1887

Abstract

Polycyclic aromatic hydrocarbons (PAHs) comprise a group of priority organic pollutants that are toxic and/or carcinogenic. Phenanthrene, the simplest PAH among recognized priority pollutants, is commonly used as a model compound for the study of PAH biodegradation. sp. strain PNB, capable of degrading phenanthrene as a sole carbon and energy source, was isolated from a municipal waste-contaminated soil sample. A combination of chromatographic and spectrometric analyses, together with oxygen uptake and enzyme activity studies, suggested the presence of phenanthrene degradation pathways in this strain. Identification of metabolites suggested that initial dioxygenation of phenanthrene took place at both 3,4- and 1,2-carbon positions; -cleavage of resultant diols led to the formation of 1-hydroxy-2-naphthoic acid and 2-hydroxy-1-naphthoic acid, respectively. The hydroxynaphthoic acids, in turn, were metabolized by a -cleavage pathway(s), leading to the formation of 2,2-dicarboxychromene and 2-hydroxychromene-2-glyoxylic acid, respectively. These metabolites were subsequently transformed to catechol via salicylic acid, which further proceeds towards the tricarboxylic acid cycle leading to complete mineralization of the compound phenanthrene. The present study establishes the metabolism of hydroxynaphthoic acids by a -cleavage pathway in the degradation of phenanthrene, expanding our current understanding of microbial degradation of PAHs.

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2012-03-01
2019-10-18
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References

  1. Adachi K. , Iwabuchi T. , Sano H. , Harayama S. . ( 1999; ). Structure of the ring cleavage product of 1-hydroxy-2-naphthoate, an intermediate of the phenanthrene-degradative pathway of Nocardioides sp. strain KP7. . J Bacteriol 181:, 757–763.[PubMed]
    [Google Scholar]
  2. Altschul S. F. , Gish W. , Miller W. , Myers E. W. , Lipman D. J. . ( 1990; ). Basic local alignment search tool. . J Mol Biol 215:, 403–410.[PubMed] [CrossRef]
    [Google Scholar]
  3. Balashova N. V. , Kosheleva I. A. , Golovchenko N. P. , Boronin A. M. . ( 1999; ). Phenanthrene metabolism by Pseudomonas and Burkholderia strains. . Process Biochem 35:, 291–296. [CrossRef]
    [Google Scholar]
  4. Barnsley E. A. . ( 1983; ). Phthalate pathway of phenanthrene metabolism: formation of 2′-carboxybenzalpyruvate. . J Bacteriol 154:, 113–117.[PubMed]
    [Google Scholar]
  5. Basta T. , Keck A. , Klein J. , Stolz A. . ( 2004; ). Detection and characterization of conjugative degradative plasmids in xenobiotic-degrading Sphingomonas strains. . J Bacteriol 186:, 3862–3872. [CrossRef] [PubMed]
    [Google Scholar]
  6. Bücker M. , Glatt H. R. , Platt K. L. , Avnir D. , Ittah Y. , Blum J. , Oesch F. . ( 1979; ). Mutagenicity of phenanthrene and phenanthrene K-region derivatives. . Mutat Res 66:, 337–348. [CrossRef] [PubMed]
    [Google Scholar]
  7. Cerniglia C. E. . ( 1992; ). Biodegradation of polycyclic aromatic hydrocarbons. . Biodegradation 3:, 351–368. [CrossRef]
    [Google Scholar]
  8. Davies J. I. , Evans W. C. . ( 1964; ). Oxidative metabolism of naphthalene by soil pseudomonads. The ring-fission mechanism. . Biochem J 91:, 251–261.[PubMed]
    [Google Scholar]
