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Functional Genomics of Denitrifying Bacteria Degrading Hydrocarbons

  • Living reference work entry
  • First Online:
Anaerobic Utilization of Hydrocarbons, Oils, and Lipids

Part of the book series: Handbook of Hydrocarbon and Lipid Microbiology ((HHLM))

  • 183 Accesses

Abstract

The betaproteobacterial Azoarcus/“Aromatoleum”/Thauera cluster harbors a large variety of denitrifiers capable of anaerobic degradation of aromatic compounds and hydrocarbons. The application of genomics and proteomics (proteogenomics) in conjunction with targeted metabolite analysis has proven instrumental to the discovery of a wide variety of novel reactions and pathways, the reconstruction of complex catabolic networks, and first steps into understanding how the latter are tuned to adapt to environmental changes. Over the past two to three decades, major advances have been achieved along three major organism-/approach-specific directions: (i) biochemistry of novel enzymatic reactions with Thauera aromatica K172 and “Aromatoleum aromaticum” EbN1, (ii) physiology and proteogenomics with “A. aromaticum” EbN1, and (iii) molecular mechanisms of transcriptional regulation with Azoarcus sp. strain CIB.

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References

  • Anders H-J, Kaetzke A, Kämpfer P, Ludwig W, Fuchs G (1995) Taxonomic position of aromatic-degrading denitrifying pseudomonad strains K 172 and KB 740 and their description as new members of the genera Thauera, as Thauera aromatica sp. nov., and Azoarcus, as Azoarcus evansii sp. nov., respectively, members of the beta subclass of the Proteobacteria. Int J Syst Bacteriol 45:327–333

    Article  CAS  PubMed  Google Scholar 

  • Barragán MJL, Blázquez B, Zamarro MT, Mancheño JM, García JL, Díaz E, Carmona M (2005) BzdR, a repressor that controls the anaerobic catabolism of benzoate in Azoarcus sp. CIB, is the first member of a new subfamily of transcriptional regulators. J Biol Chem 280:10683–10694

    Article  CAS  PubMed  Google Scholar 

  • Bellanger X, Payot S, Leblond-Bourget N, Guédon G (2014) Conjugative and mobilizable genomic islands in bacteria: evolution and diversity. FEMS Microbiol Rev 38:720–760

    Article  CAS  PubMed  Google Scholar 

  • Blázquez B, Carmona M, García JL, Díaz E (2008) Identification and analysis of a glutaryl-CoA dehydrogenase-encoding gene and its cognate transcriptional regulator from Azoarcus sp. CIB. Environ Microbiol 10:474–482

    Article  CAS  PubMed  Google Scholar 

  • Blázquez B, Carmona M, Díaz E (2018) Transcriptional regulation of the peripheral pathway for the anaerobic catabolism of toluene and m-xylene in Azoarcus sp. CIB. Front Microbiol 9:506

    Article  PubMed  PubMed Central  Google Scholar 

  • Bolden AL, Kwiatkowski CF, Colborn T (2015) New look at BTEX: are ambient levels a problem? Environ Sci Technol 49:5261–5276

    Article  CAS  PubMed  Google Scholar 

  • Boll M, Fuchs G, Heider J (2002) Anaerobic degradation of aromatic compounds and hydrocarbons. Curr Opin Chem Biol 6:604–611

    Article  CAS  PubMed  Google Scholar 

  • Breuer M, Rabus R, Heider J (2008) Method for producing optically active alcohols using an Azoarcus sp. EbN1 dehydrogenase. WO 2008/155302 A1

    Google Scholar 

  • Bugg TDH, Ahmad M, Hardiman EM, Rahmanpour R (2011) Pathways for degradation of lignin by bacteria and fungi. Nat Prod Rep 28:1883

    Article  CAS  PubMed  Google Scholar 

  • Büsing I, Höffken HW, Breuer M, Wöhlbrand L, Hauer B, Rabus R (2015a) Molecular genetic and crystal structural analysis of 1-(4-hydroxyphenyl)-ethanol dehydrogenase from ‘Aromatoleum aromaticum’ EbN1. J Mol Microbiol Biotechnol 25:327–339

