Applied Microbiology and Biotechnology

, Volume 95, Issue 3, pp 789–798 | Cite as

Biodegradation of polycyclic aromatic hydrocarbons by a halophilic microbial consortium

  • Seyed Mohammad Mehdi Dastgheib
  • Mohammad Ali Amoozegar
  • Khosro Khajeh
  • Mahmoud Shavandi
  • Antonio Ventosa
Environmental biotechnology


In this study we investigated the phenanthrene degradation by a halophilic consortium obtained from a saline soil sample. This consortium, named Qphe, could efficiently utilize phenanthrene in a wide range of NaCl concentrations, from 1% to 17% (w/v). Since none of the purified isolates could degrade phenanthrene, serial dilutions were performed and resulted in a simple polycyclic aromatic hydrocarbon (PAH)-degrading culture named Qphe-SubIV which was shown to contain one culturable Halomonas strain and one unculturable strain belonging to the genus Marinobacter. Qphe-SubIV was shown to grow on phenanthrene at salinities as high as 15% NaCl (w/v) and similarly to Qphe, at the optimal NaCl concentration of 5% (w/v), could degrade more than 90% of the amended phenanthrene in 6 days. The comparison of the substrate range of the two consortiums showed that the simplified culture had lost the ability to degrade chrysene but still could grow on other polyaromatic substrates utilized by Qphe. Metabolite analysis by HPLC and GC–MS showed that 2-hydroxy 1-naphthoic acid and 2-naphthol were among the major metabolites accumulated in the Qphe-SubIV culture media, indicating that an initial dioxygenation step might proceed at C1 and C2 positions. By investigating the growth ability on various substrates along with the detection of catechol dioxygenase gene, it was postulated that the uncultured Marinobacter strain had the central role in phenanthrene degradation and the Halomonas strain played an auxiliary role in the culture by utilizing phenanthrene metabolites whose accumulation in the media could be toxic.


Polycyclic aromatic hydrocarbons (PAHs) Phenanthrene Biodegradation Halophile Marinobacter Halomonas Consortium 


  1. Ananyina LN, Plotnikova EG, Gavrish EY, Demakov VA, Evtushenko LI (2007) Salinicola socius gen. nov., sp. nov., a moderately halophilic bacterium from a naphthalene-utilizing microbial association. Mikrobiologiya 76:324–330Google Scholar
  2. Arulazhagan P, Vasudevan N, Yeom IT (2010) Biodegradation of polycyclic aromatic hydrocarbon by bacterial consortium isolated from marine environment. Int J Environ Sci Tech 7:639–652Google Scholar
  3. Cerniglia CE (1993) Biodegradation of polycyclic aromatic hydrocarbons. Curr Opin Biotechnol 3:331–338CrossRefGoogle Scholar
  4. Dastgheib SM, Amoozegar MA, Khajeh K, Ventosa A (2011) A halotolerant Alcanivorax sp. strain with potential application in saline soil remediation. Appl Microbiol Biotechnol 90:305–312CrossRefGoogle Scholar
  5. García MT, Ventosa A, Mellado E (2005) Catabolic versatility of aromatic compound-degrading halophilic bacteria. FEMS Microbiol Ecol 1:97–109CrossRefGoogle Scholar
  6. Haritash AK, Kaushik CPJ (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15CrossRefGoogle Scholar
  7. Hart DJ, Vreeland RH (1988) Changes in the hydrophobic–hydrophilic cell surface character of Halomonas elongata in response to NaCl. J Bacteriol 170:132–135Google Scholar
  8. Kanaly RA, Harayama S (2000) Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182:2059–2067CrossRefGoogle Scholar
  9. Kasai Y, Kishira H, Harayama S (2002) Bacteria belonging to the genus Cycloclasticus play a primary role in the degradation of aromatic hydrocarbons released in a marine environment. Appl Environ Microbiol 68:5625–5633CrossRefGoogle Scholar
  10. Le Borgne S, Paniagua D, Vasquez-Duhalt R (2008) Biodegradation of organic pollutants by halophilic bacteria and archaea. J Mol Microbiol Biotechnol 15:74–92CrossRefGoogle Scholar
  11. Li J, Bai R (2005) Effect of a commercial alcohol ethoxylate surfactant (C11–15E7) on biodegradation of phenanthrene in a saline water medium by Neptunomonas naphthovorans. Biodegradation 16:57–65CrossRefGoogle Scholar
  12. Liu C, Shao Z (2005) Alcanivorax dieselolei sp. nov., a novel alkane degrading bacterium isolated from sea water and deep-sea sediment. Int J Syst Evol Microbiol 55:1181–1186CrossRefGoogle Scholar
  13. Mallick S, Chatterjee S, Dutta TK (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-(29-hydroxyphenyl)-pent-4-enoic acid. Microbiology 153:2104–2115CrossRefGoogle Scholar
  14. Margesin R, Schinner F (2001) Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 5:73–78CrossRefGoogle Scholar
  15. Martín S, Márquez MC, Sánchez-Porro C, Mellado E, Arahal DR, Ventosa A (2003) Marinobacter lipolyticus sp. nov., a novel moderate halophile with lipolytic activity. Int J Syst Evol Microbiol 53:1383–1387CrossRefGoogle Scholar
  16. McGenity TJ, Gramain A (2010) Cultivation of halophilic hydrocarbon degraders. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, BerlinGoogle Scholar
  17. McKew BA, Coulon F, Osborn AM, Timmis KN, McGenity TJ (2007) Determining the identity and roles of oil-metabolizing marine bacteria from the Thames estuary, UK. Environ Microbiol 9:165–176CrossRefGoogle Scholar
  18. Melcher RJ, Apitz SE, Hemmingsen BB (2002) Impact of irradiation and polycyclic aromatic hydrocarbon spiking on microbial populations in marine sediment for future aging and biodegradability studies. Appl Environ Microbiol 68:2858–2868CrossRefGoogle Scholar
  19. Menzie CA, Potocki BB, Santodonato J (1992) Exposure to carcinogenic PAH in the environment. Environ Sci Technol 26:1278–1284CrossRefGoogle Scholar
  20. Mesarch MB, Nakatsu CH, Nies L (2000) Development of catechol 2,3-dioxygenase-specific primers for monitoring bioremediation by competitive quantitative PCR. Appl Environ Microbiol 66:678–683CrossRefGoogle Scholar
  21. