Microbial degradation of aromatic compounds — from one strategy to four (original) (raw)

• Metzler, D. E. Biochemistry. The Chemical Reactions of Living Cells 2nd edn Vol. 2 (Academic, London, 2001). An excellent general textbook of biochemistry.
  Google Scholar
• Kirk, T. K. & Farrell, R. L. Enzymatic “combustion”: the microbial degradation of lignin. Annu. Rev. Microbiol. 41, 465–505 (1987).
  Article CAS PubMed Google Scholar
• Bugg, T. D., Ahmad, M., Hardiman, E. M. & Singh, R. The emerging role for bacteria in lignin degradation and bio-product formation. Curr. Opin. Biotechnol. 22, 394–400 (2011).
  Article CAS PubMed Google Scholar
• Hayaishi, O. From oxygenase to sleep. J. Biol. Chem. 283, 19165–19175 (2008). Reflections from the scientist who discovered oxygenases.
  Article CAS PubMed Google Scholar
• Dagley, S., Evans, W. C. & Ribbons, D. W. New pathways in the oxidative metabolism of aromatic compounds by microorganisms. Nature 188, 560–566 (1960).
  Article CAS PubMed Google Scholar
• Dagley, S., Chapman, P. J., Gibson, D. T. & Wood, J. M. Degradation of benzene nucleus by bacteria. Nature 202, 775–778 (1964).
  Article CAS PubMed Google Scholar
• Ornston, L. N. & Stanier, R. Y. The conversion of catechol and protocatechuate to β-ketoadipate by Pseudomonas putida. J. Biol. Chem. 241, 3776–3786 (1966).
  Article CAS PubMed Google Scholar
• Dagley, S. Catabolism of aromatic compounds by micro-organisms. Adv. Microb. Physiol. 6, 1–46 (1971).
  Article CAS PubMed Google Scholar
• Stanier, R. Y. & Ornston, L. N. The β-ketoadipate pathway. Adv. Microb. Physiol. 9, 89–151 (1973). A classic article on degradation of aromatic compounds.
  Article CAS PubMed Google Scholar
• Harwood, C. S. & Parales, R. E. The β-ketoadipate pathway and the biology of self-identity. Annu. Rev. Microbiol. 50, 553–590 (1996).
  Article CAS PubMed Google Scholar
• Harayama, S., Kok, M. & Neidle, E. L. Functional and evolutionary relationships among diverse oxygenases. Ann. Rev. Microbiol. 46, 565–601 (1992).
  Article CAS Google Scholar
• Que, L. & Ho, R. Y. N. Dioxygen activation by enzymes with mononuclear non-heme iron active sites. Chem. Rev. 96, 2607–2624 (1996).
  Article CAS PubMed Google Scholar
• Butler, C. S. & Mason, J. R. Structure–function analysis of the bacterial aromatic ring-hydroxylating dioxygenases. Adv. Microb. Physiol. 38, 47–84 (1997).
  Article CAS PubMed Google Scholar
• Gibson, D. T. & Parales, R. E. Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr. Opin. Biotechnol. 11, 236–243 (2000).
  Article CAS PubMed Google Scholar
• Leahy, J. G., Batchelor, P. J. & Morcomb, S. M. Evolution of the soluble diiron monooxygenases. FEMS Microbiol. Rev. 27, 449–479 (2003).
  Article CAS PubMed Google Scholar
• Vaillancourt, F. H., Bolin, J. T. & Eltis, L. D. The ins and outs of ring-cleaving dioxygenases. Crit. Rev. Biochem. Mol. Biol. 41, 241–267 (2006).
  Article CAS PubMed Google Scholar
• Lipscomb, J. D. Mechanism of extradiol aromatic ring-cleaving dioxygenases. Curr. Opin. Struct. Biol. 18, 644–649 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Berry, D. F., Francis, A. J. & Bollag, J. M. Microbial metabolism of homocyclic and heterocyclic aromatic compounds under anaerobic conditions. Microbiol. Rev. 51, 43–59 (1987).
  Article CAS PubMed PubMed Central Google Scholar
• Evans, W. C. & Fuchs, G. Anaerobic degradation of aromatic compounds. Annu. Rev. Microbiol. 42, 289–317 (1988).
  Article CAS PubMed Google Scholar
• Young, L. Y. & Häggblom, M. M. Biodegradation of toxic and environmental pollutants. Curr. Opin. Biotechnol. 2, 429–435 (1991).
  Article CAS PubMed Google Scholar
• Heider, J. & Fuchs, G. Anaerobic metabolism of aromatic compounds. Eur. J. Biochem. 243, 577–596 (1997).