    Article  CAS  PubMed  Google Scholar 

  • Büsing I, Kant M, Dörries M, Wöhlbrand L, Rabus R (2015b) The predicted σ54-dependent regulator EtpR is essential for expression of genes for anaerobic p-ethylphenol and p-hydroxy-acetophenone degradation in “Aromatoleum aromaticum” EbN1. BMC Microbiol 15:251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carmona M, Zamarro MT, Blázquez B, Durante-Rodríguez G, Juárez JF, Valderrama A, Barragán MJL, García JL, Díaz E (2009) Anaerobic catabolism of aromatic compounds: a genetic and genomic view. Microbiol Mol Biol Rev 73:71–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conrad R (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol Rev 60:609–640

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 189:3824–3833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 196:483–492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Decker K, Jungermann K, Thauer RK (1970) Energy production in anaerobic organisms. Angew Chem Int Ed 9:138–158

    Article  CAS  Google Scholar 

  • Devol AH (2015) Denitrification, anammox, and N2 production in marine sediments. Annu Rev Mar Sci 7:403–423

    Article  Google Scholar 

  • 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 190:1620–1630

    Article  CAS  PubMed  Google Scholar 

  • Dudzik A, Snoch W, Borowiecki P, Opalinska-Piskorz J, Witko M, Heider J, Szaleniec M (2015) Asymmetric reduction of ketones and β-keto esters by (S)-1-phenylethanol dehydrogenase from denitrifying bacterium Aromatoleum aromaticum. Appl Microbiol Biotechnol 99:5055–5069

    Article  CAS  PubMed  Google Scholar 

  • Duldhardt I, Gaebel J, Chrzanowski L, Nijenhuis I, Härtig C, Schauer F, Heipieper HJ (2010) Adaptation of anaerobically grown Thauera aromatica, Geobacter sulfurreducens and Desulfococcus multivorans to organic solvents on the level of membrane fatty acid composition. Microb Biotechnol 3:201–209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durante-Rodríguez G, Zamarro MT, García JL, Díaz E, Carmona M (2006) Oxygen-dependent regulation of the central pathway for the anaerobic catabolism of aromatic compounds in Azoarcus sp. strain CIB. J Bacteriol 188:2343–2354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durante-Rodríguez G, Zamarro MT, García JL, Díaz E, Carmona M (2008) New insights into the BzdR-mediated transcriptional regulation of the anaerobic catabolism of benzoate in Azoarcus sp. CIB. Microbiology 154:306–316

    Article  CAS  PubMed  Google Scholar 

  • Durante-Rodríguez G, Valderrama JA, Mancheño JM, Rivas G, Alfonso C, Arias-Palomo E, Llorca O, García JL, Díaz E, Carmona M (2010) Biochemical characterization of the transcriptional regulator BzdR from Azoarcus sp. CIB. J Biol Chem 285:35694–35705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebenau-Jehle C, Thomas M, Scharf G, Kockelkorn D, Knapp B, Schühle K, Heider J, Fuchs G (2012) Anaerobic metabolism of indoleacetate. J Bacteriol 194:2894–2903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebenau-Jehle C, Mergelsberg M, Fischer S, Brüls T, Jehmlich N, von Bergen M, Boll M (2017) An unusual strategy for anoxic biodegradation of phthalate. ISME J 11:224–236

    Article  CAS  PubMed  Google Scholar 

  • Egli T (2010) How to live at very low substrate concentration. Water Res 44:4826–4837

    Article  CAS  PubMed  Google Scholar 

  • Ferenci T (2008) Bacterial physiology, regulation and mutational adaptation in a chemostat environment. Adv Microb Physiol 53:169–229

    Article  CAS  PubMed  Google Scholar 

  • Fernández H, Prandoni N, Fernández-Pascual M, Fajardo S, Morcillo C, Díaz E, Carmona M (2014) Azoarcus sp. CIB, an anaerobic biodegrader of aromatic compounds shows an endophytic lifestyle. PLoS One 9:e110771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fowler D, Coyle M, Skiba U, Sutton MA, Cape JN, Reis S, Sheppard LJ, Jenkins A, Grizzetti B, Galloway JN, Vitousek P, Leach A, Bouwman AF, Butterbach-Bahl K, Dentener F, Stevenson D, Amann M, Voss M (2013) The global nitrogen cycle in the twenty-first century. Philos Trans R Soc B 368:20130164

    Article  CAS  Google Scholar 

  • Fu Z, Wang M, Paschke R, Rao KS, Frerman FE, Kim J-JP (2004) Crystal structures of human glutaryl-CoA dehydrogenase with and without an alternate substrate: structural bases of dehydrogenation and decarboxylation reactions. Biochemistry 43:9674–9684

