Catabolic Pathways and Enzymes Involved in the Anaerobic Degradation of Monocyclic Aromatic Compounds

Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)


Monocyclic aromatic compounds (MAC) comprise the second most abundant class of natural compounds, many of which are hazardous for the environment and human health. MAC can readily be degraded by many aerobic microorganisms by the extensive using of oxygenases for aromatic ring hydroxylation and cleavage. However, under anoxic conditions, this strategy is not an option and MAC degrading anaerobic prokaryotes employ a totally different enzyme inventory for attacking the resonance-stabilized aromatic ring system or the C–H bond of alky chains from aromatic hydrocarbons. The anaerobic degradation of MAC has become a treasure trove for the discovery of unprecedented enzymatic principles; many involve metalloenzymes catalyzing radical-based reactions. Characteristic enzymatic reactions involved in anaerobic MAC degradation comprise: (i) the addition of alkylated aromatics to fumarate by glycyl-radical enzymes, (ii) the water-dependent hydroxylation or transhydroxylation of MAC by Mo- or flavin-dependent enzymes, (iii) the carboxylation/decarboxylation of aromatic rings by UbiD-/UbiX-like enzyme systems, and (iv) the dearomatization of aromatics rings by ATP-dependent FeS-enzymes or ATP-independent W-enzymes. The multitude of MAC is converted via peripheral channeling pathways to only a few central intermediates that serve as substrates for dearomatizing ring reductases. Depending on the nature of these central intermediates, we divide the anaerobic MAC degradation pathways into five subgroups and highlight the individual characteristic enzymatic steps involved.


  1. Abu Laban N, Selesi D, Jobelius C, Meckenstock RU (2009) Anaerobic benzene degradation by gram-positive sulfate-reducing bacteria. FEMS Microbiol Ecol 68:300–311PubMedPubMedCentralCrossRefGoogle Scholar
  2. Abu Laban N, Selesi D, Rattei T, Tischler P, Meckenstock RU (2010) Identification of enzymes involved in anaerobic benzene degradation by a strictly anaerobic iron-reducing enrichment culture. Environ Microbiol 12:2783–2796PubMedPubMedCentralGoogle Scholar
  3. Ahn Y, Chae J, Zylstra GJ, Häggblom MM (2009) Degradation of phenol via phenylphosphate and carboxylation to 4-hydroxybenzoate by a newly isolated strain of the sulfate-reducing bacterium Desulfobacterium anilini. Appl Environ Microbiol 75:4248–4253PubMedPubMedCentralCrossRefGoogle Scholar
  4. Aklujkar M, Risso C, Smith J, Beaulieu D, Dubay R, Giloteaux L, DiBurro K, Holmes D (2014) Anaerobic degradation of aromatic amino acids by the hyperthermophilic archaeon Ferroglobus placidus. Microbiology 160:2694–2709PubMedPubMedCentralCrossRefGoogle Scholar
  5. Ball HA, Johnson HA, Reinhard M, Spormann AM (1996) Initial reactions in anaerobic ethylbenzene oxidation by a denitrifying bacterium, strain EB1. J Bacteriol 178:5755–5761PubMedPubMedCentralCrossRefGoogle Scholar
  6. Barker HA (1981) Amino acid degradation by anaerobic bacteria. Annu Rev Biochem 50:23–40PubMedPubMedCentralCrossRefGoogle Scholar
  7. Biegert T, Altenschmidt U, Eckerskorn C, Fuchs G (1993) Enzymes of anaerobic metabolism of phenolic compounds. 4-Hydroxybenzoate-CoA ligase from a denitrifying Pseudomonas species. Eur J Biochem 213:555–561PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bisaillon JG, Lépine F, Beaudet R, Sylvestre M (1991) Carboxylation of o-cresol by an anaerobic consortium under methanogenic conditions. Appl Environ Microbiol 57:2131–2134PubMedPubMedCentralCrossRefGoogle Scholar
  9. 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 234:921–933PubMedPubMedCentralCrossRefGoogle Scholar
  10. Boll M, Fuchs G (1998) 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 251:946–954PubMedPubMedCentralCrossRefGoogle Scholar
  11. Boll M, Albracht SS, Fuchs G (1997) 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 244:840–851PubMedPubMedCentralCrossRefGoogle Scholar
  12. Boll M, Fuchs G, Meier C, Trautwein A, El Kasmi A, Ragsdale SW, Buchanan G, Lowe DJ (2001) Redox centers of 4-hydroxybenzoyl-CoA reductase, a member of the xanthine oxidase family of molybdenum-containing enzymes. J Biol Chem 276:47853–47862PubMedPubMedCentralCrossRefGoogle Scholar
  13. Boll M, Löffler C, Morris BE, Kung JW (2014) Anaerobic degradation of homocyclic aromatic compounds via arylcarboxyl-coenzyme A esters: organisms, strategies and key enzymes. Environ Microbiol 16:612–627PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bonting CF, Fuchs G (1996) Anaerobic metabolism of 2-hydroxybenzoic acid (salicylic acid) by a denitrifying bacterium. Arch Microbiol 165:402–408PubMedPubMedCentralCrossRefGoogle Scholar