  9. Eaton R. W. , Chapman P. J. . ( 1992; ). Bacterial metabolism of naphthalene: construction and use of recombinant bacteria to study ring cleavage of 1,2-dihydroxynaphthalene and subsequent reactions. . J Bacteriol 174:, 7542–7554.[PubMed]
    [Google Scholar]
  10. Ensley B. D. , Ratzkin B. J. , Osslund T. D. , Simon M. J. , Wackett L. P. , Gibson D. T. . ( 1983; ). Expression of naphthalene oxidation genes in Escherichia coli results in the biosynthesis of indigo. . Science 222:, 167–169. [CrossRef] [PubMed]
    [Google Scholar]
  11. Evans W. C. , Fernley H. N. , Griffiths E. . ( 1965; ). Oxidative metabolism of phenanthrene and anthracene by soil pseudomonads: the ring fission mechanism. . Biochem J 95:, 819–831.[PubMed]
    [Google Scholar]
  12. Ghosal D. , Chakraborty J. , Khara P. , Dutta T. K. . ( 2010; ). Degradation of phenanthrene via meta-cleavage of 2-hydroxy-1-naphthoic acid by Ochrobactrum sp. strain PWTJD. . FEMS Microbiol Lett 313:, 103–110. [CrossRef] [PubMed]
    [Google Scholar]
  13. Ghosh D. K. , Mishra A. K. . ( 1983; ). Oxidation of phenanthrene by a strain of Micrococcus: evidence of protocatechuate pathway. . Curr Microbiol 9:, 219–224. [CrossRef]
    [Google Scholar]
  14. Gibson D. T. , Subramanian V. . ( 1984; ). Microbial degradation of aromatic hydrocarbons. . In Microbial Degradation of Organic Compounds, pp. 181–252. Edited by Gibson D. T. . . New York:: Dekker;.
    [Google Scholar]
  15. Gillam E. M. J. , Guengerich F. P. . ( 2001; ). Exploiting the versatility of human cytochrome P450 enzymes: the promise of blue roses from biotechnology. . IUBMB Life 52:, 271–277. [CrossRef] [PubMed]
    [Google Scholar]
  16. Habe H. , Omori T. . ( 2003; ). Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. . Biosci Biotechnol Biochem 67:, 225–243. [CrossRef] [PubMed]
    [Google Scholar]
  17. Harpel M. R. , Lipscomb J. D. . ( 1990; ). Gentisate 1,2-dioxygenase from pseudomonas. Purification, characterization, and comparison of the enzymes from Pseudomonas testosteroni and Pseudomonas acidovorans . . J Biol Chem 265:, 6301–6311.[PubMed]
    [Google Scholar]
  18. Hayaishi O. , Katagiri M. , Rothberg S. . ( 1957; ). Studies on oxygenases; pyrocatechase. . J Biol Chem 229:, 905–920.[PubMed]
    [Google Scholar]
  19. Holtz J. G. , Krieg N. R. , Sneath P. H. A. , Staley J. T. . ( 1994; ). Bergey’s Manual of Determinative Bacteriology, , 9th edn.. Baltimore:: Lippincott Williams and Wilkins;.
    [Google Scholar]
  20. Houghton J. E. , Shanley M. S. . ( 1994; ). Catabolic potential of pseudomonads: a regulatory perspective. . In Biological Degradation and Bioremediation of Toxic Chemicals, pp. 11–32. Edited by Chaudhry R. G. . . London:: Chapman & Hall;.
    [Google Scholar]
  21. Iwabuchi T. , Harayama S. . ( 1997; ). Biochemical and genetic characterization of 2-carboxybenzaldehyde dehydrogenase, an enzyme involved in phenanthrene degradation by Nocardioides sp. strain KP7. . J Bacteriol 179:, 6488–6494.[PubMed]
    [Google Scholar]
  22. Johnson J. L. . ( 1994; ). Similarity analysis of rRNAs. . In Methods for General and Molecular Bacteriology, pp. 683–700. Edited by Gerhardt P. , Murray R. G. E. , Wood W. A. , Krieg N. R. . . Washington, DC:: American Society for Microbiology;.