  Article CAS PubMed Google Scholar
• Heider, J. & Fuchs, G. Microbial anaerobic aromatic metabolism. Anaerobe 3, 1–22 (1997).
  Article CAS PubMed Google Scholar
• Harwood, C., Burchhardt, G., Herrmann, H. & Fuchs, G. Anaerobic metabolism of aromatic compounds via the benzoyl-CoA pathway. FEMS Microbiol. Rev. 22, 439–458 (1999).
  Article Google Scholar
• Schink, B., Philipp, B. & Müller, J. Anaerobic degradation of phenolic compounds. Naturwissenschaften 87, 12–23 (2000). A review dealing with the pathways that differ from the anaerobic benzoyl-CoA pathway.
  Article CAS PubMed Google Scholar
• Widdel, F. & Rabus, R. Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr. Opin. Biotechnol. 12, 259–276 (2001).
  Article CAS PubMed Google Scholar
• Boll, M., Fuchs, G. & Heider, J. Anaerobic oxidation of aromatic compounds and hydrocarbons. Curr. Opin. Biol. Chem. 6, 604–611 (2002).
  Article CAS Google Scholar
• Gibson, J. & Harwood, C. S. Metabolic diversity in aromatic compound utilization by anaerobic microbes. Annu. Rev. Microbiol. 56, 345–369 (2002).
  Article CAS PubMed Google Scholar
• Meckenstock, R. U., Safinowski, M. & Griebler, C. Anaerobic degradation of polycyclic aromatic hydrocarbons. FEMS Microbiol. Ecol. 49, 27–36 (2004).
  Article CAS PubMed Google Scholar
• Fuchs, G. Anaerobic metabolism of aromatic compounds. Ann. N. Y. Acad. Sci. 1125, 82–99 (2008).
  Article CAS PubMed Google Scholar
• Carmona, M. et al. Anaerobic catabolism of aromatic compounds: a genetic and genomic view. Microbiol. Mol. Biol. Rev. 73, 71–133 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Braun, K. & Gibson, D. T. Anaerobic degradation of 2-aminobenzoate (anthranilic acid) by denitrifying bacteria. Appl. Environ. Microbiol. 48, 102–107 (1984).
  Article CAS PubMed PubMed Central Google Scholar
• Tschech, A. & Fuchs, G. Anaerobic degradation of phenol by pure cultures of newly isolated denitrifying pseudomonads. Arch. Microbiol. 148, 213–217 (1987).
  Article CAS PubMed Google Scholar
• Anders, J. H., Kaetzke, A., Kämpfer, P., Ludwig, W. & Fuchs, G. Taxonomic position of aromatic-degrading denitrifying pseudomonad strains K 172 and KB 740 and their description as new members of the genera Thauera, Thauera aromatica sp. nov., and Azoarcus, as Azoarcus evansii sp. nov., respectively, members of the beta subclass of Proteobacteria. Int. J. Syst. Bacteriol. 45, 327–333 (1995).
  Article CAS PubMed Google Scholar
• Rabus, R. et al. The genome sequence of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Arch. Microbiol. 183, 27–36 (2005). An exemplary annotation of a bacterial genome with reference to degradation of aromatic compounds.
  Article CAS PubMed Google Scholar
• Rather, L. J. et al. Structure and mechanism of the diiron benzoyl-coenzyme A epoxidase BoxB. J. Biol. Chem. 286, 29241–29248 (2011). A report detailing the crystal structure of the key benzoyl-CoA epoxidase and discussing a possible mechanism of action for this enzyme.
  Article CAS PubMed PubMed Central Google Scholar
• Mohamed, M. E., Zaar, A., Ebenau-Jehle, C. & Fuchs, G. Reinvestigation of a new type of aerobic benzoate metabolism in the proteobacterium Azoarcus evansii. J. Bacteriol. 183, 1899–1908 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Zaar, A., Eisenreich, W., Bacher, A. & Fuchs, G. A novel pathway of aerobic benzoate catabolism in the bacteria Azoarcus evansii and Bacillus stearothermophilus. J. Biol. Chem. 276, 24997–25004 (2001).
  Article CAS PubMed Google Scholar
• Gescher, J., Zaar, A., Mohamed, M., Schägger, H. & Fuchs, G. Genes coding for a new pathway of aerobic benzoate metabolism in Azoarcus evansii. J. Bacteriol. 184, 6301–6315 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Zaar, A., Gescher, J., Eisenreich, W., Bacher, A. & Fuchs, G. New enzymes involved in aerobic benzoate metabolism in Azoarcus evansii. Mol. Microbiol. 54, 223–238 (2004).
