Skip to main content
PMC home page
Applied and Environmental Microbiology logoLink to Applied and Environmental Microbiology
. 1988 Apr;54(4):929–936. doi: 10.1128/aem.54.4.929-936.1988

Two-Stage Mineralization of Phenanthrene by Estuarine Enrichment Cultures

William F Guerin 1,*, Galen E Jones 1
PMCID: PMC202575  PMID: 16347614

Abstract

The polycyclic aromatic hydrocarbon phenanthrene was mineralized in two stages by soil, estuarine water, and sediment microbial populations. At high concentrations, phenanthrene was degraded, with the concomitant production of biomass and accumulation of Folin-Ciocalteau-reactive aromatic intermediates. Subsequent consumption of these intermediates resulted in a secondary increase in biomass. Analysis of intermediates by high-performance liquid chromatography, thin-layer chromatography, and UV absorption spectrometry showed 1-hydroxy-2-naphthoic acid (1H2NA) to be the predominant product. A less pronounced two-stage mineralization pattern was also observed by monitoring 14CO2 production from low concentrations (0.5 mg liter−1) of radiolabeled phenanthrene. Here, mineralization of 14C-labeled 1H2NA could explain the incremental 14CO2 produced during the later part of the incubations. Accumulation of 1H2NA by isolates obtained from enrichments was dependent on the initial phenanthrene concentration. The production of metabolites during polycyclic aromatic hydrocarbon biodegradation is discussed with regard to its possible adaptive significance and its methodological implications.