  15. Brackmann R, Fuchs G (1993) Enzymes of anaerobic metabolism of phenolic compounds. 4-Hydroxybenzoyl-CoA reductase (dehydroxylating) from a denitrifying Pseudomonas species. Eur J Biochem 213:563–571PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bräsen C, Schönheit P (2004) Unusual ADP-forming acetyl-coenzyme A synthetases from the mesophilic halophilic euryarchaeon Haloarcula marismortui and from the hyperthermophilic crenarchaeon Pyrobaculum aerophilum. Arch Microbiol 182:277–287PubMedPubMedCentralCrossRefGoogle Scholar
  17. Breese K, 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 251:916–923PubMedPubMedCentralCrossRefGoogle Scholar
  18. Breinig S, Schiltz E, Fuchs G (2000) Genes involved in anaerobic metabolism of phenol in the bacterium Thauera aromatica. J Bacteriol 182:5849–5863PubMedPubMedCentralCrossRefGoogle Scholar
  19. Brune A, Schnell S, Schink B (1992) Sequential transhydroxylations converting hydroxyhydroquinone to phloroglucinol in the strictly anaerobic, fermentative bacterium Pelobacter massiliensis. Appl Environ Microbiol 58:1861–1868PubMedPubMedCentralCrossRefGoogle Scholar
  20. Buckel W, Thauer RK (2013) Energy conservation via electron bifurcating ferredoxin reduction and proton/Na(+) translocating ferredoxin oxidation. Biochim Biophys Acta 1827:94–113PubMedPubMedCentralCrossRefGoogle Scholar
  21. Buckel W, Zhang J, Friedrich P, Parthasarathy A, Li H, Djurdjevic I, Dobbek H, Martins BM (2012) Enzyme catalyzed radical dehydrations of hydroxy acids. Biochim Biophys Acta 1824:1278–1290PubMedPubMedCentralCrossRefGoogle Scholar
  22. Buckel W, Kung JW, Boll M (2014) The benzoyl-coenzyme a reductase and 2-hydroxyacyl-coenzyme a dehydratase radical enzyme family. Chembiochem 15:2188–2194PubMedPubMedCentralCrossRefGoogle Scholar
  23. Carmona M, Zamarro MT, Blázquez B, Durante-Rodríguez G, Juárez JF, Valderrama JA, Barragán MJL, García JL, Díaz E (2009) Anaerobic catabolism of aromatic compounds: a genetic and genomic view. Microbiol Mol Biol Rev 73:71–133PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cunane LM, Chen ZW, Shamala N, Mathews FS, Cronin CN, McIntire WS (2000) Structures of the flavocytochrome p-cresol methylhydroxylase and its enzyme-substrate complex: gated substrate entry and proton relays support the proposed catalytic mechanism. J Mol Biol 295:357–374PubMedPubMedCentralCrossRefGoogle Scholar
  25. Darley PI, Hellstern JA, Medina-Bellver JI, Marqués S, Schink B, Philipp B (2007) Heterologous expression and identification of the genes involved in anaerobic degradation of 1,3-dihydroxybenzene (resorcinol) in Azoarcus anaerobius. J Bacteriol 189:3824–3833PubMedPubMedCentralCrossRefGoogle Scholar
  26. Debnar-Daumler C, Seubert A, Schmitt G, Heider J (2014) Simultaneous involvement of a tungsten-containing aldehyde: ferredoxin oxidoreductase and a phenylacetaldehyde dehydrogenase in anaerobic phenylalanine metabolism. J Bacteriol 196:483–492PubMedPubMedCentralCrossRefGoogle Scholar
  27. Dermer J, Fuchs G (2012) Molybdoenzyme that catalyzes the anaerobic hydroxylation of a tertiary carbon atom in the side chain of cholesterol. J Biol Chem 287:36905–36916PubMedPubMedCentralCrossRefGoogle Scholar
  28. Díaz E, Jiménez JI, Nogales J (2013) Aerobic degradation of aromatic compounds. Curr Opin Biotechnol 24:431–442PubMedPubMedCentralCrossRefGoogle Scholar
  29. Dickert S, Pierik AJ, Buckel W (2002) Molecular characterization of phenyllactate dehydratase and its initiator from Clostridium sporogenes. Mol Microbiol 44:49–60PubMedPubMedCentralCrossRefGoogle Scholar
  30. Ding B, Schmeling S, Fuchs G (2008) Anaerobic metabolism of catechol by the denitrifying bacterium Thauera aromatica–a result of promiscuous enzymes and regulators? J Bacteriol 190:1620–1630PubMedPubMedCentralCrossRefGoogle Scholar
  31. Ebenau-Jehle C, Thomas M, Scharf G, Kockelkorn D, Knapp B, Schühle K, Heider J, Fuchs G (2012) Anaerobic metabolism of indoleacetate. J Bacteriol 194:2894–2903PubMedPubMedCentralCrossRefGoogle Scholar
  32. Ebenau-Jehle C, Mergelsberg M, Fischer S, Brüls T, Jehmlich N, von Bergen M, Boll M (2016) An unusual strategy for the anoxic biodegradation of phthalate. ISME J 11:224. Scholar
  33. Egland PG, Pelletier DA, Dispensa M, Gibson J, Harwood CS (1997) A cluster of bacterial genes for anaerobic benzene ring biodegradation. Proc Natl Acad Sci USA 94:6484–6489PubMedPubMedCentralCrossRefGoogle Scholar
  34. Egland PG, Gibson J, Harwood CS (2001) Reductive, coenzyme A-mediated pathway for 3-chlorobenzoate degradation in the phototrophic bacterium Rhodopseudomonas palustris. Appl Environ Microbiol 67:1396–1399PubMedPubMedCentralCrossRefGoogle Scholar
  35. Elshahed MS, Gieg LM, Mcinerney MJ, Suflita JM (2001) Signature metabolites attesting to the in situ attenuation of alkylbenzenes in anaerobic environments. Environ Sci Technol 35:682–689PubMedPubMedCentralCrossRefGoogle Scholar