  Article CAS PubMed Google Scholar
• Gescher, J., Eisenreich, W., Wörth, J., Bacher, A. & Fuchs, G. Aerobic benzoyl-CoA catabolic pathway in Azoarcus evansii: studies on the non-oxygenolytic ring cleavage enzyme. Mol. Microbiol. 56, 1586–1600 (2005).
  Article CAS PubMed Google Scholar
• Gescher, J. et al. 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 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Ismail, W. Benzoyl-coenzyme A thioesterase of Azoarcus evansii: properties and function. Arch. Microbiol. 190, 451–460 (2008).
  Article CAS PubMed Google Scholar
• Bains, J., Leon, R. & Boulanger, M. J. Structural and biophysical characterization of BoxC from Burkholderia xenovorans LB400: a novel ring-cleaving enzyme in the crotonase superfamily. J. Biol. Chem. 284, 16377–16385 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Rather, L. J., Knapp, B., Haehnel, W. & Fuchs, G. Coenzyme A dependent aerobic metabolism of benzoate via epoxide formation. J. Biol. Chem. 285, 20615–20624 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Rather, L. J., Bill, E., Ismail, W. & Fuchs, G. The reducing component BoxA of benzoyl-coenzyme A epoxidase from Azoarcus evansii is a [4Fe-4S] protein. Biochim. Biophys. Acta Jun 11 2011 (doi:10.1016/j.bbapap.2011.05.023).
  Article CAS Google Scholar
• Denef, V. J. et al. Genetic and genomic insights into the role of benzoate-catabolic pathway redundancy in Burkholderia xenovorans LB400. Appl. Environ. Microbiol. 72, 585–595 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Kishore, G., Sugumaran, M. & Vaidyanathan, C. S. Metabolism of DL-(±)-phenylalanine by Aspergillus niger. J. Bacteriol. 128, 182–191 (1976).
  Article CAS PubMed PubMed Central Google Scholar
• Martinez-Blanco, H., Reglero, A., Rodriguez-Aparicio, L. B. & Luengo, J. M. Purification and biochemical characterization of phenylacetyl-CoA ligase from Pseudomonas putida. A specific enzyme for the catabolism of phenylacetic acid. J. Biol. Chem. 265, 7084–7090 (1990).
  Article CAS PubMed Google Scholar
• Olivera, E. R. et al. Molecular characterization of the phenylacetic acid catabolic pathway in Pseudomonas putida U: the phenylacetyl-CoA catabolon. Proc. Natl Acad. Sci. USA 95, 6419–6424 (1998). A summary of the early information on the phenylacetyl-CoA oxidation pathway, mainly based on genetic evidence.
  Article CAS PubMed PubMed Central Google Scholar
• Ferrández, A., Garcia, J. L. & Diaz, E. Transcriptional regulation of the divergent paa catabolic operons for phenylacetic acid degradation in Escherichia coli. J. Biol. Chem. 275, 12214–12222 (2000).
  Article PubMed Google Scholar
• Luengo, J. M., Garcia, J. L. & Olivera, E. R. The phenylacetyl-CoA catabolon: a complex catabolic unit with broad biotechnological applications. Mol. Microbiol. 39, 1434–1442 (2001).
  Article CAS PubMed Google Scholar
• Mohamed, M. E. S., Ismail, W., Heider, J. & Fuchs, G. Aerobic metabolism of phenylacetic acids in Azoarcus evansii. Arch. Microbiol. 178, 180–192 (2002).
  Article CAS Google Scholar
• Rost, R., Haas, S., Hammer, E., Herrmann, H. & Burchhardt, G. Molecular analysis of aerobic phenylacetate degradation in Azoarcus evansii. Mol. Genet. Genomics 267, 656–663 (2002).
  Article CAS PubMed Google Scholar
• Ismail, W. et al. Functional genomics by NMR spectroscopy. Phenylacetate catabolism in Escherichia coli. Eur. J. Biochem. 270, 3047–3054 (2003).
  Article CAS PubMed Google Scholar
• Fernandez, C., Ferrandez, A., Minambres, B., Diaz, E. & Garcia. J. L. Genetic characterization of the phenylacetyl-coenzyme A oxygenase from the aerobic phenylacetic acid degradation pathway of Escherichia coli. Appl. Environ. Microbiol. 72, 7422–7426 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Teufel, R. et al. Bacterial phenylalanine and phenylacetate catabolic pathway revealed. Proc. Natl Acad. Sci. USA 107, 14390–14395 (2010). A study that identifies the individual intermediates and enzyme steps of phenylacetyl-CoA oxidation.