    [Google Scholar]
  23. Keith L. H. , Telliard W. A. . ( 1979; ). Priority pollutants: I - a perspective view. . Environ Sci Technol 13:, 416–423. [CrossRef]
    [Google Scholar]
  24. Keum Y. S. , Seo J. S. , Hu Y. , Li Q. X. . ( 2006; ). Degradation pathways of phenanthrene by Sinorhizobium sp. C4. . Appl Microbiol Biotechnol 71:, 935–941. [CrossRef] [PubMed]
    [Google Scholar]
  25. Kiyohara H. , Nagao K. . ( 1978; ). The catabolism of phenanthrene and naphthalene by bacteria. . J Gen Microbiol 105:, 69–75.[CrossRef]
    [Google Scholar]
  26. Kiyohara H. , Nagao K. , Nomi R. . ( 1976; ). Degradation of phenanthrene through o-phthalate by an Aeromonas sp. . Agric Biol Chem 40:, 1075–1082. [CrossRef]
    [Google Scholar]
  27. Kojima Y. , Itada N. , Hayaishi O. . ( 1961; ). Metapyrocatachase: a new catechol-cleaving enzyme. . J Biol Chem 236:, 2223–2228.[PubMed]
    [Google Scholar]
  28. Krivobok S. , Kuony S. , Meyer C. , Louwagie M. , Willison J. C. , Jouanneau Y. . ( 2003; ). Identification of pyrene-induced proteins in Mycobacterium sp. strain 6PY1: evidence for two ring-hydroxylating dioxygenases. . J Bacteriol 185:, 3828–3841. [CrossRef] [PubMed]
    [Google Scholar]
  29. Kuykendall L. D. , Roy M. A. , O’Neill J. J. , Devine T. E. . ( 1988; ). Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum . . Int J Syst Bacteriol 38:, 358–361. [CrossRef]
    [Google Scholar]
  30. Lowry O. H. , Rosebrough N. J. , Farr A. L. , Randall R. J. . ( 1951; ). Protein measurement with the Folin phenol reagent. . J Biol Chem 193:, 265–275.[PubMed]
    [Google Scholar]
  31. Mallick S. , Chatterjee S. , Dutta T. K. . ( 2007; ). A novel degradation pathway in the assimilation of phenanthrene by Staphylococcus sp. strain PN/Y via meta-cleavage of 2-hydroxy-1-naphthoic acid: formation of trans-2,3-dioxo-5-(2′-hydroxyphenyl)-pent-4-enoic acid. . Microbiology 153:, 2104–2115. [CrossRef] [PubMed]
    [Google Scholar]
  32. Mallick S. , Chakraborty J. , Dutta T. K. . ( 2011; ). Role of oxygenases in guiding diverse metabolic pathways in the bacterial degradation of low-molecular-weight polycyclic aromatic hydrocarbons: a review. . Crit Rev Microbiol 37:, 64–90. [CrossRef] [PubMed]
    [Google Scholar]
  33. Maruyama T. , Park H.-D. , Ozawa K. , Tanaka Y. , Sumino T. , Hamana K. , Hiraishi A. , Kato K. . ( 2006; ). Sphingosinicella microcystinivorans gen. nov., sp. nov., a microcystin-degrading bacterium. . Int J Syst Evol Microbiol 56:, 85–89. [CrossRef] [PubMed]
    [Google Scholar]
  34. Miller L. T. . ( 1982; ). Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. . J Clin Microbiol 16:, 584–586.[PubMed]
    [Google Scholar]
  35. Moody J. D. , Freeman J. P. , Doerge D. R. , Cerniglia C. E. . ( 2001; ). Degradation of phenanthrene and anthracene by cell suspensions of Mycobacterium sp. strain PYR-1. . Appl Environ Microbiol 67:, 1476–1483. [CrossRef] [PubMed]
    [Google Scholar]
  36. Ngai K. L. , Neidle E. L. , Ornston L. N. . ( 1990; ). Catechol and chlorocatechol 1,2-dioxygenases. . Methods Enzymol 188:, 122–126. [CrossRef] [PubMed]
    [Google Scholar]
  37. Parales R. E. . ( 2003; ). The role of active-site residues in naphthalene dioxygenase. . J Ind Microbiol Biotechnol 30:, 271–278. [CrossRef] [PubMed]
    [Google Scholar]