  36. Engelmann T, Kaufmann F, Diekert G (2001) Isolation and characterization of a veratrol: corrinoid protein methyl transferase from Acetobacterium dehalogenans. Arch Microbiol 175:376–383PubMedPubMedCentralCrossRefGoogle Scholar
  37. Evans PJ, Ling W, Goldschmidt B, Ritter ER, Young LY (1992) Metabolites formed during anaerobic transformation of toluene and o-xylene and their proposed relationship to the initial steps of toluene mineralization. Appl Environ Microbiol 58:496–501PubMedPubMedCentralCrossRefGoogle Scholar
  38. Fuchs G, Boll M, Heider J (2011) Microbial degradation of aromatic compounds – from one strategy to four. Nat Rev Microbiol 9:803–816PubMedPubMedCentralCrossRefGoogle Scholar
  39. Funk MA, Marsh E, Neil G, Drennan CL (2015) Substrate-bound structures of benzylsuccinate synthase reveal how toluene is activated in anaerobic hydrocarbon degradation. J Biol Chem 290:22398–22408PubMedPubMedCentralCrossRefGoogle Scholar
  40. Gallus C, Schink B (1998) Anaerobic degradation of alpha-resorcylate by Thauera aromatica strain AR-1 proceeds via oxidation and decarboxylation to hydroxyhydroquinone. Arch Microbiol 169:333–338PubMedPubMedCentralCrossRefGoogle Scholar
  41. Gorny N, Schink B (1994a) Complete anaerobic oxidation of hydroquinone by Desulfococcus sp. strain Hy5: indications of hydroquinone carboxylation to gentisate. Arch Microbiol 162:131–135CrossRefGoogle Scholar
  42. Gorny N, Schink B (1994b) Anaerobic degradation of catechol by Desulfobacterium sp. strain Cat2 proceeds via carboxylation to protocatechuate. Appl Environ Microbiol 60:3396–3400PubMedPubMedCentralCrossRefGoogle Scholar
  43. Gorny N, Schink B (1994c) Hydroquinone degradation via reductive dehydroxylation of gentisyl-CoA by a strictly anaerobic fermenting bacterium. Arch Microbiol 161:25–32CrossRefGoogle Scholar
  44. Haddock JD, Ferry JG (1989) Purification and properties of phloroglucinol reductase from Eubacterium oxidoreducens G-41. J Biol Chem 264:4423–4427PubMedPubMedCentralGoogle Scholar
  45. Harayama S, Kok M, Neidle EL (1992) Functional and evolutionary relationships among diverse oxygenases. Annu Rev Microbiol 46:565–601PubMedPubMedCentralCrossRefGoogle Scholar
  46. Harwood CS, Parales RE (1996) The beta-ketoadipate pathway and the biology of self-identity. Annu Rev Microbiol 50:553–590PubMedPubMedCentralCrossRefGoogle Scholar
  47. Heider J (2001) A new family of CoA-transferases. FEBS Lett 509:345–349PubMedPubMedCentralCrossRefGoogle Scholar
  48. Heider J, Fuchs G (1997a) Anaerobic metabolism of aromatic compounds. Eur J Biochem 243:577–596PubMedPubMedCentralCrossRefGoogle Scholar
  49. Heider J, Fuchs G (1997b) Microbial anaerobic aromatic metabolism. Anaerobe 3:1–22PubMedPubMedCentralCrossRefGoogle Scholar
  50. Heider J, Schühle K (2013) Anaerobic biodegradation of hydrocarbons including methane. In: Rosenberg E, Delong E, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: prokaryotic physiology and biochemistry. Springer, Heidelberg, pp 601–630Google Scholar
  51. Heider J, Spormann AM, Beller HR, Widdel F (1998) Anaerobic bacterial metabolism of hydrocarbons. FEMS Microbiol Rev 22:459–473CrossRefGoogle Scholar
  52. Heider J, Schühle K, Frey J, Schink B (2016a) Activation of acetone and other simple ketones in anaerobic bacteria. J Mol Microbiol Biotechnol 26:152–164PubMedPubMedCentralCrossRefGoogle Scholar
  53. Heider J, Szaleniec M, Martins BM, Seyhan D, Buckel W, Golding BT (2016b) Structure and function of benzylsuccinate synthase and related fumarate-adding glycyl radical enzymes. J Mol Microbiol Biotechnol 26:29–44PubMedPubMedCentralCrossRefGoogle Scholar
  54. Heider J, Szaleniec M, Sünwoldt K, Boll M (2016c) Ethylbenzene dehydrogenase and related molybdenum enzymes involved in oxygen-independent alkyl chain hydroxylation. J Mol Microbiol Biotechnol 26:45–62PubMedPubMedCentralCrossRefGoogle Scholar
  55. Hirsch W, Schägger H, Fuchs G (1998) Phenylglyoxylate:NAD+ oxidoreductase (CoA benzoylating), a new enzyme of anaerobic phenylalanine metabolism in the denitrifying bacterium Azoarcus evansii. Eur J Biochem 251:907–915PubMedPubMedCentralCrossRefGoogle Scholar
  56. Holmes DE, Risso C, Smith JA, Lovley DR (2011) Anaerobic oxidation of benzene by the hyperthermophilic archaeon Ferroglobus placidus. Appl Environ Microbiol 77:5926–5933PubMedPubMedCentralCrossRefGoogle Scholar
  57. Hopper DJ, Taylor DG (1977) The purification and properties of p-cresol-(acceptor) oxidoreductase (hydroxylating), a flavocytochrome from Pseudomonas putida. Biochem J 167:155–162PubMedPubMedCentralCrossRefGoogle Scholar
  58. Hopper DJ, Bossert ID, Rhodes-Roberts ME (1991) p-cresol methylhydroxylase from a denitrifying bacterium involved in anaerobic degradation of p-cresol. J Bacteriol 173:1298–1301PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hug LA, Maphosa F, Leys D, Löffler FE, Smidt H, Edwards EA, Adrian L (2013) Overview of organohalide-respiring bacteria and a proposal for a classification system for reductive dehalogenases. Philos Trans R Soc B Biol Sci 368:20120322CrossRefGoogle Scholar