  Article CAS PubMed PubMed Central Google Scholar
• Teufel, R. et al. Studies on the mechanism of ring-hydrolysis in phenylacetate degradation: a metabolic branching point. J. Biol. Chem. 286, 11021–11034 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Grishin, A. M. et al. Structural and functional studies of the Escherichia coli phenylacetyl-CoA monooxygenase complex. J. Biol. Chem. 286, 10735–10743 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Song, F. et al. Structure, function, and mechanism of the phenylacetate pathway hot dog-fold thioesterase PaaI. J. Biol. Chem. 281, 11028–11038 (2006).
  Article CAS PubMed Google Scholar
• Holden, H. M., Benning, M. M., Haller, T. & Gerlt, J. A. The crotonase superfamily: divergently related enzymes that catalyze different reactions involving acyl coenzyme A thioesters. Acc. Chem. Res. 34, 145–157 (2001).
  Article CAS PubMed Google Scholar
• del Peso-Santos, T. et al. Coregulation by phenylacetyl-coenzyme A-responsive PaaX integrates control of the upper and lower pathways for catabolism of styrene by Pseudomonas sp. strain Y2. J. Bacteriol. 188, 4812–4821 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Cao, Y. et al. Crystallization and preliminary X-ray characterization of a PaaX-like protein from Sulfolobus solfataricus P2. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 65, 776–778 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Schühle, K., Jahn, M., Ghisla, S. & Fuchs, G. Two similar gene clusters coding for enzymes of a new type of aerobic 2-aminobenzoate (anthranilate) metabolism in the bacterium Azoarcus evansii. J. Bacteriol. 183, 5268–5278 (2001).
  Article PubMed PubMed Central Google Scholar
• Buder, R. & Fuchs. G. 2-Aminobenzoyl CoA monooxygenase/ reductase, a novel type of flavoenzyme. Purification and some properties of the enzyme. Eur. J. Biochem. 185, 629–635 (1989).
  Article CAS PubMed Google Scholar
• Buder, R., Ziegler, K., Fuchs, G., Langkau, B. & Ghisla, S. 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 (1989).
  Article CAS PubMed Google Scholar
• Langkau, B., Ghisla, S., Buder, R., Ziegler, K. & Fuchs, G. 2-Aminobenzoyl-CoA monoxygenase/reductase, a novel type of flavoenzyme. Identification of the products. Eur. J. Biochem. 191, 365–371 (1990).
  Article CAS PubMed Google Scholar
• Langkau, B., Vock, P., Massey, V., Fuchs, G. & Ghisla, S. 2-Aminobenzoyl-CoA monooxygenase/reductase. Evidence for two distinct loci catalyzing substrate monooxygenation and hydrogenation. Eur. J. Biochem. 230, 676–685 (1995).
  Article CAS PubMed Google Scholar
• Hartmann, S. et al. Mechanistic studies with 2-aminobenzoyl-CoA monooxygenase/reductase. Proc. Natl Acad. Sci. USA 96, 7831–7836 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Torres, R. A. & Bruice, T. C. Theoretical investigation of the [1,2]-sigmatropic hydrogen migration in the mechanism of oxidation of 2-aminobenzoyl-CoA by 2-aminobenzoyl-CoA monooxygenase/reductase. Proc. Natl Acad. Sci. USA 96, 14748–14752 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Ishiyama, D., Vujaklija, D. & Davies, J. Novel pathway of salicylate degradation by Streptomyces sp. strain WA46. Appl. Environ. Microbiol. 70, 1297–12306 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Birch, A. J. Reduction by dissolving metals. Part I. J. Chem. Soc. 1944, 430–436 (1944).
  Article Google Scholar
• Kung, J. W. et al. Reversible biological Birch reduction at an extremely low redox potential. J. Am. Chem. Soc. 132, 9850–9856 (2010). An investigation that determines the extremely low redox potential of enzymatic reduction of the key intermediate benzoyl-CoA.
  Article CAS PubMed Google Scholar
• Buckel, W. & Keese, R. One-electron redox reactions of CoASH esters in anaerobic bacteria—a mechanistic proposal. Angew. Chem. Int. Ed. Engl. 34, 1502–1506 (1995).
  Article CAS Google Scholar
• Möbitz, H. & Boll, M. 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 (2002).
  Article PubMed CAS Google Scholar
• Boll, M. et al. 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 (2000).
  Article CAS PubMed Google Scholar
• Boll, M. Key enzymes in the anaerobic aromatic metabolism catalysing Birch-like reductions. Biochim. Biophys. Acta 1707, 34–50 (2005).
  Article CAS PubMed Google Scholar
• Boll, M., Albracht, S. S. & Fuchs, G. Benzoyl-CoA reductase (dearomatizing), a key enzyme of anaerobic aromatic metabolism. A study of adenosinetriphosphatase activity, ATP stoichiometry of the reaction and EPR properties of the enzyme. Eur. J. Biochem. 244, 840–851 (1997).