    Article  CAS  PubMed  Google Scholar 

  • Fuchs G, Boll M, Heider J (2011) Microbial degradation of aromatic compounds – from one strategy to four. Nat Rev Microbiol 9:803–816

    Article  CAS  PubMed  Google Scholar 

  • Gallus C, Schink B (1998) Anaerobic degradation of α-resorcylate by Thauera aromatica strain AR-1 proceeds via oxidation and decarboxylation to hydroxyhydroquinone. Arch Microbiol 169:333–338

    Article  CAS  PubMed  Google Scholar 

  • Gibson DT, Parales RE (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11:236–243

    Article  CAS  PubMed  Google Scholar 

  • Harms G, Rabus R, Widdel F (1999) Anaerobic oxidation of the aromatic plant hydrocarbon p-cymene by newly isolated denitrifying bacteria. Arch Microbiol 172:303–312

    Article  CAS  PubMed  Google Scholar 

  • Heider J, Fuchs G (1997) Anaerobic metabolism of aromatic compounds. Eur J Biochem 243:577–596

    Article  CAS  PubMed  Google Scholar 

  • Heider J, Fuchs G (2005) Genus Thauera. In: Garrity G (ed) Bergey’s manual of systematic bacteriology, vol 2, part C, 2nd edn. Springer, Heidelberg, pp 907–913

    Chapter  Google Scholar 

  • Heider J, Szaleniec M, Sünwoldt K, Boll M (2016) Ethylbenzene dehydrogenase and related molybdenum enzymes involved in oxygen-independent alkyl chain hydroxylation. J Mol Microbiol Biotechnol 26:45–62

    Article  CAS  PubMed  Google Scholar 

  • Heipieper HJ, Neumann G, Cornelissen S, Meinhardt F (2007) Solvent-tolerant bacteria for biotransformations in two-phase fermentation systems. Appl Microbiol Biotechnol 74:961–973

    Article  CAS  PubMed  Google Scholar 

  • Hess A, Zarda B, Hahn D, Häner A, Stax D, Höhener P, Zeyer P (1997) In situ analysis of denitrifying toluene- and m-xylene-degrading bacteria in a diesel fuel-contaminated laboratory aquifer column. Appl Environ Microbiol 63:2136–2141

    CAS  PubMed  PubMed Central  Google Scholar 

  • Höffken HW, Duong M, Friedrich T, Breuer M, Hauer B, Reinhardt R, Rabus R, Heider J (2006) Crystal structure and enzyme kinetics of the (S)-specific 1-phenylethanol dehydrogenase of the denitrifying bacterium strain EbN1. Biochemistry 45:82–93

    Article  CAS  PubMed  Google Scholar 

  • Jiang K, Sanseverino J, Chauhan A, Lucas S, Copeland A, Lapidus A, Del Rio TG, Dalin E, Tice H, Bruce D, Goodwin L, Pitluck S, Sims D, Brettin T, Detter JC, Han C, Chang YJ, Larimer F, Land M, Hauser L, Kyrpides NC, Mikhailova N, Moser S, Jegier P, Close D, DeBruyn JM, Wang Y, Layton AC, Allen MS, Sayler GS (2012) Complete genome sequence of Thauera aminoaromatica strain MZ1T. Stand Genomic Sci 6:325–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jobst B, Schühle K, Linne U, Heider J (2010) ATP-dependent carboxylation of acetophenone by a novel type of carboxylase. J Bacteriol 192:1387–1394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 15:148–166

    Article  CAS  PubMed  Google Scholar 

  • Juárez JF, Liu H, Zamarro MT, McMahon S, Liu H, Naismith JH, Eberlein C, Boll M, Carmona M, Díaz E (2015) Unraveling the specific regulation of the central pathway for anaerobic degradation of 3-methylbenzoate. J Biol Chem 290:12165–12183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Junghare M, Patil Y, Schink B (2015) Draft genome sequence of a nitrate-reducing, o-phthalate degrading bacterium, Azoarcus sp. strain PA01T. Stand Genomic Sci 10:90

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 18:3175–3188

    Article  CAS  PubMed  Google Scholar 

  • Kloer DP, Hagel C, Heider J, Schulz GE (2006) Crystal structure of ethylbenzene dehydrogenase from Aromatoleum aromaticum. Structure 14:1377–1388

