Unusual reactions involved in anaerobic metabolism of phenolic compounds
-
Matthias Boll
Abstract
Aerobic bacteria use molecular oxygen as a common co-substrate for key enzymes of aromatic metabolism. In contrast, in anaerobes all oxygen-dependent reactions are replaced by a set of alternative enzymatic processes. The anaerobic degradation of phenol to a non-aromatic product involves enzymatic processes that are uniquely found in the aromatic metabolism of anaerobic bacteria: (i) ATP-dependent phenol carboxylation to 4-hydroxybenzoate via a phenylphosphate intermediate (biological Kolbe-Schmitt carboxylation); (ii) reductive dehydroxylation of 4-hydroxybenzoyl-CoA to benzoyl-CoA; and (iii) ATP-dependent reductive dearomatization of the key intermediate benzoyl-CoA in a ‘Birch-like’ reduction mechanism. This review summarizes the results of recent mechanistic studies of the enzymes involved in these three key reactions.
References
Biegert, T., Altenschmidt, U., Eckerskorn, C., and Fuchs, G. (1993). Enzymes of anaerobic metabolism of phenolic compounds. 4-Hydroxybenzoate-CoA ligase from a denitrifying Pseudomonas species. Eur. J. Biochem.213, 555–561.Suche in Google Scholar
Birch, A.J., Hinde, A.K., and Radom, L. (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.Suche in Google Scholar
Blattner, F.R., Plunkett, G., Bloch, C.A., Perna, N.T., Burland, V., Riley, M., Collado-Vides, J., Glasner, J.D., Rode, C.K., Mayhew, G.F., et al. (1997). The complete genome sequence of Escherichia coli K-12. Science277, 1453–1474.10.1126/science.277.5331.1453Suche in Google Scholar
Boll, M. (2005). Key enzymes in the anaerobic aromatic metabolism catalysing Birch-like reductions. Biochim. Biophys. Acta1707, 34–50.10.1016/j.bbabio.2004.01.009Suche in Google Scholar
Boll, M. and 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.Suche in Google Scholar
Boll, M., Albracht, S.J.P., and Fuchs, G. (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.Suche in Google Scholar
Boll, M., Fuchs, G., Tilley, G., Armstrong, F.A., and Lowe, D.J. (2000a). Unusual spectroscopic and electrochemical properties of the 2[4Fe-4S] ferredoxin of Thauera aromatica. Biochemistry39, 4929–4938.10.1021/bi9927890Suche in Google Scholar
Boll, M., Laempe, D., Eisenreich, W., Bacher, A., Mittelberger, T. Heinze, J., and Fuchs, G. (2000b). 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, 21889–21895.10.1074/jbc.M001833200Suche in Google Scholar
Boll, M., Fuchs, G., Meier, C. Trautwein, A.X., and Lowe, D.J. (2000c). EPR and Mössbauer studies of benzoyl-CoA reductase. J. Biol. Chem.275, 31857–31868.10.1074/jbc.M001508200Suche in Google Scholar
Boll, M., Fuchs, G., Meier, C., Trautwein, A.X., El Kasmi, A., Ragsdale, S.W., Buchanan, G., and Lowe, D.J. (2001a). Redox centers of 4-hydroxybenzoyl-CoA reductase, a member of the xanthine oxidase family of molybdenum-containing enzymes. J. Biol. Chem.276, 47853–47862.10.1074/jbc.M106766200Suche in Google Scholar
Boll, M., Fuchs, G., and Lowe, D.J. (2001b). Single turnover EPR studies of benzoyl-CoA reductase. Biochemistry40, 7612–7620.10.1021/bi002771lSuche in Google Scholar
Boll, M., Fuchs, G., and Heider, H. (2002). Anaerobic metabolism of aromatic compounds. Curr. Opin. Chem. Biol.6, 604–611.10.1016/S1367-5931(02)00375-7Suche in Google Scholar
Boll, M., Schink, B., Messerschmidt, A., and Kroneck, P.M.H. (2005). Novel bacterial molybdenum and tungsten enzymes: three-dimensional structure, spectroscopy, and reaction mechanism. Biol. Chem.386, 999–1006.10.1515/BC.2005.116Suche in Google Scholar PubMed
Brackmann, R. and Fuchs, G. (1993). Enzymes of anaerobic metabolism of phenolic compounds – 4-hydroxybenzoyl-CoA reductase (dehydroxylating) from a denitrifying Pseudomonas species. Eur. J. Biochem.213, 563–571.10.1111/j.1432-1033.1993.tb17795.xSuche in Google Scholar PubMed