  Article CAS PubMed Google Scholar
• Boll, M. & Fuchs, G. 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 (1995). The first description of an ATP-dependent benzoyl-CoA reductase.
  Article CAS PubMed Google Scholar
• Unciuleac, M. & Boll, M. Mechanism of ATP-driven electron transfer catalyzed by the benzene ring-reducing enzyme benzoyl-CoA reductase. Proc. Natl Acad. Sci. USA 98, 13619–13624 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Breese, K., Boll, M., Alt-Mörbe, J., Schägger, H. & Fuchs, G. Genes coding for the benzoyl-CoA pathway of anaerobic aromatic metabolism in the bacterium Thauera aromatica. Eur. J. Biochem. 256, 148–154 (1998).
  Article CAS PubMed Google Scholar
• Egland, P. G., Pelletier, D. A., Dispensa, M., Gibson, J. & Harwood, C. S. A cluster of bacterial genes for anaerobic benzene ring biodegradation. Proc. Natl Acad. Sci. USA 94, 6484–6489 (1997). A report on the genes involved in anaerobic benzoate metabolism.
  Article CAS PubMed PubMed Central Google Scholar
• Laempe, D., Jahn, M. & Fuchs, G. 6-Hydroxycyclohex-1-ene-1-carbonyl-CoA dehydrogenase and 6-oxocyclohex-1-ene-1-carbonyl-CoA hydrolase, enzymes of the benzoyl-CoA pathway of anaerobic aromatic metabolism in the denitrifying bacterium Thauera aromatica. Eur. J. Biochem. 263, 420–429 (1999).
  Article CAS PubMed Google Scholar
• Laempe, D., Eisenreich, W., Bacher, A. & Fuchs, G. Cyclohexa-1,5-diene-1-carbonyl-CoA hydratase [corrected], an enzyme involved in anaerobic metabolism of benzoyl-CoA in the denitrifying bacterium Thauera aromatica. Eur. J. Biochem. 255, 618–627 (1998).
  Article CAS PubMed Google Scholar
• Boll, M. & Fuchs, G. Identification and characterization of the natural electron donor ferredoxin and of FAD as a possible prosthetic group of benzoyl-CoA reductase (dearomatizing), a key enzyme of anaerobic aromatic metabolism. Eur. J. Biochem. 251, 946–954 (1998).
  Article CAS PubMed Google Scholar
• Boll, M., Fuchs, G., Tilley, G., Armstrong, F. A. & Lowe, D. J. Unusual spectroscopic and electrochemical properties of the 2[4Fe-4S] ferredoxin of Thauera aromatica. Biochemistry 39, 4929–4938 (2000).
  Article CAS PubMed Google Scholar
• Boll, M., Fuchs, G., Meier, C., Trautwein, A. & Lowe, D. J. EPR and Mössbauer studies of benzoyl-CoA reductase. J. Biol. Chem. 275, 31857–31868 (2000).
  Article CAS PubMed Google Scholar
• Thiele, B., Rieder, O., Golding, B. T., Müller, M. & Boll, M. Mechanism of enzymatic Birch reduction: stereochemical course and exchange reactions of benzoyl-CoA reductase. J. Am. Chem. Soc. 130, 14050–14051 (2008).
  Article CAS PubMed Google Scholar
• Peters, F., Rother, M. & Boll, M. Selenocysteine-containing proteins in anaerobic benzoate metabolism of Desulfococcus multivorans. J. Bacteriol. 186, 2156–2163 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Holmes, D. E., Risso, C., Smith, J. A. & Lovley, D. R. Anaerobic oxidation of benzene by the hyperthermophilic archaeon Ferroglobus placidus. Appl. Environm. Microbiol. 77, 5926–5933 (2011).
  Article CAS Google Scholar
• Kung, J. W. et al. Identification and characterization of the tungsten-containing class of benzoyl-coenzyme A reductases. Proc. Natl Acad. Sci. USA 106, 17687–17692 (2009). The first description of an ATP-independent benzoyl-CoA reductase.
  Article CAS PubMed PubMed Central Google Scholar
• Kuntze, K. et al. 6-Oxocyclohex-1-ene-1-carbonyl-coenzyme A hydrolases from obligately anaerobic bacteria: characterization and identification of its gene as a functional marker for aromatic compounds degrading anaerobes. Environ. Microbiol. 10, 1547–1556 (2008).
  Article CAS PubMed Google Scholar
• Peters, F., Shinoda, Y., McInerney, M. J. & Boll, M. 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 (2007).