    Article  CAS  PubMed  Google Scholar 

  • Kniemeyer O, Heider J (2001a) Ethylbenzene dehydrogenase, a novel hydrocarbon-oxidizing molybdenum/iron-sulfur/heme enzyme. J Biol Chem 276:21381–21386

    Article  CAS  PubMed  Google Scholar 

  • Kniemeyer O, Heider J (2001b) (S)-1-Phenylethanol dehydrogenase of Azoarcus sp. strain EbN1, an enzyme of anaerobic ethylbenzene catabolism. Arch Microbiol 176:129–135

    Article  CAS  PubMed  Google Scholar 

  • Koch J, Fuchs G (1992) Enzymatic reduction of benzoyl-CoA to alicyclic compounds, a key reaction in anaerobic aromatic metabolism. Eur J Biochem 205:195–202

    Article  CAS  PubMed  Google Scholar 

  • Krause A, Ramakumar A, Bartels D, Battistoni F, Bekel T, Boch J, Böhm M, Friedrich F, Hurek T, Krause L, Linke B, McHardy AC, Sarkar A, Schneiker S, Syed AA, Thauer R, Vorhölter F-J, Weidner S, Pühler A, Reinhold-Hurek B, Kaiser O, Goesmann A (2006) Complete genome of the mutualistic, N2-fixing grass endophyte Azoarcus sp. strain BH72. Nat Biotechnol 24:1385–1391

    Article  CAS  PubMed  Google Scholar 

  • Kube M, Heider J, Amann J, Hufnagel P, Kühner S, Beck A, Reinhardt R, Rabus R (2004) Genes involved in the anaerobic degradation of toluene in a denitrifying bacterium, strain EbN1. Arch Microbiol 181:182–194

    Article  CAS  PubMed  Google Scholar 

  • Kühner S, Wöhlbrand L, Fritz I, Wruck W, Hultschig C, Hufnagel P, Kube M, Reinhardt R, Rabus R (2005) Substrate-dependent regulation of anaerobic degradation pathways for toluene and ethylbenzene in a denitrifying bacterium, strain EbN1. J Bacteriol 187:1493–1503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuntze K, Kiefer P, Baumann S, Seifert J, von Bergen M, Vorholt JA, Boll M (2011) Enzymes involved in the anaerobic degradation of meta-substituted halobenzoates. Mol Microbiol 82:758–769

    Article  CAS  PubMed  Google Scholar 

  • Lahme S, Eberlein C, Jarling R, Kube M, Boll M, Wilkes H, Reinhardt R, Rabus R (2012a) Anaerobic degradation of 4-methylbenzoate via a specific 4-methylbenzoyl-CoA pathway. Environ Microbiol 14:1118–1132

    Article  CAS  PubMed  Google Scholar 

  • Lahme S, Harder J, Rabus R (2012b) Anaerobic degradation of 4-methylbenzoate by a newly isolated denitrifying bacterium, strain pMbN1. Appl Environ Microbiol 78:1606–1610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lahme S, Trautwein K, Strijkstra A, Dörries M, Wöhlbrand L, Rabus R (2014) Benzoate mediates the simultaneous repression of anaerobic 4-methylbenzoate and succinate utilization in Magnetospirillum sp. strain pMbN1. BMC Microbiol 14:269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • López Barragán MJ, Carmona M, Zamarro MT, Thiele B, Boll M, Fuchs G, García JL, Díaz E (2004) The bzd gene cluster, coding for anaerobic benzoate catabolism, in Azoarcus sp. strain CIB. J Bacteriol 186:5762–5774

    Article  CAS  PubMed  Google Scholar 

  • Martín-Moldes Z, Zamarro MT, del Cerro C, Valencia A, Gómez MJ, Arcas A, Udaondo Z, García JL, Nogales J, Carmona M, Díaz E (2015) Whole-genome analysis of Azoarcus sp. strain CIB provides genetic insights to its different lifestyles and predicts novel metabolic features. Syst Appl Microbiol 38:462–471