  38. Peng R.-H. , Xiong A.-S. , Xue Y. , Fu X.-Y. , Gao F. , Zhao W. , Tian Y.-S. , Yao Q.-H. . ( 2008; ). Microbial biodegradation of polyaromatic hydrocarbons. . FEMS Microbiol Rev 32:, 927–955. [CrossRef] [PubMed]
    [Google Scholar]
  39. Pinyakong O. , Habe H. , Supaka N. , Pinpanichkarn P. , Juntongjin K. , Yoshida T. , Furihata K. , Nojiri H. , Yamane H. , Omori T. . ( 2000; ). Identification of novel metabolites in the degradation of phenanthrene by Sphingomonas sp. strain P2. . FEMS Microbiol Lett 191:, 115–121. [CrossRef] [PubMed]
    [Google Scholar]
  40. Pinyakong O. , Habe H. , Omori T. . ( 2003; ). The unique aromatic catabolic genes in sphingomonads degrading polycyclic aromatic hydrocarbons (PAHs). . J Gen Appl Microbiol 49:, 1–19. [CrossRef] [PubMed]
    [Google Scholar]
  41. Romine M. F. , Stillwell L. C. , Wong K. K. , Thurston S. J. , Sisk E. C. , Sensen C. , Gaasterland T. , Fredrickson J. K. , Saffer J. D. . ( 1999; ). Complete sequence of a 184-kilobase catabolic plasmid from Sphingomonas aromaticivorans F199. . J Bacteriol 181:, 1585–1602.[PubMed]
    [Google Scholar]
  42. Schuler L. , Jouanneau Y. , Chadhain S. M. N. , Meyer C. , Pouli M. , Zylstra G. J. , Hols P. , Agathos S. N. . ( 2009; ). Characterization of a ring-hydroxylating dioxygenase from phenanthrene-degrading Sphingomonas sp. strain LH128 able to oxidize benz[a]anthracene. . Appl Microbiol Biotechnol 83:, 465–475. [CrossRef] [PubMed]
    [Google Scholar]
  43. Seo J. S. , Keum Y. S. , Hu Y. , Lee S. E. , Li Q. X. . ( 2006; ). Phenanthrene degradation in Arthrobacter sp. P1-1: initial 1,2-, 3,4- and 9,10-dioxygenation, and meta- and ortho-cleavages of naphthalene-1,2-diol after its formation from naphthalene-1,2-dicarboxylic acid and hydroxyl naphthoic acids. . Chemosphere 65:, 2388–2394. [CrossRef] [PubMed]
    [Google Scholar]
  44. Seo J. S. , Keum Y. S. , Hu Y. , Lee S. E. , Li Q. X. . ( 2007; ). Degradation of phenanthrene by Burkholderia sp. C3: initial 1,2- and 3,4-dioxygenation and meta- and ortho-cleavage of naphthalene-1,2-diol. . Biodegradation 18:, 123–131. [CrossRef] [PubMed]
    [Google Scholar]
  45. Seo J. S. , Keum Y. S. , Li Q. X. . ( 2009; ). Bacterial degradation of aromatic compounds. . Int J Environ Res Public Health 6:, 278–309. [CrossRef] [PubMed]
    [Google Scholar]
  46. Smibert R. M. , Krieg N. R. . ( 1994; ). Phenotypic characterization. . In Methods for General and Molecular Bacteriology, pp. 611–654. Edited by Gerhardt P. , Murray R. G. E. , Wood W. A. , Krieg N. R. . . Washington, DC:: American Society for Microbiology;.
    [Google Scholar]
  47. Stolz A. . ( 2009; ). Molecular characteristics of xenobiotic-degrading sphingomonads. . Appl Microbiol Biotechnol 81:, 793–811. [CrossRef] [PubMed]
    [Google Scholar]
  48. Takeuchi M. , Hamana K. , Hiraishi A. . ( 2001; ). Proposal of the genus Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. . Int J Syst Evol Microbiol 51:, 1405–1417.[PubMed]
    [Google Scholar]
  49. Yabuuchi E. , Kosako Y. . ( 2005; ). Order IV. Sphingomonadaceae . . In Bergey’s Manual of Systematic Bacteriology, , 2nd edn., vol. 2, pp. 233–286. Edited by Brenner D. J. , Krieg N. R. , Staley J. T. , Garrity G. M. . . New York:: Springer;.
    [Google Scholar]
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