  60. Jobst B, Schühle K, Linne U, Heider J (2010) ATP-dependent carboxylation of acetophenone by a novel type of carboxylase. J Bacteriol 192:1387–1394PubMedPubMedCentralCrossRefGoogle Scholar
  61. Johannes J, Bluschke A, Jehmlich N, von Bergen M, Boll M (2008) Purification and characterization of active-site components of the putative p-cresol methylhydroxylase membrane complex from Geobacter metallireducens. J Bacteriol 190:6493–6500PubMedPubMedCentralCrossRefGoogle Scholar
  62. Juárez JF, Zamarro MT, Eberlein C, Boll M, Carmona M, Díaz E (2013) Characterization of the mbd cluster encoding the anaerobic 3-methylbenzoyl-CoA central pathway. Environ Microbiol 15:148–166PubMedPubMedCentralCrossRefGoogle Scholar
  63. Junghare M, Spiteller D, Schink B (2016) Enzymes involved in the anaerobic degradation of ortho-phthalate by the nitrate-reducing bacterium Azoarcus sp. strain PA01. Environ Microbiol 18:3175. Scholar
  64. Kaster A, Moll J, Parey K, Thauer RK (2011) Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea. Proc Natl Acad Sci USA 108:2981–2986PubMedPubMedCentralCrossRefGoogle Scholar
  65. Kazumi J, Häggblom MM, Young LY (1995) Diversity of anaerobic microbial processes in chlorobenzoate degradation: nitrate, iron, sulfate and carbonate as electron acceptors. Appl Microbiol Biotechnol 43:929–936PubMedPubMedCentralCrossRefGoogle Scholar
  66. Kloer DP, Hagel C, Heider J, Schulz GE (2006) Crystal structure of ethylbenzene dehydrogenase from Aromatoleum aromaticum. Structure 14:1377–1388PubMedPubMedCentralCrossRefGoogle Scholar
  67. Kluge C, Tschech A, Fuchs G (1990) Anaerobic metabolism of resorcylic acids (m-dihydroxybenzoic acids) and resorcinol (1,3-benzenediol) in a fermenting and in a denitrifying bacterium. Arch Microbiol 155:68–74CrossRefGoogle Scholar
  68. Kniemeyer O, Heider J (2001a) Ethylbenzene dehydrogenase, a novel hydrocarbon-oxidizing molybdenum/iron-sulfur/heme enzyme. J Biol Chem 276:21381–21386PubMedPubMedCentralCrossRefGoogle Scholar
  69. Kniemeyer O, Heider J (2001b) (S)-1-phenylethanol dehydrogenase of Azoarcus sp. strain EbN1, an enzyme of anaerobic ethylbenzene catabolism. Arch Microbiol 176:129–135PubMedPubMedCentralCrossRefGoogle Scholar
  70. Koch J, Eisenreich W, Bacher A, Fuchs G (1993) Products of enzymatic reduction of benzoyl-CoA, a key reaction in anaerobic aromatic metabolism. Eur J Biochem 211:649–661PubMedPubMedCentralCrossRefGoogle Scholar
  71. 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 181:6403–6410PubMedPubMedCentralCrossRefGoogle Scholar
  72. Kunapuli U, Griebler C, Beller HR, Meckenstock RU (2008) Identification of intermediates formed during anaerobic benzene degradation by an iron-reducing enrichment culture. Environ Microbiol 10:1703–1712PubMedPubMedCentralCrossRefGoogle Scholar
  73. Kung JW, Löffler C, Dörner K, Heintz D, Gallien S, van Dorsselaer A, Friedrich T, Boll M (2009) Identification and characterization of the tungsten-containing class of benzoyl-coenzyme A reductases. Proc Natl Acad Sci USA 106:17687–17692PubMedPubMedCentralCrossRefGoogle Scholar
  74. Kung JW, Baumann S, von Bergen M, Müller M, Hagedoorn P, Hagen WR, Boll M (2010) Reversible biological Birch reduction at an extremely low redox potential. J Am Chem Soc 132:9850–9856PubMedPubMedCentralCrossRefGoogle Scholar
  75. Kuntze K, Shinoda Y, Moutakki H, McInerney MJ, Vogt C, Richnow H, Boll M (2008) 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 10:1547–1556PubMedPubMedCentralCrossRefGoogle Scholar
  76. Kuntze K, Vogt C, Richnow H, Boll M (2011a) Combined application of PCR-based functional assays for the detection of aromatic-compound-degrading anaerobes. Appl Environ Microbiol 77:5056–5061PubMedPubMedCentralCrossRefGoogle Scholar
  77. Kuntze K, Kiefer P, Baumann S, Seifert J, von Bergen M, Vorholt JA, Boll M (2011b) Enzymes involved in the anaerobic degradation of meta-substituted halobenzoates. Mol Microbiol 82:758–769PubMedPubMedCentralCrossRefGoogle Scholar
  78. Lack A, Fuchs G (1994) Evidence that phenol phosphorylation to phenylphosphate is the first step in anaerobic phenol metabolism in a denitrifying Pseudomonas sp. Arch Microbiol 161:132–139PubMedPubMedCentralGoogle Scholar
  79. Laempe D, Eisenreich W, Bacher A, Fuchs G (1998) 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 255:618–627PubMedPubMedCentralCrossRefGoogle Scholar
  80. Laempe D, Jahn M, Fuchs G (1999) 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 263:420–429PubMedPubMedCentralCrossRefGoogle Scholar