Full text

PDF
933

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abbott B. J., Gledhill W. E. The extracellular accumulation of metabolic products by hydrocarbon-degrading microorganisms. Adv Appl Microbiol. 1971;14:249–388. doi: 10.1016/s0065-2164(08)70546-x. [DOI] [PubMed] [Google Scholar]
  2. Aranha H. G., Brown L. R. Effect of nitrogen source on end products of naphthalene degradation. Appl Environ Microbiol. 1981 Jul;42(1):74–78. doi: 10.1128/aem.42.1.74-78.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barnsley E. A. Phthalate pathway of phenanthrene metabolism: formation of 2'-carboxybenzalpyruvate. J Bacteriol. 1983 Apr;154(1):113–117. doi: 10.1128/jb.154.1.113-117.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bauer J. E., Capone D. G. Degradation and mineralization of the polycyclic aromatic hydrocarbons anthracene and naphthalene in intertidal marine sediments. Appl Environ Microbiol. 1985 Jul;50(1):81–90. doi: 10.1128/aem.50.1.81-90.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bumpus J. A., Tien M., Wright D., Aust S. D. Oxidation of persistent environmental pollutants by a white rot fungus. Science. 1985 Jun 21;228(4706):1434–1436. doi: 10.1126/science.3925550. [DOI] [PubMed] [Google Scholar]
  6. Cerniglia C. E., Freeman J. P., Mitchum R. K. Glucuronide and sulfate conjugation in the fungal metabolism of aromatic hydrocarbons. Appl Environ Microbiol. 1982 May;43(5):1070–1075. doi: 10.1128/aem.43.5.1070-1075.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cox D. P., Williams A. L. Biological Process for Converting Naphthalene to cis-1,2-Dihydroxy-1,2-Dihydronaphthalene. Appl Environ Microbiol. 1980 Feb;39(2):320–326. doi: 10.1128/aem.39.2.320-326.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dagley S. Determinants of biodegradability. Q Rev Biophys. 1978 Nov;11(4):577–602. doi: 10.1017/s0033583500005679. [DOI] [PubMed] [Google Scholar]
  9. Dalton H., Stirling D. I. Co-metabolism. Philos Trans R Soc Lond B Biol Sci. 1982 Jun 11;297(1088):481–496. doi: 10.1098/rstb.1982.0056. [DOI] [PubMed] [Google Scholar]
  10. EVANS W. C., FERNLEY H. N., GRIFFITHS E. OXIDATIVE METABOLISM OF PHENANTHRENE AND ANTHRACENE BY SOIL PSEUDOMONADS. THE RING-FISSION MECHANISM. Biochem J. 1965 Jun;95:819–831. doi: 10.1042/bj0950819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. FOSTER J. W. Hydrocarbons as substrates for microorganisms. Antonie Van Leeuwenhoek. 1962;28:241–274. doi: 10.1007/BF02538739. [DOI] [PubMed] [Google Scholar]
  12. Gibson D. T., Mahadevan V., Jerina D. M., Yogi H., Yeh H. J. Oxidation of the carcinogens benzo [a] pyrene and benzo [a] anthracene to dihydrodiols by a bacterium. Science. 1975 Jul 25;189(4199):295–297. doi: 10.1126/science.1145203. [DOI] [PubMed] [Google Scholar]
  13. Guerin W. F., Jones G. E. Mineralization of phenanthrene by a Mycobacterium sp. Appl Environ Microbiol. 1988 Apr;54(4):937–944. doi: 10.1128/aem.54.4.937-944.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Harder W., Dijkhuizen L. Strategies of mixed substrate utilization in microorganisms. Philos Trans R Soc Lond B Biol Sci. 1982 Jun 11;297(1088):459–480. doi: 10.1098/rstb.1982.0055. [DOI] [PubMed] [Google Scholar]
  15. Herbes S. E. Rates of microbial transformation of polycyclic aromatic hydrocarbons in water and sediments in the vicinity of a coal-coking wastewater discharge. Appl Environ Microbiol. 1981 Jan;41(1):20–28. doi: 10.1128/aem.41.1.20-28.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Herbes S. E., Schwall L. R. Microbial transformation of polycyclic aromatic hydrocarbons in pristine and petroleum-contaminated sediments. Appl Environ Microbiol. 1978 Feb;35(2):306–316. doi: 10.1128/aem.35.2.306-316.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Herbes S. E., Schwall L. R., Williams G. A. Rate of microbial transformation of polycyclic aromatic hydrocarbons: a chromatographic quantification procedure. Appl Environ Microbiol. 1977 Aug;34(2):244–246. doi: 10.1128/aem.34.2.244-246.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hulbert M. H. Cometabolism: a critique. J Theor Biol. 1977 Nov 21;69(2):287–291. doi: 10.1016/0022-5193(77)90137-0. [DOI] [PubMed] [Google Scholar]
  19. Jerina D. M., Selander H., Yagi H., Wells M. C., Davey J. F., Mahadevan V., Gibson D. T. Dihydrodiols from anthracene and phenanthrene. J Am Chem Soc. 1976 Sep 15;98(19):5988–5996. doi: 10.1021/ja00435a035. [DOI] [PubMed] [Google Scholar]
  20. KLAUSMEIER R. E., STRAWINSKI R. J. Microbial oxidation of naphthalene. I. Factors concerning salicylate accumulation. J Bacteriol. 1957 Apr;73(4):461–464. doi: 10.1128/jb.73.4.461-464.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kiyohara H., Nagao K., Kouno K., Yano K. Phenanthrene-degrading phenotype of Alcaligenes faecalis AFK2. Appl Environ Microbiol. 1982 Feb;43(2):458–461. doi: 10.1128/aem.43.2.458-461.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kiyohara H., Nagao K., Yana K. Rapid screen for bacteria degrading water-insoluble, solid hydrocarbons on agar plates. Appl Environ Microbiol. 1982 Feb;43(2):454–457. doi: 10.1128/aem.43.2.454-457.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  24. MURPHY J. F., STONE R. W. The bacterial dissimilation of naphthalene. Can J Microbiol. 1955 Aug;1(7):579–588. doi: 10.1139/m55-070. [DOI] [PubMed] [Google Scholar]
  25. Maccubbin A. E., Black P., Trzeciak L., Black J. J. Evidence for polynuclear aromatic hydrocarbons in the diet of bottom-feeding fish. Bull Environ Contam Toxicol. 1985 Jun;34(6):876–882. doi: 10.1007/BF01609820. [DOI] [PubMed] [Google Scholar]
  26. Perry J. J. Microbial cooxidations involving hydrocarbons. Microbiol Rev. 1979 Mar;43(1):59–72. doi: 10.1128/mr.43.1.59-72.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Phillips D. H. Fifty years of benzo(a)pyrene. Nature. 1983 Jun 9;303(5917):468–472. doi: 10.1038/303468a0. [DOI] [PubMed] [Google Scholar]
  28. ROGOFF M. H., WENDER I. 3-Hydroxy-2-naphthoic acid as an intermediate in bacterial dissimilation of anthracene. J Bacteriol. 1957 Jul;74(1):108–109. doi: 10.1128/jb.74.1.108-109.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. ROGOFF M. H., WENDER I. The microbiology of coal. I. Bacterial oxidation of phenanthrene. J Bacteriol. 1957 Feb;73(2):264–268. doi: 10.1128/jb.73.2.264-268.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shamsuzzaman K. M., Barnsley E. A. The regulation of naphthalene oxygenase in pseudomonads. J Gen Microbiol. 1974 Jul;83(0):165–170. doi: 10.1099/00221287-83-1-165. [DOI] [PubMed] [Google Scholar]
  31. Skriabin G. K., Starovoitov I. I., Borisoglebskaia A. N., Borodin A. M. Okislenie naftalina shtammom Pseduomonas putida, nesushchim mutantnuiu plazmidu. Mikrobiologiia. 1978 Mar-Apr;47(2):273–277. [PubMed] [Google Scholar]
  32. WALKER N., WILTSHIRE G. H. The breakdown of naphthalene by a soil bacterium. J Gen Microbiol. 1953 Apr;8(2):273–276. doi: 10.1099/00221287-8-2-273. [DOI] [PubMed] [Google Scholar]
  33. Wodzinski R. S., Johnson M. J. Yields of bacterial cells from hydrocarbons. Appl Microbiol. 1968 Dec;16(12):1886–1891. doi: 10.1128/am.16.12.1886-1891.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Applied and Environmental Microbiology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES