Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Metabolism of fluoranthene by Mycobacterium sp. strain AP1

Abstract

The pyrene-degrading Mycobacterium strain AP1 was found to utilize fluoranthene as a sole source of carbon and energy. Identification of metabolites formed from fluoranthene (by growing cells and washed-cell suspensions), the kinetics of metabolite accumulation, and metabolite-feeding studies all indicated that strain AP1 oxidizes fluoranthene using three alternative routes. The first route is initiated by dioxygenation at C-7 and C-8 and, following meta cleavage and pyruvate release, produces a hydroxyacenaphthoic acid that is decarboxylated to acenaphthenone (V). Monooxygenation of this ketone to the quinone and subsequent hydrolysis generates naphthalene-1,8-dicarboxylic acid (IV), which is further degraded via benzene-1,2,3-tricarboxylic acid (III). A second route involves dioxygenation at C-1 and C-2, followed by dehydrogenation and meta cleavage of the resulting diol. A two-carbon fragment excision of the meta cleavage product yields 9-fluorenone-1-carboxylic acid (II), which appears to undergo angular dioxygenation and further degradation to produce benzene-1,2,3-tricarboxylic acid (III), merging this route with the 7,8-dioxygenation route. Decarboxylation of benzene-1,2,3-tricarboxylic acid to phthalate (VIII), as well as further oxidation of the latter, would connect both routes with the central metabolism. The identification of Z-9-carboxymethylenefluorene-1-carboxylic acid (I) suggests a third route for fluoranthene degradation involving dioxygenation at C-2, C-3, and ortho cleavage. There is no evidence of any further degradation of this compound.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Black TH (1983) The preparation and reactions of diazomethane. Aldrichimica Acta 16:39

  2. Boldrin B, Tiehm A, Fritzsche C (1993) Degradation of phenanthrene, fluorene, fluoranthene, and pyrene by a Mycobacterium sp. Appl Environ Microbiol 59:1927–1930

  3. Casellas M, Grifoll M, Bayona JM, Solanas AM (1997) New metabolites in the degradation of fluorene by Arthrobacter sp. strain F101. Appl Environ Microbiol 63:1–8

  4. Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368

  5. Daniels L, Handson RS, Philips JA (1994) Chemical analysis. In: Gerhardt AP, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. ASM Press, Washington, DC, pp 512

  6. Gordon L, Dobson DW (2001) Fluoranthene degradation in Pseudomonas alcaligenes PA-10. Biodegradation 12:393–400

  7. Grifoll M, Selifonov SA, Chapman PJ (1994) Evidence for a novel pathway in the degradation of fluorene by Pseudomonas sp. strain F274. Appl Environ Microbiol 60:2438–2449

  8. Grifoll M, Selifonov SA, Gatlin CV, Chapman PJ (1995) Actions of a versatile fluorene-degrading bacterial isolate on polycyclic aromatic hydrocarbons. Appl Environ Microbiol 61:3711–3723

  9. Hareland WA, Crawford RL, Chapman PJ, Dagley S (1975) Metabolic function and properties of 4-hydroxyphenyl acetic 1-hydroxylase from Pseudomonas acidovorans. J Bacteriol 121:272–285

  10. Heitkamp MA, Freeman JP, Miller DW, Cerniglia CE (1988) Pyrene degradation by a Mycobacterium sp. Identification of ring oxidation and ring fission products. Appl Environ Microbiol 54:2556–2565

  11. Ho Y, Jackson M, Yang Y, Mueller JG, Pritchard PH (2000) Characterization of fluoranthene- and pyrene-degrading bacteria isolated from PAH contaminated soil and sediments. J Ind Microbiol Biotech 24:100–112

  12. Imuta M, Ziffer H (1978) Convenient method for the preparation of reactive oxiranes by direct epoxidation. J Org Chem 44:1351–1352

  13. International Association for Research Cancer (1983) IARC monographs on the evaluation of the carcinogenic risk of chemicals to humans. Polynuclear aromatic compounds, part 1. Int Assoc Res Chem Monogr 32:57–62 and 355–364

  14. Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons. A review of the microbial degradation of benzo[a]pyrene. Int Biodeterior Biodegrad 45:57–88

