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The biodegradation of aromatic hydrocarbons by bacteria

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Abstract

Aromatic compounds of both natural and man-made sources abound in the environment. The degradation of such chemicals is mainly accomplished by microorganisms. This review provides key background information but centres on recent developments in the bacterial degradation of selected man-made aromatic compounds. An aromatic compound can only be considered to be biodegraded if the ring undergoes cleavage, and this is taken as the major criteria for inclusion in this review (although the exact nature of the enzymic ring-cleavage has not been confirmed in all cases discussed).

The biodegradation of benzene, certain arenes, biphenyl and selected fused aromatic hydrocarbons, by single bacterial isolates, are dealt with in detail.

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References

  • Amund, OO & Higgins, IJ (1985) The degradation of 1-phenylalkanes by an oil degrading strain of Acinetobacter lwoffi. Antonie van Leeuwenhoek 51: 45–56

    Google Scholar 

  • Arvin, E, Jensen, BK & Gundersen, AT (1989) Substrate interactions during the areobic degradation of benzene. Appl. Environ. Microbiol. 55: 3221–3225

    Google Scholar 

  • Axell, BC & Geary, PJ (1975) The metabolism of benzene by bacteria. Biochem. J. 136: 927–934

    Google Scholar 

  • Baggi, G, Catelani, D, Galli, E & Treccani, V (1972) The microbial degradation of phenylalkanes. Biochem. J. 126: 1091–1097

    Google Scholar 

  • Baggi, G, Boga, MM, Catelani, D, Galli, E & Trecccani, V (1983) Styrene catabolism by a strain of Pseudomonas fluorescens. Syst. Appl Microbiol. 4: 141–147

    Google Scholar 

  • Baggi, G, Barbieri, P, Galli, E & Tollari, S (1987) Isolation of a Pseudomonas stutzeri strain that degrades o-xxylene. Appl. Environ. Microbiol. 53: 2129–2132

    Google Scholar 

  • Ballard DGH, Courtis A, Shirley IM & Taylor SC (1983) A biotech route to polyphenylene: J. Chem. Soc., Chem. Comm. pp 954–955

  • Bateman, JN, Speers, B, Feduik, L & Hartline, RA (1986) Naphthalene association and uptake in Pseudomonas putida. J. Bacteriol. 166: 155–161

    Google Scholar 

  • Bauer, JE & Capone, DG (1988) Effects of co-occurring aromatic hydrocarbons on the degradation of individual polycyclic aromatic hydrocarbons in marine sediment slurries. Appl. Environ. Microbiol. 54: 1649–1655

    Google Scholar 

  • Bayly, RC & Barbour, MG (1984) The degradation of aromatic compounds by the meta and gentisate pathways. In: Gibson, DT (Ed) Microbial Degradation of Organic Compounds (pp 253–294). Marcel Dekker, New York

    Google Scholar 

  • Berry, DF, Francis, AJ & Bollag, J-M (1987) Microbial metabolism of homocyclic aromatic compounds under anaerobic conditions. Microbiol. Revs. 51: 43–49

    Google Scholar 

  • Bestetti, G & Galli, E (1984) Plasmid-coded degradation of ethylbenzene and 1-phenylethanol in Pseudomonas fluoresens. FEMS Microbiol. Letts. 21: 165–168

    Google Scholar 

  • Bestetti, G, Galli, E, Benigini, C Orsini, F & Pelizzoni, F (1989) Biotransformation of styrenes by a Pseudomonas putida. Appl. Microbiol. Biotechnol. 30: 252–256

    Google Scholar 

  • Burlage, RS, Hooper, SW & Sayler, GS (1989) The TOL (pWWO) catabolic plasmid. Appl. Environ. Microbiol 55: 1323–1328

    Google Scholar 

  • Catelani, D, Sorlini, C & Treccani, V (1971) The metabolism of biphenyl by Pseudomonas putida. Experientia 27: 1173–1174

    Google Scholar 

  • Catelani, D, Colombi, A, Sorlini, C & Treccani, V (1973) Metabolism of biphenyl. 2-Hydroxy-6-oxo-6-phenylhexa-2,4-dienoate: the meta cleavage product from 2,3-dihydroxybiphenyl by Pseudomonas putida. Biochem. J. 134: 1063–1066

    Google Scholar 

  • Catelani, D & Colombi, A (1974) Metabolism of biphenyl. Structure and physical properties of 2-hydroxy-6-oxo-6-phenylhexa-2,4-dienoate, the meta cleavage product from 2,3-dihydroxybiphenyl by Pseudomonas putida. Biochem. J. 143: 431–434