  Article CAS PubMed Google Scholar
• Wischgoll, S. et al. Gene clusters involved in anaerobic benzoate degradation of Geobacter metallireducens. Mol. Microbiol. 58, 1238–1252 (2005).
  Article CAS PubMed Google Scholar
• Löffler, C. et al. Occurrence, genes and expression of the W/Se-containing class II benzoyl-coenzyme A reductases in anaerobic bacteria. Environ. Microbiol. 13, 696–709 (2011).
  Article PubMed CAS Google Scholar
• Heintz, D. et al. Differential membrane proteome analysis reveals novel proteins involved in the degradation of aromatic compounds in Geobacter metallireducens. Mol. Cell. Proteomics 8, 2159–2169 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Kaster, A. K., Moll, J., Parey, K. & Thauer, R. K. Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea. Proc. Natl Acad. Sci. USA 108, 2981–2986 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Thauer, R. K., Kaster, A. K., Seedorf, H., Buckel, W. & Hedderich, R. Methanogenic archaea: ecologically relevant differences in energy conservation. Nature Rev. Microbiol. 6, 579–591 (2008).
  Article CAS Google Scholar
• Wang, S., Huang, H., Moll, J. & Thauer, R. K. NADP+ reduction with reduced ferredoxin and NADP+ reduction with NADH are coupled via an electron-bifurcating enzyme complex in Clostridium kluyveri. J. Bacteriol. 192, 5115–5123 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Herrmann, G., Jayamani, E., Mai, G. & Buckel, W. Energy conservation via electron-transferring flavoprotein in anaerobic bacteria. J. Bacteriol. 190, 784–791 (2008).
  Article CAS PubMed Google Scholar
• Li, F. et al. 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 (2008).
  Article CAS PubMed Google Scholar
• Parales, R. E., Parales, J. V., Pelletier, D. A. & Ditty, J. L. Diversity of microbial toluene degradation pathways. Adv. Appl. Microbiol. 64, 1–73 (2008).
  Article CAS PubMed Google Scholar
• Heider, J. & Rabus, R. in Microbial Biodegradation: Genomics and Molecular Biology (ed. Díaz, E.) 25–54 (Caister Academic, Norfolk, 2008).
  Google Scholar
• Heider, J. Adding handles to unhandy substrates: anaerobic hydrocarbon activation mechanisms. Curr. Opin. Chem. Biol. 11, 188–194 (2007).
  Article CAS PubMed Google Scholar
• Evans, P. J., Ling, W., Goldschmidt, B., Ritter, E. R. & Young, L. Y. Metabolites formed during anaerobic transformation of toluene and _o_-xylene and their proposed relationship to the initial steps of toluene mineralization. Appl. Environ. Microbiol. 58, 496–501 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Beller, H. R., Reinhard, M. & Grbić-Galić, D. Metabolic by-products of anaerobic toluene degradation by sulfate-reducing enrichment cultures. Appl. Environ. Microbiol. 58, 3192–3195 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Seyfried, B., Glod, G., Schocher, R., Tschech, A. & Zeyer, J. Initial reactions in the anaerobic oxidation of toluene and _m_-xylene by denitrifying bacteria. Appl. Environ. Microbiol. 60, 4047–4052 (1994).
  Article CAS PubMed PubMed Central Google Scholar
• Migaud, M. E., Chee-Sanford, J. C., Tiedje, J. M. & Frost, J. W. Benzylfumaric, benzylmaleic, and _Z_- and _E_-phenylitaconic acids: synthesis, characterization, and correlation with a metabolite generated by Azoarcus tolulyticus Tol-4 during anaerobic toluene degradation. Appl. Environ. Microbiol. 62, 974–978 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Biegert, T., Fuchs, G. & Heider, J. 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 (1996). A classic paper demonstrating that the addition of fumarate to a hydrocarbon constitutes the initial attack not only on toluene, but also on various other hydrocarbon compounds.
  Article CAS PubMed Google Scholar
• Beller, H. R. & Spormann, A. M. Analysis of the novel benzylsuccinate synthase reaction for anaerobic toluene activation based on structural studies of the product. J. Bacteriol. 180, 5454–5457 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Leutwein, C. & Heider, J. Anaerobic toluene-catabolic pathway in denitrifying Thauera aromatica: activation and β-oxidation of the first intermediate, (R)-(+)-benzylsuccinate. Microbiology 145, 3265–3271 (1999).
  Article CAS PubMed Google Scholar
• Leuthner, B. et al. 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 (1998).
  Article CAS PubMed Google Scholar
• Leuthner, B. & Heider, J. Anaerobic toluene catabolism of Thauera aromatica: a toluene-induced operon codes for the enzymes of β-oxidation of the intermediate benzylsuccinate. J. Bacteriol. 182, 272–277 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Hermuth, K., Leuthner, B. & Heider, J. Operon structure and expression of the genes for benzylsuccinate synthase in Thauera aromatica strain K172. Arch. Microbiol. 177, 132–138 (2002).