    Article  CAS  PubMed  Google Scholar 

  • Martín-Moldes Z, Blázquez B, Baraquet C, Harwood CS, Zamarro MT, Díaz E (2016) Degradation of cyclic diguanosine monophosphate by a hybrid two-component protein protects Azoarcus sp. strain CIB from toluene toxicity. PNAS 113:13174–13179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mergelsberg M, Willistein M, Meyer H, Stärk H-J, Bechtel DF, Pierik AJ, Boll M (2017) Phthaloyl-coenzyme A decarboxylase from Thauera chlorobenzoica: the prenylated flavin-, K+- and Fe2+-dependent key enzyme of anaerobic phthalate degradation. Environ Microbiol 19:3734–3744

    Article  CAS  PubMed  Google Scholar 

  • Molina-Fuentes A, Pacheco D, Marín P, Philipp B, Schink B, Marqués S (2015) Identification of the gene cluster for the anaerobic degradation of 3,5-dihydroxybenzoate (α-resorcylate) in Thauera aromatica strain AR-1. Appl Environ Microbiol 81:7201–7214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morales G, Linares JF, Beloso A, Albar JP, Martínez JL, Rojo F (2004) The Pseudomonas putida Crc global regulator controls the expression of genes from several chromosomal catabolic pathways for aromatic compounds. J Bacteriol 186:1337–1344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 197:1051–1062

    Article  CAS  PubMed  Google Scholar 

  • 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 6:1561

    Article  PubMed  PubMed Central  Google Scholar 

  • Nazina TN, Shestakova NM, Semenova EM, Korshunova AV, Kostrukova NK, Tourova TP, Min L, Feng Q, Poltaraus AB (2017) Diversity of metabolically active Bacteria in water-flooded high-temperature heavy oil reservoir. Front Microbiol 8:707

    Article  PubMed  PubMed Central  Google Scholar 

  • Novick A, Szilard L (1950) Description of the chemostat. Science 112:715–716

    Article  CAS  PubMed  Google Scholar 

  • Overton EB, Wade TL, Radović JR, Meyer BM, Miles MS, Larter SR (2016) Chemical composition of Macondo and other crude oils and compositional alterations during oil spills. Oceanography 29:50–63

    Article  Google Scholar 

  • Pacheco-Sánchez D, Molina-Fuentes Á, Marín P, Medina-Bellver J-I, González-López Ó, Marqués S (2017) The Azoarcus anaerobius 1,3-dihydroxybenzene (resorcinol) anaerobic degradation pathway is controlled by the coordinated activity of two enhancer-binding proteins. Appl Environ Microbiol 83:e03042–e03016

    Article  PubMed  PubMed Central  Google Scholar 

  • Pajares S, Bohannan BJM (2016) Ecology of nitrogen fixing, nitrifying and denitrifying microorganisms in tropical forest soils. Front Microbiol 7:1045

    PubMed  PubMed Central  Google Scholar 

  • Rabus R (2005) Functional genomics of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Arch Microbiol 68:580–587

    CAS  Google Scholar 

  • Rabus R, Widdel F (1995) Anaerobic degradation of ethylbenzene and other aromatic hydrocarbons by new denitrifying bacteria. Arch Microbiol 163:96–103

    Article  CAS  PubMed  Google Scholar 

  • Rabus R, Widdel F (1996) Utilization of alkylbenzenes during anaerobic growth of pure cultures of denitrifying bacteria on crude oil. Appl Environ Microbiol 62:1238–1241

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rabus R, Kube M, Beck A, Widdel F, Reinhardt R (2002) Genes involved in the anaerobic degradation of ethylbenzene in a denitrifying bacterium, strain EbN1. Arch Microbiol 178:506–516

    Article  CAS  PubMed  Google Scholar 

  • 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 183:27–36

    Article  CAS  PubMed  Google Scholar 

  • Rabus R, Trautwein K, Wöhlbrand L (2014) Towards habitat-oriented systems biology of “Aromatoleum aromaticum” EbN1. Chemical sensing, catabolic network modulation and growth control in anaerobic aromatic compound degradation. Appl Microbiol Biotechnol 98:3371–3388

    Article  CAS  PubMed  Google Scholar 

  • Rabus R, Boll M, Heider J, Meckenstock RU, Buckel W, Einsle O, Ermler U, Golding BT, Gunsalus RP, Kroneck PMH, 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 (2016a) Anaerobic microbial degradation of hydrocarbons: from enzymatic reactions to the environment. J Mol Microbiol Biotechnol 26:5–28

    Article  CAS  PubMed  Google Scholar 

  • Rabus R, Boll M, Golding B, Wilkes H (2016b) Anaerobic degradation of p-alkylated benzoates and toluenes. J Mol Microbiol Biotechnol 26:63–75