Breese, K. and Fuchs, G. (1998). 4-Hydroxybenzoyl-CoA reductase (dehydroxylating) from the denitrifying bacterium Thauera aromatica. Prosthetic groups, electron donor, and genes of a member of the molybdenum-flavin-iron-sulfur proteins. Eur. J. Biochem.251, 916–923.Suche in Google Scholar
Breinig, S. and Fuchs, G. (2000). Genes involved in the anaerobic metabolism of phenol in the bacterium Thauera aromatica. J. Bacteriol.182, 5849–5863.10.1128/JB.182.20.5849-5863.2000Suche in Google Scholar
Buckel, W. and Keese, R. (1995). One-electron reactions of CoASH esters in anaerobic bacteria. Angew. Chem. Int. Ed.34, 1502–1506.10.1002/anie.199515021Suche in Google Scholar
Cavin, J.F., Dartois, V., and Divies, C. (1998). Gene cloning, transcriptional analysis, purification, and characterization of phenolic acid decarboxylase from Bacillus subtilis. Appl. Environ. Microbiol.64, 1466–1471.10.1128/AEM.64.4.1466-1471.1998Suche in Google Scholar
Chow, K.T., Pope, M.K., and Davies, J. (1999). Characterization of a vanillic acid non-oxidative decarboxylation gene cluster from Streptomyces sp. D7. Microbiology145, 2393–2403.Suche in Google Scholar
Cosper, M.M., Cosper, N.J., Hong, W., Shokes, J.E., Broderick, W.E., Broderick, J.B., Johnson, M.K., and Scott, R.A. (2003). Structural studies of the interaction of S-adenosylmethionine with the [4Fe-4S] clusters in biotin synthase and pyruvate formate-lyase activating enzyme. Protein Sci.12, 1573–1577.10.1110/ps.0302203Suche in Google Scholar
Gibson, J. and Harwood, C.S. (2002). Metabolic diversity in aromatic compound utilization by anaerobic microbes. Annu. Rev. Microbiol.56, 345–369.10.1146/annurev.micro.56.012302.160749Suche in Google Scholar
Gibson, J., Dispensa, M., Fogg, G.C., Evans, D.T., and Harwood, C.S. (1994). 4-Hydroxybenzoate-coenzyme A ligase from Rhodopseudomonas palustris: purification, gene sequence, and role in anaerobic degradation. J. Bacteriol.176, 634–641.10.1128/jb.176.3.634-641.1994Suche in Google Scholar
Gibson, J., Dispensa, M., and Harwood, C.S. (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, 634–642.10.1128/jb.179.3.634-642.1997Suche in Google Scholar
Gorny, N. and Schink, B. (1994). Anaerobic degradation of catechol by Desulfobacterium sp. strain Cat2 proceeds via carboxylation to protocatechuate. Appl. Environ. Microbiol.60, 3396–3400.Suche in Google Scholar
Haddock, J.D. and Ferry, J.G. (1989). Purification and properties of phloroglucinol reductase from Eubacterium oxidoreducens G-41. J. Biol. Chem.264, 4423–4427.10.1016/S0021-9258(18)83759-0Suche in Google Scholar
Haruki, E. (1982). Organic syntheses with carbon dioxide. In: Organic and Bio-organic Chemistry of Carbon Dioxide, S. Inoue and N. Yamazaki, eds. (New York, USA: Halsted Press), pp. 5–78.Suche in Google Scholar
Harwood, C.S., Burchhardt, G., Herrmann, H., and Fuchs, G. (1999). Anaerobic metabolism of aromatic compounds via the benzoyl-CoA pathway. FEMS Microbiol. Rev.22, 439–458.Suche in Google Scholar
He, Z. and Wiegel, J. (1995). Purification and characterization of an oxygen-sensitive 4-hydroxybenzoate decarboxylase from Clostridium hydroxybenzoicum. Eur. J. Biochem.229, 77–82.10.1111/j.1432-1033.1995.tb20440.xSuche in Google Scholar PubMed
Hille, R. (2005). Molybdenum-containing hydroxylases. Arch. Biochem. Biophys.433, 107–116.10.1016/j.abb.2004.08.012Suche in Google Scholar PubMed
Huang, J., He, Z., and Wiegel, J. (1999). Cloning, characterization, and expression of a novel gene encoding a 4-hydroxybenzoate decarboxylase from Clostridium hydroxybenzoicum. J. Bacteriol.181, 5119–5122.10.1128/JB.181.16.5119-5122.1999Suche in Google Scholar PubMed PubMed Central
Kluge, C., Tschech, A., and Fuchs, G. (1990). Anaerobic metabolism of resorcyclic acids (m-dihydroxybenzoic acids) and resorcinol (1,3-benzenediol) in a fermenting and in a denitrifying bacterium. Arch. Microbiol.155, 68–74.10.1007/BF00291277Suche in Google Scholar