  81. Laempe D, Jahn M, Breese K, Schägger H, Fuchs G (2001) Anaerobic metabolism of 3-hydroxybenzoate by the denitrifying bacterium Thauera aromatica. J Bacteriol 183:968–979PubMedPubMedCentralCrossRefGoogle Scholar
  82. Lahme S, Eberlein C, Jarling R, Kube M, Boll M, Wilkes H, Reinhardt R, Rabus R (2012) Anaerobic degradation of 4-methylbenzoate via a specific 4-methylbenzoyl-CoA pathway. Environ Microbiol 14:1118–1132PubMedPubMedCentralCrossRefGoogle Scholar
  83. Leuthner B, Heider J (2000) Anaerobic toluene catabolism of Thauera aromatica: the bbs operon codes for enzymes of β-oxidation of the intermediate benzylsuccinate. J Bacteriol 182:272–277PubMedPubMedCentralCrossRefGoogle Scholar
  84. Leuthner B, Leutwein C, Schulz H, Hörth P, Haehnel W, Schiltz E, Schägger H, Heider J (1998) Biochemical and genetic characterization of benzylsuccinate synthase from Thauera aromatica: a new glycyl radical enzyme catalysing the first step in anaerobic toluene metabolism. Mol Microbiol 28:615–628PubMedPubMedCentralCrossRefGoogle Scholar
  85. Lochmeyer C, Koch J, Fuchs G (1992) Anaerobic degradation of 2-aminobenzoic acid (anthranilic acid) via benzoyl-coenzyme A (CoA) and cyclohex-1-enecarboxyl-CoA in a denitrifying bacterium. J Bacteriol 174:3621–3628PubMedPubMedCentralCrossRefGoogle Scholar
  86. Löffler C, Kuntze K, Vazquez JR, Rugor A, Kung JW, Böttcher A, Boll M (2011) Occurrence, genes and expression of the W/Se-containing class II benzoyl-coenzyme A reductases in anaerobic bacteria. Environ Microbiol 13:696–709PubMedPubMedCentralCrossRefGoogle Scholar
  87. Luo F, Gitiafroz R, Devine CE, Gong Y, Hug LA, Raskin L, Edwards EA (2014) Metatranscriptome of an anaerobic benzene-degrading, nitrate-reducing enrichment culture reveals involvement of carboxylation in benzene ring activation. Appl Environ Microbiol 80:4095–4107PubMedPubMedCentralCrossRefGoogle Scholar
  88. Mai X, Adams MW (1994) Indolepyruvate ferredoxin oxidoreductase from the hyperthermophilic archaeon Pyrococcus furiosus. A new enzyme involved in peptide fermentation. J Biol Chem 269:16726–16732PubMedPubMedCentralGoogle Scholar
  89. Mai X, Adams MW (1996) Purification and characterization of two reversible and ADP-dependent acetyl coenzyme A synthetases from the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 178:5897–5903PubMedPubMedCentralCrossRefGoogle Scholar
  90. McIntire W, Hopper DJ, Singer TP (1985) p-cresol methylhydroxylase. Assay and general properties. Biochem J 228:325–335PubMedPubMedCentralCrossRefGoogle Scholar
  91. Meckenstock RU, Boll M, Mouttaki H, Koelschbach JS, Cunha Tarouco P, Weyrauch P, Dong X, Himmelberg AM (2016) Anaerobic degradation of benzene and polycyclic aromatic hydrocarbons. J Mol Microbiol Biotechnol 26:92–118PubMedPubMedCentralCrossRefGoogle Scholar
  92. Messerschmidt A, Niessen H, Abt D, Einsle O, Schink B, Kroneck PM (2004) Crystal structure of pyrogallol-phloroglucinol transhydroxylase, an Mo enzyme capable of intermolecular hydroxyl transfer between phenols. Proc Natl Acad Sci USA 101:11571–11576PubMedPubMedCentralCrossRefGoogle Scholar
  93. Möbitz H, Boll M (2002) A Birch-like mechanism in enzymatic benzoyl-CoA reduction: a kinetic study of substrate analogues combined with an ab initio model. Biochemistry 41:1752–1758PubMedPubMedCentralCrossRefGoogle Scholar
  94. Morasch B, Meckenstock RU (2005) Anaerobic degradation of p-xylene by a sulfate-reducing enrichment culture. Curr Microbiol 51:127–130PubMedPubMedCentralCrossRefGoogle Scholar
  95. Morasch B, Schink B, Tebbe CC, Meckenstock RU (2004) Degradation of o-xylene and m-xylene by a novel sulfate-reducer belonging to the genus Desulfotomaculum. Arch Microbiol 181:407–417PubMedPubMedCentralCrossRefGoogle Scholar
  96. Muhr E, Schühle K, Clermont L, Sünwoldt K, Kleinsorge D, Seyhan D, Kahnt J, Schall I, Cordero PR, Schmitt G, Heider J (2015) Enzymes of anaerobic ethylbenzene and p-ethylphenol catabolism in ‘Aromatoleum aromaticum’: differentiation and differential induction. Arch Microbiol 197:1051–1062PubMedPubMedCentralCrossRefGoogle Scholar
  97. Muhr E, Leicht O, González Sierra S, Thanbichler M, Heider J (2016) A fluorescent bioreporter for acetophenone and 1-phenylethanol derived from a specifically induced catabolic operon. Front Microbiol 6:1561PubMedPubMedCentralCrossRefGoogle Scholar
  98. Müller JA, Schink B (2000) Initial steps in the fermentation of 3-hydroxybenzoate by Sporotomaculum hydroxybenzoicum. Arch Microbiol 173:288–295PubMedPubMedCentralCrossRefGoogle Scholar
  99. 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 172:287–294PubMedPubMedCentralCrossRefGoogle Scholar
  100. 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 183:752–757PubMedPubMedCentralCrossRefGoogle Scholar
  101. Narmandakh A, Gad’on N, Drepper F, Knapp B, Haehnel W, Fuchs G (2006) Phosphorylation of phenol by phenylphosphate synthase: role of histidine phosphate in catalysis. J Bacteriol 188:7815–7822PubMedPubMedCentralCrossRefGoogle Scholar