  Article CAS PubMed Google Scholar
• Kühner, S. et al. Substrate-dependent regulation of anaerobic degradation pathways for toluene and ethylbenzene in a denitrifying bacterium, strain EbN1. J. Bacteriol. 187, 1493–1503 (2005).
  Article PubMed PubMed Central CAS Google Scholar
• Heider, J., Spormann, A. M., Beller, H. R. & Widdel, F. Anaerobic bacterial metabolism of hydrocarbons. FEMS Microbiol. Rev. 22, 459–473 (1998). A summary of the early findings on anaerobic degradation of hydrocarbon compounds.
  Article CAS Google Scholar
• Leutwein, C. & Heider, J. Succinyl-CoA: (R)-benzylsuccinate CoA-transferase: an enzyme of the anaerobic toluene catabolic pathway in denitrifying bacteria. J. Bacteriol. 183, 4288–4295 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Grundmann, O. et al. Genes encoding a tentative enzyme for anaerobic activation of _n_-alkanes in the denitrifying bacterium, strain HxN1. Environ. Microbiol. 10, 376–385 (2008).
  Article CAS PubMed Google Scholar
• Rabus, R. & Heider, J. Initial reactions of anaerobic metabolism of alkylbenzenes in denitrifying and sulfate-reducing bacteria. Arch. Microbiol. 170, 377–384 (1998).
  Article CAS Google Scholar
• Ball, H. A., Johnson, H. A., Reinhard, M. & Spormann, A. M. Initial reactions in anaerobic ethylbenzene oxidation by a denitrifying bacterium, strain EB1. J. Bacteriol. 178, 5755–5761 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Kniemeyer, O. & Heider, J. Ethylbenzene dehydrogenase, a novel hydrocarbon-oxidising molybdenum/iron-sulfur/heme enzyme. J. Biol. Chem. 276, 21381–21386 (2001).
  Article CAS PubMed Google Scholar
• Johnson, H. A., Pelletier, D. A. & Spormann, A. M. Isolation and characterization of anaerobic ethylbenzene dehydrogenase, a novel Mo-Fe-S. enzyme. J. Bacteriol. 183, 4536–4542 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Kloer, D. P., Hagel, C., Heider, J. & Schulz, G. E. Crystal Structure of ethylbenzene dehydrogenase from Aromatoleum aromaticum. Structure 14, 1377–1388 (2006). The elucidation of the structure of ethylbenzene dehydrogenase.
  Article CAS PubMed Google Scholar
• Szaleniec, M. et al. Kinetics and mechanism of oxygen-independent hydrocarbon-hydroxylation by ethylbenzene dehydrogenase. Biochemistry 46, 7637–7646 (2007).
  Article CAS PubMed Google Scholar
• Szaleniec, M., Borowski, T., Schühle, K., Witko, M. & Heider, J. Ab inito modelling of ethylbenzene dehydrogenase reaction mechanism. J. Am. Chem. Soc. 132, 6014–6024 (2010).
  Article CAS PubMed Google Scholar
• Höffken, H. W. et al. Crystal structure and enzyme kinetics of the (S)-specific 1-phenylethanol dehydrogenase of the denitrifying bacterium strain EbN1. Biochemistry 45, 82–93 (2006).
  Article PubMed CAS Google Scholar
• Jobst, B., Schühle, K., Linne, U. & Heider, J. ATP-dependent carboxylation of acetophenone by a novel type of carboxylase. J. Bacteriol. 192, 1387–1394 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, X. & Young, L. Y. Carboxylation as an initial reaction in the anaerobic metabolism of naphthalene and phenanthrene by sulfidogenic consortia. Appl. Environ. Microbiol. 63, 4759–4764 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Kunapuli, U, Griebler, C., Beller, H. R. & Meckenstock, R. U. Identification of intermediates formed during anaerobic benzene degradation by an iron-reducing enrichment culture. Environ. Microbiol. 10, 1703–1710 (2008).
  Article CAS PubMed Google Scholar
• Abu Laban, N., Selesi, D., Rattei, T., Tischler, P. & Meckenstock, R. U. Identification of enzymes involved in anaerobic benzene degradation by a strictly anaerobic iron-reducing enrichment culture. Environ. Microbiol. 12, 2783–2796 (2010).
  CAS PubMed Google Scholar
• Bergmann, F. D., Selesi, D. & Meckenstock, R. U. Identification of new enzymes potentially involved in anaerobic naphthalene degradation by the sulfate-reducing enrichment culture N47. Arch. Microbiol. 193, 241–250 (2011).