Kosugi, Y., Imaoka, Y., Gotoh, F., Rahim, M.A., Matsui, Y., and Sakanishi, K. (2003). Carboxylations of alkali metal phenoxides with carbon dioxide. Org. Biomol. Chem.1, 817–821.10.1039/b210793gSuche in Google Scholar PubMed
Lack, A. and Fuchs, G. (1992). Carboxylation of phenylphosphate by phenol carboxylase, an enzyme system of anaerobic phenol metabolism. J. Bacteriol.174, 3629–3636.10.1128/jb.174.11.3629-3636.1992Suche in Google Scholar PubMed PubMed Central
Lack, A. and Fuchs, G. (1994). Evidence that phenol phosphorylation to phenylphosphate is the first step in anaerobicphenol metabolism in a denitrifying Pseudomonas sp. Arch. Microbiol.161, 132–139.Suche in Google Scholar
Lack, A., Tommasi, I., Aresta, M., and Fuchs, G. (1991). Catalytic properties of phenol carboxylase. In vitro study of CO2: 4-hydroxybenzoate isotope exchange reaction. Eur. J. Biochem.197, 473–479.Suche in Google Scholar
Laempe, D., Jahn, M., Breese, K., Schägger, H., and Fuchs, G. (2001). Anaerobic metabolism of 3-hydroxybenzoate by the denitrifying bacterium Thauera aromatica.J. Bacteriol.183, 968–1979.10.1128/JB.183.3.968-979.2001Suche in Google Scholar PubMed PubMed Central
Lawrence, C.C., Bennati, M., Obias, H.V., Bar, G., Griffin, R.G., and Stubbe, J. (1999). High-field EPR detection of a disulfide radical anion in the reduction of cytidine 5′-diphosphate by the E441Q R1 mutant of Escherichia coli ribonucleotide reductase. Proc. Natl. Acad. Sci. USA96, 8979–8984.10.1073/pnas.96.16.8979Suche in Google Scholar PubMed PubMed Central
Möbitz, H. and Boll, M. (2002) 1. A Birch-like mechanism in enzymatic benzoyl-CoA reduction – a kinetic study of substrate analogues combined with an ab initio model. Biochemistry41, 1752–1758.Suche in Google Scholar
Möbitz, H., Friedrich, T., and Boll, M. (2004). Substrate binding and reduction of benzoyl-CoA reductase: evidence for nucleotide-dependent conformational changes. Biochemistry43, 1376–1385.10.1021/bi0358871Suche in Google Scholar PubMed
Mortensen, J. and Heinze, J. (1984). Die elektrochemische Reduktion von Benzol – erste direkte Bestimmung des Re-doxpotentials. Angew. Chem.96, 64–65.10.1002/ange.19840960121Suche in Google Scholar
Philipp, B., Kemmler, D., Hellstern, J., Gorny, N., Caballero, A., and Schink, B. (2002). Anaerobic degradation of protocatechuate (3,4-dihydroxybenzoate) by Thauera aromatica strain AR-1. FEMS Microbiol. Lett.212, 139–143.10.1111/j.1574-6968.2002.tb11257.xSuche in Google Scholar PubMed
Rabus, R., Kube, M., Heider, J., Beck, A., Heitmann, K., Widdel, F., and Reinhardt, R. (2005). The genome sequence of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Arch. Microbiol.183, 27–36.10.1007/s00203-004-0742-9Suche in Google Scholar PubMed
Reichenbecher, W. and Schink, B. (1997). Desulfovibrioinopinatus, sp. nov., a new sulfate-reducing bacterium that degrades hydroxyhydroquinone. Arch. Microbiol.168, 338–344.Suche in Google Scholar
Schmeling, S., Narmandakh, A., Schmitt, O., Gad'on, N., Schühle, K., and Fuchs, G. (2004). Phenylphosphate synthase: a new phosphotransferase catalyzing the first step in anaerobic phenol metabolism in Thauera aromatica. J. Bacteriol.186, 8044–8057.10.1128/JB.186.23.8044-8057.2004Suche in Google Scholar PubMed PubMed Central
Schühle, K. and Fuchs, G. (2004). Phenylphosphate carboxylase: a new C-C lyase involved in anaerobic phenol metabolism in Thauera aromatica. J. Bacteriol.186, 4556–4567.10.1128/JB.186.14.4556-4567.2004Suche in Google Scholar PubMed PubMed Central
Shinoda Y., Sakai, M.U., Hiraishi, A., and Kato, N. (2000). Isolation and characterization of a new denitrifying spirillum capable of anaerobic degradation of phenol. Appl. Environ. Microbiol.66, 1286–1291.10.1128/AEM.66.4.1286-1291.2000Suche in Google Scholar PubMed PubMed Central