  102. Nobu MK, Narihiro T, Hideyuki T, Qiu Y, Sekiguchi Y, Woyke T, Goodwin L, Davenport KW, Kamagata Y, Liu W (2015) The genome of Syntrophorhabdus aromaticivorans strain UI provides new insights for syntrophic aromatic compound metabolism and electron flow. Environ Microbiol 17:4861–4872PubMedPubMedCentralCrossRefGoogle Scholar
  103. Paizs C, Bartlewski-Hof U, Rétey J (2007) Investigation of the mechanism of action of pyrogallol-phloroglucinol transhydroxylase by using putative intermediates. Chemistry 13:2805–2811PubMedPubMedCentralCrossRefGoogle Scholar
  104. Parthasarathy A, Kahnt J, Chowdhury NP, Buckel W (2013) Phenylalanine catabolism in Archaeoglobus fulgidus VC-16. Arch Microbiol 195:781–797PubMedPubMedCentralCrossRefGoogle Scholar
  105. Payne KA, White MD, Fisher K, Khara B, Bailey SS, Parker D, Rattray NJ, Trivedi DK, Goodacre R, Beveridge R, Barran P, Rigby SE, Scrutton NS, Hay S, Leys D (2015) New cofactor supports α,β-unsaturated acid decarboxylation via 1,3-dipolar cycloaddition. Nature 522:497–501PubMedPubMedCentralCrossRefGoogle Scholar
  106. Peters F, Shinoda Y, McInerney MJ, Boll M (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 189:1055–1060PubMedPubMedCentralCrossRefGoogle Scholar
  107. Philipp B, Schink B (1998) Evidence of two oxidative reaction steps initiating anaerobic degradation of resorcinol (1,3-dihydroxybenzene) by the denitrifying bacterium Azoarcus anaerobius. J Bacteriol 180:3644–3649PubMedPubMedCentralCrossRefGoogle Scholar
  108. Philipp B, Schink B (2012) Different strategies in anaerobic biodegradation of aromatic compounds: nitrate reducers versus strict anaerobes. Environ Microbiol Rep 4:469–478PubMedPubMedCentralCrossRefGoogle Scholar
  109. Porter AW, Young LY (2013) The bamA gene for anaerobic ring fission is widely distributed in the environment. Front Microbiol 4:302PubMedPubMedCentralCrossRefGoogle Scholar
  110. Qiu Y, Sekiguchi Y, Imachi H, Kamagata Y, Tseng I, Cheng S, Ohashi A, Harada H (2004) Identification and isolation of anaerobic, syntrophic phthalate isomer-degrading microbes from methanogenic sludges treating wastewater from terephthalate manufacturing. Appl Environ Microbiol 70:1617–1626PubMedPubMedCentralCrossRefGoogle Scholar
  111. Qiu Y, Sekiguchi Y, Hanada S, Imachi H, Tseng I, Cheng S, Ohashi A, Harada H, Kamagata Y (2006) Pelotomaculum terephthalicum sp. nov. and Pelotomaculum isophthalicum sp. nov.: two anaerobic bacteria that degrade phthalate isomers in syntrophic association with hydrogenotrophic methanogens. Arch Microbiol 185:172–182PubMedPubMedCentralCrossRefGoogle Scholar
  112. Qiu Y, Hanada S, Ohashi A, Harada H, Kamagata Y, Sekiguchi Y (2008) Syntrophorhabdus aromaticivorans gen. nov., sp. nov., the first cultured anaerobe capable of degrading phenol to acetate in obligate syntrophic associations with a hydrogenotrophic methanogen. Appl Environ Microbiol 74:2051–2058PubMedPubMedCentralCrossRefGoogle Scholar
  113. Rabus R, Heider J (1998) Initial reactions of anaerobic metabolism of alkylbenzenes in denitrifying and sulfate-reducing bacteria. Arch Microbiol 170:377–384CrossRefGoogle Scholar
  114. Rabus R, Widdel F (1995) Anaerobic degradation of ethylbenzene and other aromatic hydrocarbons by new denitrifying bacteria. Arch Microbiol 163:96–103PubMedPubMedCentralCrossRefGoogle Scholar
  115. Rabus R, Kube M, Heider J, Beck A, Heitmann K, Widdel F, Reinhardt R (2005) The genome sequence of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Arch Microbiol 183:27–36PubMedPubMedCentralCrossRefGoogle Scholar
  116. Rabus R, Boll M, Golding B, Wilkes H (2016a) Anaerobic degradation of p-alkylated benzoates and toluenes. J Mol Microbiol Biotechnol 26:63–75PubMedPubMedCentralCrossRefGoogle Scholar
  117. Rabus R, Boll M, Heider J, Meckenstock RU, Buckel W, Einsle O, Ermler U, Golding BT, Gunsalus RP, Kroneck PM, Krüger M, Lueders T, Martins BM, Musat F, Richnow HH, Schink B, Seifert J, Szaleniec M, Treude T, Ullmann GM, Vogt C, von Bergen M, Wilkes H (2016b) Anaerobic microbial degradation of hydrocarbons: from enzymatic reactions to the environment. J Mol Microbiol Biotechnol 26:5–28PubMedPubMedCentralCrossRefGoogle Scholar
  118. Reichenbecher W, Brune A, Schink B (1994) Transhydroxylase of Pelobacter acidigallici: a molybdoenzyme catalyzing the conversion of pyrogallol to phloroglucinol. Biochim Biophys Acta 1204:217–224PubMedPubMedCentralCrossRefGoogle Scholar
  119. Reichenbecher W, Philipp B, Suter MJ, Schink B (2000) Hydroxyhydroquinone reductase, the initial enzyme involved in the degradation of hydroxyhydroquinone (1,2,4-trihydroxybenzene) by Desulfovibrio inopinatus. Arch Microbiol 173:206–212PubMedPubMedCentralCrossRefGoogle Scholar