    Google Scholar 

  • Catelani, D, Colombi, A, Sorlini, C & Treccani, V (1977) Metabolism of quaternary carbon compounds: 2,2-dimethylheptane and tertbutylbenzene. Appl. Environ. Microbiol. 34: 351–354

    Google Scholar 

  • Cerniglia, CE (1984) Microbial metabolism of polycyclic aromatic compounds. Adv. Appl. Microbiol. 30: 31–71

    Google Scholar 

  • Cerniglia, CE & Heitkamp, MA (1989) Microbial degradation of polycyclic compounds (PAH) in the aquatic environment In: Varanasi, V (Ed) Metabolism of PAHS in the Aquatic Environment (pp 41–68). CRC Press Inc. Boca Raton; Florida

    Google Scholar 

  • Cripps, RE, Trudgill, PW & Wheatley, JG (1978) The metabolism of 1-phenylethanol and actophenone by Nocardia T5 and an Arthrobacter species. Eur. J. Biochem. 86: 175–186

    Google Scholar 

  • Cripps, RE & Watkinson, RJ (1978) Polycyclic aromatic hydrocarbons: Metabolism and environment l aspects. In: Watkinson, RJ (Ed) Developments in the Biodegradation of Hydrocarbons (pp 113–134). Applied Science Publishers, London

    Google Scholar 

  • Dagley, S (1981) New perspectives in aromatic catabolism. In: Leisinger, T, Cook, AM, Hütter, R & Nüesch, J (Eds) Microbial Degradation of Xenobiotics and Recalcitrant Compounds (pp 181–186). Academic Press, New York

    Google Scholar 

  • Dagley, S (1986) Biochemistry of aromatic hydrocarbon degradation in Pseudomonads. In: Sokatch, JR (Ed) The Bacteria (Vol 10) (pp 527–555). Academic Press, New York

    Google Scholar 

  • Davey, JF & Gibson, DT (1974) Bacterial metabolism of p- and m-xylene: Oxidation of the methyl substituent. J. Bacteriol. 119: 923–929

    Google Scholar 

  • Davis, RS, Hossler, FE & Stone, RW (1968) Metabolism of p- and m-xylene by species of Pseudomonas. Can. J. Microbiol 27: 1005–1009

    Google Scholar 

  • DeFrank, JJ & Ribbons, DW (1976) The p-cymene pathway in Pseudomonas putida PL: Isolation of a dihydrodiol accumulated by a mutant. Biochem. Biophys. Res. Commun. 70: 1129–1135

    Google Scholar 

  • DeFrank, JJ & Ribbons, DW (1977a) p-Cymene pathway in Pseudomonas putida: Initial reactions. J. Bacteriol. 129: 1356–1364

    Google Scholar 

  • DeFrank, JJ & Ribbons, DW (1977b) p-Cymene pathway in Pseudomonas putida: ring cleavage of 2,3-dihydroxy-p-cumate and subsequent reactions. J. Bacteriol. 129: 1365–1375

    Google Scholar 

  • Duggleby, CJ & Williams, PA (1986) Purification and some properties of the 2-hydroxy-6-oxohepta-2,4-dienoate hydrolase (2-hydroxymuconic semialdehyde hydrolase) encoded by the TOL plasmid pWWO from Pseudomonas putida mt 2. J Gen Microbiol 132: 717–726

    Google Scholar 

  • Dunn, NW & Gunsalus, IC (1973) Transmissible plasmid coding for the early enzymes of naphthalene oxidation in Pseudomonas putida. J. Bacteriol. 114: 974–979

    Google Scholar 

  • Durham, DR & Stewart, DB (1987) Recruitment of naphthalene dissimilatory enzymes for the oxidation of 1,4-dichloronaphthalene to 3,6-dichlorosalicylate, a precursor of the herbicide Dicamba. J. Bacteriol. 169: 2889–2892

    Google Scholar 

  • Dzhusupova, DB, Baskunov, BP, Golovleva, LA, Alieva, RM & Ilyaletdinov, AN (1985) Peculiarities of the oxidation of α-methylstyrene by bacteria of the genus Pseudomonas. Mikrobiologiya 54: 136–140

    Google Scholar 

  • Eaton, RW & Timmis, KN (1986) Characterization of a plasmid-specified pathway for catabolism of isopropylbenzene in Pseudomonas putida RE 204. J Bacteriol 168: 123–131

    Google Scholar 

  • Evans, WC & Fuchs, G (1988) Anaerobic degradation of aromatic compounds. Annu. Rev. Microbiol 42: 289–317

