol. Chem. 275: 21889-21895.
95. BOLL, M., G. FUCHS, C. MEIER, et al. 2000. EPR and Mössbauer studies of benzoyl-CoA reductase. J. Biol. Chem. 275: 31857-31868.
96. BOLL, M., G. FUCHS & D.J. LOWE. 2001. Single turnover EPR studies of benzoyl-CoA reductase. Biochemistry 40: 7612-7620.
97. BIRCH, A.J., A.K. HINDE & L. RADOM. 1980. A theoretical approach to the Birch reduction. Structures and stabilities of the radical anions of substituted benzenes. J. Am. Chem. Soc. 102: 3370-3376.
98. MÖBITZ, H., T. FRIEDRICH & M. BOLL. 2004. Substrate binding and reduction of benzoyl-CoA reductase: evidence for nucleotide-dependent conformational changes. Biochemistry 43: 1376-85.
99. UNCIULEAC, M. & M. BOLL. 2001. Mechanism of ATP-driven electron transfer catalyzed by the benzene ring-reducing enzyme benzoyl-CoA reductase. Proc. Natl. Acad. Sci. USA 98: 13619-13624.
100. MÖBITZ, H. & M. BOLL. 2002. A Birch-like mechanism in enzymatic benzoyl-CoA reduction: a kinetic study of substrate analogues combined with an ab initio model. Biochemistry 41: 1752-1758.
101. PETERS, F., M. ROTHER & M. BOLL. 2004. Selenocysteine-containing proteins in anaerobic benzoate metabolism of Desulfococcus multivorans. J. Bacteriol. 186: 2156-2163.
102. WISCHGOLL, S., D. HEINTZ, F. PETERS, et al. 2005. Gene clusters involved in anaerobic benzoate degradation of Geobacter metallireducens. Mol. Microbiol. 58: 1238-1252.
103. PETERS, F., Y. SHINODA, M.J. MCI NERNEY & M. BOLL. 2007. Cyclohexa-1,5-diene-1-carbonyl- coenzyme A (CoA) hydratases of Geobacter metallireducens and Syntrophus aciditrophicus: evidence for a common benzoyl-CoA degradation pathway in facultative and strict anaerobes. J. Bacteriol. 189: 1055-1060.