  120. Rhee SK, Fuchs G (1999) Phenylacetyl-CoA: acceptor oxidoreductase, a membrane-bound molybdenum-iron-sulfur enzyme involved in anaerobic metabolism of phenylalanine in the denitrifying bacterium Thauera aromatica. Eur J Biochem 262:507–515PubMedPubMedCentralCrossRefGoogle Scholar
  121. Rotaru A, Probian C, Wilkes H, Harder J (2010) Highly enriched betaproteobacteria growing anaerobically with p-xylene and nitrate. FEMS Microbiol Ecol 71:460–468PubMedPubMedCentralCrossRefGoogle Scholar
  122. Rudolphi A, Tschech A, Fuchs G (1991) Anaerobic degradation of cresols by denitrifying bacteria. Arch Microbiol 155:238–248PubMedPubMedCentralCrossRefGoogle Scholar
  123. Schennen U, Braun K, Knackmuss HJ (1985) Anaerobic degradation of 2-fluorobenzoate by benzoate-degrading, denitrifying bacteria. J Bacteriol 161:321–325PubMedPubMedCentralCrossRefGoogle Scholar
  124. Schink B, Pfennig N (1982) Fermentation of trihydroxybenzenes by Pelobacter acidigallici gen. nov. sp. nov., a new strictly anaerobic non-sporeforming bacterium. Arch Microbiol 133:195–201CrossRefGoogle Scholar
  125. Schink B, Stams AJ (2013) Syntrophism among prokaryotes. In: Rosenberg E, Delong E, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes. Vol 2, Ecophysiology and biochemistry. Springer, Berlin, pp 471–493Google Scholar
  126. Schink B, Philipp B, Müller J (2000) Anaerobic degradation of phenolic compounds. Naturwissenschaften 87:12–23PubMedPubMedCentralCrossRefGoogle Scholar
  127. Schleinitz KM, Schmeling S, Jehmlich N, von Bergen M, Harms H, Kleinsteuber S, Vogt C, Fuchs G (2009) Phenol degradation in the strictly anaerobic iron-reducing bacterium Geobacter metallireducens GS-15. Appl Environ Microbiol 75:3912–3919PubMedPubMedCentralCrossRefGoogle Scholar
  128. Schmeling S, Fuchs G (2009) Anaerobic metabolism of phenol in proteobacteria and further studies of phenylphosphate carboxylase. Arch Microbiol 191:869–878PubMedPubMedCentralCrossRefGoogle Scholar
  129. Schmeling S, Narmandakh A, Schmitt O, Gad'on N, Schühle K, Fuchs G (2004) Phenylphosphate synthase: a new phosphotransferase catalyzing the first step in anaerobic phenol metabolism in Thauera aromatica. J Bacteriol 186:8044–8057PubMedPubMedCentralCrossRefGoogle Scholar
  130. Schmid G, René SB, Boll M (2015) Enzymes of the benzoyl-coenzyme A degradation pathway in the hyperthermophilic archaeon Ferroglobus placidus. Environ Microbiol 17:3289–3300PubMedPubMedCentralCrossRefGoogle Scholar
  131. Schühle K, Fuchs G (2004) Phenylphosphate carboxylase: a new C-C lyase involved in anaerobic phenol metabolism in Thauera aromatica. J Bacteriol 186:4556–4567PubMedPubMedCentralCrossRefGoogle Scholar
  132. Schühle K, Nies J, Heider J (2016) An indolacetate-CoA ligase and a phenylsuccinyl-CoA transferase involved in anaerobic metabolism of auxin. Environ Microbiol 18:3120. Scholar
  133. Selmer T, Andrei PI (2001) p-hydroxyphenylacetate decarboxylase from Clostridium difficile. A novel glycyl radical enzyme catalysing the formation of p-cresol. Eur J Biochem 268:1363–1372PubMedPubMedCentralCrossRefGoogle Scholar
  134. Selmer T, Pierik AJ, Heider J (2005) New glycyl radical enzymes catalysing key metabolic steps in anaerobic bacteria. Biol Chem 386:981–988PubMedPubMedCentralCrossRefGoogle Scholar
  135. Selvaraj B, Buckel W, Golding BT, Ullmann GM, Martins BM (2016) Structure and function of 4-Hydroxyphenylacetate decarboxylase and its cognate activating enzyme. J Mol Microbiol Biotechnol 26:76–91PubMedPubMedCentralCrossRefGoogle Scholar
  136. Song B, Palleroni NJ, Häggblom MM (2000) Isolation and characterization of diverse halobenzoate-degrading denitrifying bacteria from soils and sediments. Appl Environ Microbiol 66:3446–3453PubMedPubMedCentralCrossRefGoogle Scholar
  137. Song B, Palleroni NJ, Kerkhof LJ, Häggblom MM (2001) Characterization of halobenzoate-degrading, denitrifying Azoarcus and Thauera isolates and description of Thauera chlorobenzoica sp. nov. Int J Syst Evol Microbiol 51:589–602PubMedPubMedCentralCrossRefGoogle Scholar
  138. Stanier RY, Ornston LN (1973) The beta-ketoadipate pathway. Adv Microb Physiol 9:89–151PubMedPubMedCentralCrossRefGoogle Scholar
  139. Strijkstra A, Trautwein K, Jarling R, Wöhlbrand L, Dörries M, Reinhardt R, Drozdowska M, Golding BT, Wilkes H, Rabus R (2014) Anaerobic activation of p-cymene in denitrifying betaproteobacteria: methyl group hydroxylation versus addition to fumarate. Appl Environ Microbiol 80:7592–7603PubMedPubMedCentralCrossRefGoogle Scholar
  140. Szaleniec M, Heider J (2016) Modeling of the reaction mechanism of enzymatic radical C-C coupling by benzylsuccinate synthase. Int J Mol Sci 17:514PubMedPubMedCentralCrossRefGoogle Scholar
  141. Szaleniec M, Borowski T, Schühle K, Witko M, Heider J (2010) Ab initio modeling of ethylbenzene dehydrogenase reaction mechanism. J Am Chem Soc 132:6014–6024PubMedPubMedCentralCrossRefGoogle Scholar