    Google Scholar 

  • Foght, JM, Fedorak, PM & Westlake, DWS (1990) Mineralization of [14C]hexadecane and [14C]phenanthrene in crude oil: Specificity amoung bacterial isolates. Can. J. Microbiol 36: 169–175

    Google Scholar 

  • Franklin, FCH, Bagdasarian, M, Bagdasarian, MM & Timmis, KN (1981) Molecular and functional analysis of TOL plasmid pWWO from Pseudomonas putida and cloning of the entire regulated aromatic ring meta cleavage pathway. Proc. Acad. Sci. USA 78: 7458–7462

    Google Scholar 

  • Furukawa, K & Suzuki, H (1988) Gene manipulation of catabolic activities for production of intermediates of various biphenyl compounds. Appl. Microbiol. Biotechnol. 29: 363–369

    Google Scholar 

  • Gibson, DT (1971) The microbial oxidation of aromatic compounds. Crit. Rev. Microbiol. 1: 199–223

    Google Scholar 

  • Gibson, DT, Koch, JR & Kallio, RE (1968) Oxidative degradation of aromatic hydrocarbons by micro-organisms. I Enzymatic formation of catechol from benzene. Biochemistry 7: 2643–2656

    Google Scholar 

  • Gibson, DT, Cardini, GE, Maesels, FC & Kallio, RE (1970) Incorporation of 18O into benzene. Biochemistry 9: 1631–1635

    Google Scholar 

  • Gibson, DT, Roberts, RL, Wells, MC & Kobal, VM (1973) Oxidation of biphenyl by a Beijerincki species. Biochem. Biophys. Res. Commun. 50: 211–219

    Google Scholar 

  • Gibson, DT, Gschwendt, B, Yeh, WK & Kobal, VM (1973) Initial reaction in the oxidation of ethylbenzene by Pseudomonas putida. Biochemistry 12: 1520–1528

    Google Scholar 

  • Gibson, DT, Mahadevan, V & Davey, JF (1974) Bacterial metabolism of p- and m-xylene: Oxidation of the aromatic ring. J. Bacteriol. 119: 930–936

    Google Scholar 

  • Gibson, DT & Subramanian, V (1984) Microbial Degradation of aromatic hydrocarbons. In: Gibson, DT (Ed) Microbial Degradation of Organic Compounds (pp 361–369). Marcel Dekker New York

    Google Scholar 

  • Hartmans, S, Smits, JP, van der Werf, MJ, Volkering, F & de Bont, JAM (1989) Metabolism of styrene oxide ande 2-phenylethanol in the styrene-degrading Xanthobacter strain 124X. Appl. Environ. Microbiol. 55: 2850–2855

    Google Scholar 

  • Hartmans, S, van der Werf, MJ & de Bont, JAM (1990) Bacterial degradation of styrene involving a novel flavin adenine dinucleotide-dependent styrene monooxygenase. Appl. Environ. Microbiol. 56: 1347–1351

    Google Scholar 

  • Heitkamp, MA & Cerniglia, CE (1988) Mineralization of polycyclic aromatic hydrocarbons by a bacterium isolated from sediment below an oil field. Appl. Environ. Microbiol. 54: 1612–1614

    Google Scholar 

  • Högn, T & Jaenicke, L (1972) Benzene metabolism of Moraxella sp. Eur. J. Biochem. 30: 369–375

    Google Scholar 

  • Hooper, DJ (1978) Microbial degradation of aromatic hydrocarbons. In: Watkinson, RJ (Ed) Developments in the Biodegradation of Hydrocarbons (pp 85–112). Applied Science Publishers, London

    Google Scholar 

  • Ishigooka, H, Yashida, Y, Omori, T & Minoda, Y (1986) Enzymatic dioxygenation of biphenyl 2,3-diol and 3-isopropylcatechol. Agric. Biol. Chem. 50: 1045–1046

    Google Scholar 

  • Jigami, Y, Omori, T & Minoda, Y (1974a) A new ring fission product suggestive of a unknown reductive step in the degradation of n-butylbenzene by Pseudomonas. Agric. Biol. Chem. 38: 1757–1759

    Google Scholar 

  • Jigami, Y, Omori, T, Minoda, Y & Yamada, K (1974b) Formation of of 3-ethylsalicylic acid from 3-ethyltoluene by Pseudomonas ovalis. Agric. Biol. Chem. 38: 467–469

    Google Scholar 

  • Jigami, Y, Omori, T & Minoda, Y (1975) The degradation of isopropylbenzene and isobutylbenzene by Pseudomonas sp. Agric. Biol. Chem. 39: 1817–1788