    Article  CAS  PubMed  Google Scholar 

  • Ramos JL, Duque E, Gallegos M-T, Godoy P, Ramos-González MI, Rojas A, Terán W, Segura A (2002) Mechanisms of solvent tolerance in Gram-negative bacteria. Annu Rev Microbiol 56:743–768

    Article  CAS  PubMed  Google Scholar 

  • Reeve CD, Carver MA, Hopper DJ (1989) The purification and characterization of 4-ethylphenol methylenehydroxylase, a flavocytochrome from Pseudomonas putida JD1. Biochem J 263:431–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Römling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77:1–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaechter M, Maaløe O, Kjeldgaard NO (1958) Dependency of medium and temperature of cell size and chemical composition during balanced growth of Salmonella typhimurium. J Gen Microbiol 19:592–606

    Article  CAS  PubMed  Google Scholar 

  • Schmitt G, Arndt F, Kahnt J, Heider J (2017) Adaptations to a loss-of-function mutation in the betaproteobacterium Aromatoleum aromaticum: recruitment of alternative enzymes for anaerobic phenylalanine degradation. J Bacteriol 199:e00383–e00317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schühle K, Heider J (2012) Acetone and butanone metabolism of the denitrifying bacterium “Aromatoleum aromaticum” demonstrates novel biochemical properties of an ATP-dependent aliphatic ketone carboxylase. J Bacteriol 194:131–141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schühle K, Nies J, Heider J (2016) An indoleacetate-CoA ligase and a phenylsuccinyl-CoA transferase involved in anaerobic metabolism of auxin. Environ Microbiol 18:3120–3132

    Article  CAS  PubMed  Google Scholar 

  • Shapleigh JP (2013) Denitrifying prokaroytes. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes – prokaryotic physiology and biochemistry, vol 10. Springer, Heidelberg, pp 405–425

    Google Scholar 

  • Sikkema J, DE Bont JAM, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 51:589–602

    Article  CAS  PubMed  Google Scholar 

  • Springer N, Ludwig W, Philipp B, Schink B (1998) Azoarcus anaerobius sp. nov., a resorcinol-degrading, strictly anaerobic, denitrifying bacterium. Int J Syst Bacteriol 48:953–956

    Article  PubMed  Google Scholar 

  • 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 80:7592–7603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiedje JM, Sexstone AJ, Myrold DD, Robinson JA (1982) Denitrification: ecological niches, competition and survival. Antonie Van Leeuwenhoek 48:569–583

    Article  CAS  PubMed  Google Scholar 

  • 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–e00916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiedt O, Mergelsberg M, Eisenreich W, Boll M (2017) Promiscuous defluorinating enoyl-CoA hydratases/hydrolases allow for complete anaerobic degradation of 2-fluorobenzoate. Front Microbiol 8:2579

    Article  PubMed  PubMed Central  Google Scholar 

  • Tiedt O, Fuchs J, Eisenreich W, Boll M (2018) A catalytically versatile benzoyl-CoA reductase, key enzyme in the degradation of methyl- and halobenzoates in denitrifying bacteria. J Biol Chem. https://doi.org/10.1074/jbc.RA118.003329

  • Tijhuis L, van Loosdrecht MCM, Heijnen JJ (1993) A thermodynamically based correlation for maintenance Gibbs energy requirements in aerobic and anaerobic chemotrophic growth. Biotechnol Bioeng 42:509–519

    Article  CAS  PubMed  Google Scholar 

  • Trautwein K, Kühner S, Wöhlbrand L, Halder T, Kuchta K, Steinbüchel A, Rabus R (2008) Solvent stress response of the denitrifying bacterium “Aromatoleum aromaticum” strain EbN1. Appl Environ Microbiol 74:2267–2274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trautwein K, Grundmann O, Wöhlbrand L, Eberlein C, Boll M, Rabus R (2012a) Benzoate mediates repression of C4-dicarboxylate utilization in “Aromatoleum aromaticum” EbN1. J Bacteriol 194:518–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trautwein K, Lahme S, Wöhlbrand L, Feenders C, Mangelsdorf K, Harder J, Steinbüchel A, Blasius B, Reinhardt R, Rabus R (2012b) Physiological and proteomic adaptation of “Aromatoleum aromaticum” EbN1 to low growth rates in benzoate-limited, anoxic chemostats. J Bacteriol 194:2165–2180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trautwein K, Wilkes H, Rabus R (2012c) Proteogenomic evidence for β-oxidation of plant-derived 3-phenylpropanoids in “Aromatoleum aromaticum” EbN1. Proteomics 12:1402–1413