  15. Juhasz AL, Britz ML, Stanley GA (1997) Degradation of fluoranthenene, pyrene, benz[a]anthracene and dibenz[a,h,]anthracene by Burkholderia cepacia. J Appl Microbiol 83:189–198

  16. Kanaly RA, Harayama S (2000) Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182:2059–2067

  17. Kästner M (2000) Degradation of aromatic and polyaromatic compounds. In: Rehm HJ, Reed G, Pühler A, Stadler P (eds) Environmental processes II: soil decontamination, biotechnology, vol. 11b. Wiley, New York, pp 212–239

  18. Kelley I, Freeman JP, Evans FE, Cerniglia CE (1993) Identification of metabolites from the degradation of fluoranthene by Mycobacterium sp. strain PYR-1. Appl Environ Microbiol 59:800–806

  19. Kiyohara H, Nagao K (1978) The catabolism of phenanthrene and naphthalene by bacteria. J Gen Microbiol 105:69–75

  20. López Z, Vila J, Grifoll M (2005) Metabolism of fluoranthene by mycobacterial strains isolated by their ability to grow in fluoranthene or pyrene. J Ind Microbiol Biotech (in press)

  21. Neidhard FC, Ingraham JL, Schaechter M (1990) Physiology of the bacterial cell. A molecular approach. Sinauer Associates, Sunderland, Massachusetts

  22. Rehmann K, Hertkorn N, Kettrup AA (2001) Fluoranthene metabolism in Mycobacterium sp. strain KR20: identity of pathway intermediates during degradation and growth. Microbiology 147:2783–2794

  23. Schocken MJ, Gibson DT (1984) Bacterial oxidation of the polycyclic aromatic hydrocarbons acenaphthene and acenaphthylene. Appl Environ Microbiol 48:10–16

  24. Selifonov SA, Grifoll M, Eaton RW, Chapman PJ (1995) Oxidation of naphthenoaromatic and methyl-substituted aromatic compounds by naphthalene 1,2-dioxygenase. Appl Environ Microbiol 62:507–514

  25. Šepič E, Bricelj M, Leškovsek H (1998) Degradation of fluoranthene by Pasteurella sp. IFA and Mycobacterium sp. PYR-1: isolation and identification of metabolites. J Appl Microbiol 85:746–754

  26. Story SP, Parker SH, Hayasaka S, Riley MB, Kline EL (2001) Convergent and divergent points in catabolic pathways involved in utilization of fluoranthene, naphthalene, anthracene, and phenanthrene by Sphingomonas paucimobilis var. EPA505. J Ind Microbiol Biotech 26:369–382

  27. van Herwijnen R, Springael D, Slot P, Govers HAJ, Parsons JR (2003) Degradation of anthracene by Mycobacterium sp. strain LB501T proceeds via a novel pathway, through o-phthalic acid. Appl Environ Microbiol 69:186–190

  28. Vila J, López Z, Sabaté J, Minguillón C, Solanas AM, Grifoll M (2001) Identification of a novel metabolite in the degradation of pyrene by Mycobacterium sp. strain AP1. Actions of the isolate on two- and three-ring polycyclic aromatic hydrocarbons. Appl Environ Microbiol 67:5497–5505

  29. Weissenfels WD, Beyer M, Klein J, Rehm HJ (1991) Microbial metabolism of fluoranthene: isolation and identification of ring fission products. Appl Microbiol Biotechnol 34:435–528

Download references

Acknowledgements

This research was funded by a grant from the Spanish Government's National Plan for Research (REN-2001-3523). Zaira López was the recipient of a doctoral fellowship from the National Council for Science and Technology (CONACyT) of Mexico (123106/139030). The authors are members of the Centre de Referència en Biotecnologia (CeRBa), which receives funding from the Generalitat de Catalunya. We are grateful to Asunción Marín (Serveis Científico-Tècnics, Universitat de Barcelona) for the acquisition of GC-MS data.

Author information

Correspondence to Magdalena Grifoll.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

López, Z., Vila, J., Minguillón, C. et al. Metabolism of fluoranthene by Mycobacterium sp. strain AP1. Appl Microbiol Biotechnol 70, 747–756 (2006). https://doi.org/10.1007/s00253-005-0120-9

Download citation

Keywords

  • PAHs
  • Dicarboxylic Acid
  • Fluoranthene
  • Mineral Salt Medium
  • Naphthalic Anhydride