    Google Scholar 

  • Khan, AA & Walia, SK (1990) Identification and localization of 3-phenylcatechol dioxygenase and 2-hydroxy-6-oxo-6-phenylhexa-2,4-dienoate hydrolase genes of Pseudomonas putida and expression in Eschericha coli. Appl. Environ. Microbiol. 56: 956–962

    Google Scholar 

  • Kunz, DA & Chapman, PJ (1981) Catabolism of pseudocumene and 3-ethyltoluene by Pseudomonas putida (arvilla) mt-2: evidence for new functions of the TOL (pWWO) plasmid. J. Bacteriol. 146: 179–191

    Google Scholar 

  • Laflamme, RE & Hite, RA (1978) The global distribution of polycyclic aromatic hydrocarbons in recent sediments. Geochim. Cosmomchim. Acta. 42: 289–303

    Google Scholar 

  • Ley, SV, Sternfeld & Taylor, SC (1987) Microbiol Oxidation in synthesis: a six step preparation of (+)-pinitol from benzene. Tetrahydron Lett. 28: 225–226

    Google Scholar 

  • Lovley, DR & Lonergan, DJ (1990) Anaerobic oxidation of toluene, phenol and p-cresol by the dissimilatory iron-reducting organism, GS-15. Appl. Environ Microbiol. 56: 1858–1864

    Google Scholar 

  • Lunt DO & Evans WC (1970) The microbial metabolism of biphenyl. Biochem J 118: 54P

  • Marr, EK & Stone, RW (1961) Bacterial oxidation of benzene. J. Bacteriol. 85: 425–430

    Google Scholar 

  • McCarty, PL, Rittmann, BE & Bouwer, EJ (1984) Microbial processes affecting chemical transformations in groundwater. In: Bitton, G & Gerba, CP (Eds) Groundwater Pollution Micobiology (pp 89–115). John Wiley & Sons, New York

    Google Scholar 

  • Mueller, JG, Chapman, PJ, Blattmann, BO & Pritchard, PH (1990) Isolation and characterization of a fluoranthene-utilizing strain of Pseudomonas paucimobilis. Appl Environ. Microbiol. 56: 1079–1086

    Google Scholar 

  • Nakazawa, T, Inouye, S & Nakazawa, A (1980) Physical and functional analysis of RP4-TOL plasmid recombinants: Analysis of insertion and deletion mutants. J. Bacteriol. 144: 222–231

    Google Scholar 

  • Omori, T, Jigami, Y & Minoda, Y (1974) Microbial oxidation of α-methylstyrene and β-methylstyrene. Agric. Biol. Chem. 38: 409–415

    Google Scholar 

  • Omori, T, Ishigooka, H & Minoda, Y (1986) Purification and some properties of 2-hydroxy-6-oxo-6-phenylhexa-2,4-dienoic acid (HODPA) reducing enzyme from Pseudomonas cruciviae S93B1, involved in the degradation of biphenyl. Agric. Biol. Chem. 50: 1513–1518

    Google Scholar 

  • Ramos, JL, Mermod, N & Timmis, KN (1987) Regulatory circuits controlling transcription of TOL plasmid operon encoding meta-cleavage pathway for degradation of alkylbenzoates by Pseudomonas. Mol. Microbiol. 1: 293–300

    Google Scholar 

  • Sala-Trepat, JM, Murray, K & Williams, PA (1972) The metabolic divergence in the meta cleavage pathway of catechols by Pseudomonas putida NCIB 10015. Eur. J. Biochem. 28: 347–356

    Google Scholar 

  • Sariaslani, FS, Harper, DB & Higgins, IJ (1974) Microbial degradation of hydrocarbons. Biochem. J. 140: 31–45

    Google Scholar 

  • Schell, MA (1986) Homology between nucleotide sequences of promoter regions of nah and sal operons of NAH7 plasmid of Pseudomonas putida. Proc. Natl. Acad. Sci. USA 83: 369–373

    Google Scholar 

  • Schell, MA & Wender, PE (1986) Indentification of the nahR genee product and nucleotide sequence required for its activation of the sal operon. J. Bacteriol. 166: 9–14

    Google Scholar 

  • Schraa, G, Bethe, BM, van Neerven, ARW, van den Tweel, WJJ, van der Wende, E & Zehnder, AJB (1987) Degradation 1,2-dimethylbenzene by Corynebacterium strain C125. Antonie van Leewenhoek 53: 159–170

    Google Scholar 

  • Schwartz, RD (1981) A novel reaction: meta hydroxylation of biphenyl by an actinomycete. Enzyme Microbial Technol. 3: 158–159