  142. Szaleniec M, Dudzik A, Kozik B, Borowski T, Heider J, Witko M (2014) Mechanistic basis for the enantioselectivity of the anaerobic hydroxylation of alkylaromatic compounds by ethylbenzene dehydrogenase. J Inorg Biochem 139:9–20PubMedPubMedCentralCrossRefGoogle Scholar
  143. Thiele B, Rieder O, Golding BT, Müller M, Boll M (2008) Mechanism of enzymatic Birch reduction: stereochemical course and exchange reactions of benzoyl-CoA reductase. J Am Chem Soc 130:14050–14051PubMedPubMedCentralCrossRefGoogle Scholar
  144. Tiedt O, Mergelsberg M, Boll K, Müller M, Adrian L, Jehmlich N, von Bergen M, Boll M (2016) ATP-dependent C-F bond cleavage allows the complete degradation of 4-fluoroaromatics without oxygen. MBio 7:e00990–e00916PubMedPubMedCentralCrossRefGoogle Scholar
  145. Tor JM, Lovley DR (2001) Anaerobic degradation of aromatic compounds coupled to Fe(III) reduction by Ferroglobus placidus. Environ Microbiol 3:281–287PubMedPubMedCentralCrossRefGoogle Scholar
  146. Trautwein K, Wilkes H, Rabus R (2012) Proteogenomic evidence for β-oxidation of plant-derived 3-phenylpropanoids in “Aromatoleum aromaticum” EbN1. Proteomics 12:1402–1413PubMedPubMedCentralCrossRefGoogle Scholar
  147. Tschech A, Schink B (1985) Fermentative degradation of resorcinol and resorcylic acids. Arch Microbiol 143:52–59CrossRefGoogle Scholar
  148. Unciuleac M, Warkentin E, Page CC, Boll M, Ermler U (2004) Structure of a xanthine oxidase-related 4-hydroxybenzoyl-CoA reductase with an additional [4Fe-4S] cluster and an inverted electron flow. Structure 12:2249–2256PubMedPubMedCentralCrossRefGoogle Scholar
  149. Verfürth K, Pierik AJ, Leutwein C, Zorn S, Heider J (2004) Substrate specificities and electron paramagnetic resonance properties of benzylsuccinate synthases in anaerobic toluene and m-xylene metabolism. Arch Microbiol 181:155–162PubMedPubMedCentralCrossRefGoogle Scholar
  150. Weinert T, Huwiler SG, Kung JW, Weidenweber S, Hellwig P, Stärk H, Biskup T, Weber S, Cotelesage JJ, George GN, Ermler U, Boll M (2015) Structural basis of enzymatic benzene ring reduction. Nat Chem Biol 11:586–591PubMedPubMedCentralCrossRefGoogle Scholar
  151. White MD, Payne KA, Fisher K, Marshall SA, Parker D, Rattray NJ, Trivedi DK, Goodacre R, Rigby SE, Scrutton NS, Hay S, Leys D (2015) UbiX is a flavin prenyltransferase required for bacterial ubiquinone biosynthesis. Nature 522:502–506PubMedPubMedCentralCrossRefGoogle Scholar
  152. Wilkes H, Buckel W, Golding BT, Rabus R (2016) Metabolism of hydrocarbons in n-alkane-utilizing anaerobic bacteria. J Mol Microbiol Biotechnol 26:138–151PubMedPubMedCentralCrossRefGoogle Scholar
  153. Wischgoll S, Heintz D, Peters F, Erxleben A, Sarnighausen E, Reski R, van Dorsselaer A, Boll M (2005) Gene clusters involved in anaerobic benzoate degradation of Geobacter metallireducens. Mol Microbiol 58:1238–1252PubMedPubMedCentralCrossRefGoogle Scholar
  154. Wöhlbrand L, Wilkes H, Halder T, Rabus R (2008) Anaerobic degradation of p-ethylphenol by “Aromatoleum aromaticum” strain EbN1: pathway, regulation, and involved proteins. J Bacteriol 190:5699–5709PubMedPubMedCentralCrossRefGoogle Scholar
  155. 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 Tol2, a marine, aromatic compound-degrading, sulfate-reducing bacterium. Environ Microbiol 15:1334–1355PubMedPubMedCentralCrossRefGoogle Scholar
  156. Yu L, Blaser M, Andrei PI, Pierik AJ, Selmer T (2006) 4-Hydroxyphenylacetate decarboxylases: properties of a novel subclass of glycyl radical enzyme systems. Biochemistry 45:9584–9592PubMedPubMedCentralCrossRefGoogle Scholar
  157. Zargar K, Saville R, Phelan RM, Tringe SG, Petzold CJ, Keasling JD, Beller HR (2016) In vitro characterization of phenylacetate decarboxylase, a novel enzyme catalyzing toluene biosynthesis in an anaerobic microbial community. Sci Rep 6:31362PubMedPubMedCentralCrossRefGoogle Scholar
  158. Zhang T, Tremblay P, Chaurasia AK, Smith JA, Bain TS, Lovley DR (2013) Anaerobic benzene oxidation via phenol in Geobacter metallireducens. Appl Environ Microbiol 79:7800–7806PubMedPubMedCentralCrossRefGoogle Scholar
  159. Zhang T, Tremblay P, Chaurasia AK, Smith JA, Bain TS, Lovley DR (2014) Identification of genes specifically required for the anaerobic metabolism of benzene in Geobacter metallireducens. Front Microbiol 5:245PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Microbiology, Faculty of BiologyAlbert-Ludwigs-Universität FreiburgFreiburgGermany
  2. 2.Institute of Biology II, MicrobiologyAlbert-Ludwigs-Universität FreiburgFreiburgGermany
  3. 3.Faculty of Biology, Institute of Biologie IIUniversität FreiburgFreiburgGermany
  4. 4.Fachbereich BiologieUniversität MarburgMarburgGermany
  5. 5.Laboratory of Microbial Biochemistry, and LOEWE-Center for Synthetic MicrobiologyPhilipps-University of MarburgMarburgGermany

Personalised recommendations