Surdhar, P.S. and Armstrong, D.A. (1987). Reduction potentials and exchange reactions of thiyl radicals and disulfide anion radicals. J. Phys. Chem.91, 6532–6537.10.1021/j100310a022Suche in Google Scholar
Tschech, A. and Fuchs, G. (1987). Anaerobic degradation of phenol by pure cultures of newly isolated denitrifying pseudomonads. Arch. Microbiol.145, 213–217.10.1007/BF00414814Suche in Google Scholar PubMed
Unciuleac, M. and Boll, M. (2001). Mechanism of ATP-driven electron transfer catalyzed by the benzene ring-reducing enzyme benzoyl-CoA reductase. Proc. Natl. Acad. Sci. USA98, 13619–13624.10.1073/pnas.241375598Suche in Google Scholar PubMed PubMed Central
Unciuleac, M., Warkentin, E., Page, C.C., Boll, M., and Ermler, U. (2004). Structure of a xanthine oxidase-related 4-hydroxybenzoyl-CoA reductase with an additional [4Fe-4S] cluster and an inverted electron flow. Structure12, 2249–2256.10.1016/j.str.2004.10.008Suche in Google Scholar PubMed
©2005 by Walter de Gruyter Berlin New York
Artikel in diesem Heft
- Highlight: Radicals in Enzymatic Catalysis
- Radical-mediated dehydration reactions in anaerobic bacteria
- Heterodisulfide reductase from methanogenic archaea: a new catalytic role for an iron-sulfur cluster
- Structural and functional comparison of HemN to other radical SAM enzymes
- New glycyl radical enzymes catalysing key metabolic steps in anaerobic bacteria
- Unusual reactions involved in anaerobic metabolism of phenolic compounds
- Novel bacterial molybdenum and tungsten enzymes: three-dimensional structure, spectroscopy, and reaction mechanism
- Spectroscopic and theoretical approaches for studying radical reactions in class I ribonucleotide reductase
- Biomimetic metal-radical reactivity: aerial oxidation of alcohols, amines, aminophenols and catechols catalyzed by transition metal complexes
- Combinatorial approaches to functional models for galactose oxidase
- Spectroscopic characterization of the iron-oxo intermediate in cytochrome P450
- Impact of Mycoplasma hyorhinis infection on l-arginine metabolism: differential regulation of the human and murine iNOS gene
- Degradation of the sodium taurocholate cotransporting polypeptide (NTCP) by the ubiquitin-proteasome system
- Identification of three novel mutations in the dihydropyrimidine dehydrogenase gene associated with altered pre-mRNA splicing or protein function
Artikel in diesem Heft
- Highlight: Radicals in Enzymatic Catalysis
- Radical-mediated dehydration reactions in anaerobic bacteria
- Heterodisulfide reductase from methanogenic archaea: a new catalytic role for an iron-sulfur cluster
- Structural and functional comparison of HemN to other radical SAM enzymes
- New glycyl radical enzymes catalysing key metabolic steps in anaerobic bacteria
- Unusual reactions involved in anaerobic metabolism of phenolic compounds
- Novel bacterial molybdenum and tungsten enzymes: three-dimensional structure, spectroscopy, and reaction mechanism
- Spectroscopic and theoretical approaches for studying radical reactions in class I ribonucleotide reductase
- Biomimetic metal-radical reactivity: aerial oxidation of alcohols, amines, aminophenols and catechols catalyzed by transition metal complexes
- Combinatorial approaches to functional models for galactose oxidase
- Spectroscopic characterization of the iron-oxo intermediate in cytochrome P450
- Impact of Mycoplasma hyorhinis infection on l-arginine metabolism: differential regulation of the human and murine iNOS gene
- Degradation of the sodium taurocholate cotransporting polypeptide (NTCP) by the ubiquitin-proteasome system
- Identification of three novel mutations in the dihydropyrimidine dehydrogenase gene associated with altered pre-mRNA splicing or protein function