  Article CAS PubMed Google Scholar
• Schühle, K. & Fuchs, G. Phenylphosphate carboxylase: a new C-C lyase involved in anaerobic phenol metabolism in Thauera aromatica. J. Bacteriol. 186, 4556–4567 (2004).
  Article PubMed PubMed Central CAS Google Scholar
• Huang, J., He, Z. & Wiegel, J. Cloning, characterization, and expression of a novel gene encoding a reversible 4-hydroxybenzoate decarboxylase from Clostridium hydroxybenzoicum. J. Bacteriol. 181, 5119–5122 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Gerischer, U. Specific and global regulators of genes associated with the degradation of aromatic compounds in bacteria. J. Mol. Microbiol. Biotechnol. 4, 111–121 (2002).
  CAS PubMed Google Scholar
• Carmona, M., Prieto, M. A., Galán, B., García, J. L. & Díaz, E. in Microbial Biodegradation (ed. Díaz, E.) 99–143 (Caister Academic, Norfolk, 2008).
  Google Scholar
• Durante-Rodríguez, G. et al. Biochemical characterization of the transcriptional regulator BzdR from Azoarcus sp. CIB. J. Biol. Chem. 285, 35694–35705 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Dispensa, M. et al. Anaerobic growth of Rhodopseudomonas palustris on 4-hydroxybenzoate is dependent on AadR, a member of the cyclic AMP receptor protein family of transcriptional regulators. J. Bacteriol. 174, 5803–5813 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Egland, P. G. & Harwood, C. S. BadR, a new MarR family member, regulates anaerobic benzoate degradation by Rhodopseudomonas palustris in concert with AadR, an FNR family member. J. Bacteriol. 181, 2102–2109 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Juárez, J. F. et al. Identification of the Geobacter metallireducens bamVW two-component system, involved in transcriptional regulation of aromatic degradation. Appl. Environ. Microbiol. 76, 383–385 (2010).
  Article PubMed CAS Google Scholar
• Lau, P. C. et al. A bacterial basic region leucine zipper histidine kinase regulating toluene degradation. Proc. Natl Acad. Sci. USA 94, 1453–1458 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Leuthner, B. & Heider, J. A two-component system involved in regulation of anaerobic toluene metabolism in Thauera aromatica. FEMS Microbiol. Lett. 166, 35–41 (1998).
  Article CAS PubMed Google Scholar
• Shingler, V., Bartilson, M. & Moore, T. Cloning and nucleotide sequence of the gene encoding the positive regulator (DmpR) of the phenol catabolic pathway encoded by pVI150 and identification of DmpR as a member of the NtrC family of transcriptional activators. J. Bacteriol. 175, 1596–1604 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Breinig, S., Schiltz, E. & Fuchs, G. Genes involved in anaerobic metabolism of phenol in the bacterium Thauera aromatica. J. Bacteriol. 182, 5849–5863 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Prieto, M. A. et al. Aromatic metabolism versus carbon availability: the regulatory network that controls catabolism of less-preferred carbon sources in Escherichia coli. FEMS Microbiol Rev. 28, 503–518 (2004).
  Article CAS PubMed Google Scholar
• Kurbatov, L., Albrecht, D., Herrmann, H. & Petruschka, L. Analysis of the proteome of Pseudomonas putida KT2440 grown on different sources of carbon and energy. Environ. Microbiol. 8, 466–478 (2006).
  Article CAS PubMed Google Scholar
• Petruschka, L., Burchhardt, G., Müller, C., Weihe, C. & Herrmann, H. The cyo operon of Pseudomonas putida is involved in carbon catabolite repression of phenol degradation. Mol. Genet. Genomics 266, 199–206 (2001).
  Article CAS PubMed Google Scholar
• Barragán, M. J. L. et al. The bzd gene cluster, coding for anaerobic benzoate catabolism, in Azoarcus sp. strain CIB. J. Bacteriol. 186, 5762–5774 (2004).
  Article PubMed Central CAS Google Scholar
• Wöhlbrand, L. et al. Functional proteomic view of metabolic regulation in “_Aromatoleum aromaticum_” strain EbN1. Proteomics 7, 2222–2239 (2007).
  Article PubMed CAS Google Scholar
• Pelletier, D. A. & Harwood, C. S. 2-Hydroxycyclohexanecarboxyl coenzyme A dehydrogenase, an enzyme characteristic of the anaerobic benzoate degradation pathway used by Rhodopseudomonas palustris. J. Bacteriol. 182, 2753–2760 (2000).
  Article CAS PubMed PubMed Central Google Scholar