    Google Scholar 

  • Shirai, K (1986) Screening microorganisms for catechol production from benzene. Agric. Biol. Chem. 50: 2875–2880

    Google Scholar 

  • Shirai, K (1987) Catechol production from benzene through reaction with resting and immobilized cells of a mutant strain of Pseudomonas. Agric. Biol. Chem. 51: 121–128

    Google Scholar 

  • Shirai, K & Hisatsuka, K (1979) Isolation and identification of styrene assimiliating bacteria. Agric. Biol. Chem. 43: 1595–1596

    Google Scholar 

  • Simpson, HD, Green, J & Dalton, H (1987) Purification and some properties of a novel heat-stable cis-toluene dihydrodiol dehydrogenase. Biochem. J. 244: 585–590

    Google Scholar 

  • Sielicki, M, Focht, DD & Martin, JP (1978) Microbial transformations of styrene and [14C]styrene in soil and enrichment cultures. Appl. Environ. Microbiol. 35: 124–128

    Google Scholar 

  • Smith, MR & Ratledge, C (1989a) Catabolism of alkylbenzenes by Pseudomonas sp. NCIB 10643. Appl. Microbiol. Biotechnol. 32: 68–75

    Google Scholar 

  • Smith, MR & Ratledge, C (1989b) Catabolism of biphenyl by Pseudomonas sp. NCIB 10643 and Nocardia sp. NCIB 10503. Appl. Microbiol. Biotechnol. 30: 395–401

    Google Scholar 

  • Smith MR, Ewing M & Ratledge C (1991) The interactions of various aromatic substrates degraded by Pseudomonas sp. NCIB 10643: Synergistic inhibition of growth by two compounds which serve as growth substrates. Appl. Micobiol. Biotechnol. (in press)

  • Starovoitov, II, Selfionov, SA, Nefedova, MY & Adanin, VM (1986) Catabolism of diphenyl by Pseudomonas putida strain BS893 containing biodegradation plasmid pBS241. Microbiology (Engl. Transl.) 54: 726–727

    Google Scholar 

  • van den Tweel, WJJ, Janssens & de Bont, JAM (1986) Degradation of 4-hydroxyphenylacetate by Xanthobacter 124X. Antonie van Leeuwenhoek 52: 309–318

    Google Scholar 

  • van den Tweel, WJJ, Vorage, MJAW, Marsman, EH, Koppejan, J, Tramper, J & de Bont, JAM (1988) Continuous production of cis-1,2-dihydroxycyclohexa-3,5-diene (cis-benzeneglycol) from benzene by a mutant of a benzene degrading Pseudomonas sp. Enzyme Microbial Technol. 10: 134–142

    Google Scholar 

  • Vecht, SE, Platt, MW, Er-El, Z & Goldberg, I (1988) The growth of Pseudomonas putida on m-toluic acid and on toluene in batch and chemostat cultures. Appl. Microbiol. Biotechnol. 27: 587–592

    Google Scholar 

  • Weissenfels, WD, Beyer, M & Klein, J (1990) Degradation of fluorene and fluoranthene by pure bacterial cultures. Appl. Microbiol. Biotechnol. 32: 479–484

    Google Scholar 

  • Wigmore, GJ, Bayley, RC & Di Berardino, D (1974) Pseudomonas putida mutants defective in the catabolism of the products of meta fission of catechol and its methyl analogues. J. Bacteriol. 120: 31–37

    Google Scholar 

  • Winstanley, C, Taylor, SC & Williams, PA (1987) pWW174: A large plasmid from Acinetobacter calcoaceticus encoding benzene catabolism by the β-ketoadipate pathway. Mol. Microbiol. 1: 219–227

    Google Scholar 

  • You, IS & Gunsalus, IC (1986) Regulation of the nah and sal operons of plasmid NAH7: Evidence for a new function in nahR. Biochem. Biophys. Res. Commun. 141: 986–992

    Google Scholar 

  • You, IS, Ghosal, D & Gunsalus, IC (1988) Nucleotide sequence of plasmid NAH7 gene nahR and DNA binding of the nahR product. J. Bacteriol. 170: 5409–5415

    Google Scholar 

  • Zeyer, J, Eicher, P, Dolfing, J & Schwarzenbach, RP (1990) Anaerobic degradation of aromatic compounds. In: Kamely, D, Chakrabarty, A & Omenn, GS (Eds) Biotechnology and Biodegradation (pp 33–40). Gulf Publishing Company, Houston

    Google Scholar 

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Smith, M.R. The biodegradation of aromatic hydrocarbons by bacteria. Biodegradation 1, 191–206 (1990). https://doi.org/10.1007/BF00058836

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