    Article  CAS  PubMed  Google Scholar 

  • Umezawa T (2010) The cinnamate/monolignol pathway. Phytochem Rev 9:1–17

    Article  CAS  Google Scholar 

  • Valderrama JA, Durante-Rodríguez G, Blázquez B, Garciá JL, Carmona M, Díaz E (2012) Bacterial degradation of benzoate. Cross-regulation between aerobic and anaerobic pathways. J Biol Chem 287:10494–10508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valderrama JA, Shingler V, Carmona M, Díaz E (2014) AccR is a master regulator involved in carbon catabolite repression of the anaerobic catabolism of aromatic compounds in Azoarcus sp. CIB. J Biol Chem 289:1892–1904

    Article  CAS  PubMed  Google Scholar 

  • Weidenweber S, Schühle K, Demmer U, Warkentin E, Ermler U, Heider J (2017) Structure of the acetophenone carboxylase core complex: prototype of a new class of ATP-dependent carboxylases/hydrolases. Sci Rep 7:39674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Widdel F, Rabus R (2001) Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr Opin Biotechnol 12:259–276

    Article  CAS  PubMed  Google Scholar 

  • Widdel F, Knittel K, Galushko A (2010) Anaerobic hydrocarbon-degrading microorganisms: an overview. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology, vol 29. Springer, Heidelberg, pp 1997–2021

    Chapter  Google Scholar 

  • Wischgoll S, Taubert M, Peters F, Jehmlich N, von Bergen M, Boll M (2009) Decarboxylating and nondecarboxylating glutaryl-coenzyme A dehydrogenases in the aromatic metabolism of obligately anaerobic bacteria. J Bacteriol 191:4401–4409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wöhlbrand L, Rabus R (2009) Development of a genetic system for the denitrifying bacterium ‘Aromatoleum aromaticum’ strain EbN1. J Mol Microbiol Biotechnol 17:41–52

    Article  CAS  PubMed  Google Scholar 

  • Wöhlbrand L, Kallerhoff B, Lange D, Hufnagel P, Thiermann J, Reinhardt R, Rabus R (2007) Functional proteomic view of metabolic regulation in “Aromatoleum aromaticum” strain EbN1. Proteomics 7:2222–2239

    Article  CAS  PubMed  Google Scholar 

  • 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 190:5699–5709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin Y, Wang Y, Tang W, Song L (2017) Thauera phenolivorans sp. nov., a phenol degrading bacterium isolated from activated sludge. Antonie Van Leeuwenhoek. https://doi.org/10.1007/s10482-017-0918-3

  • Zamarro MT, Martín-Moldes Z, Díaz E (2016) The ICEXTD of Azoarcus sp. CIB, an integrative and conjugative element with aerobic and anaerobic catabolic properties. Environ Microbiol 18:5018–5031

    Article  CAS  PubMed  Google Scholar 

  • Zink K-G, Rabus R (2010) Stress-induced changes in phospholipids in betaproteobacterium Aromatoleum aromaticum strain EbN1 due to alkylbenzene growth substrates. J Mol Microbiol Biotechnol 18:92–101

    Article  CAS  PubMed  Google Scholar 

  • Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:513–616

    Google Scholar 

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Authors and Affiliations

  1. General & Molecular Microbiology, Institute for Chemistry and Biology of the Marine Environment (ICBM), University Oldenburg, Oldenburg, Germany

    R. Rabus

  2. Organic Geochemistry, Institute for Chemistry and Biology of the Marine Environment (ICBM), University Oldenburg, Oldenburg, Germany

    H. Wilkes

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  1. R. Rabus
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  2. H. Wilkes
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Correspondence to R. Rabus .

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  1. Institut für Biologie II, Universität Freiburg Institut für Biologie II, Freiburg, Baden-Württemberg, Germany

    Matthias Boll

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Rabus, R., Wilkes, H. (2019). Functional Genomics of Denitrifying Bacteria Degrading Hydrocarbons. In: Boll, M. (eds) Anaerobic Utilization of Hydrocarbons, Oils, and Lipids. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-33598-8_11-1

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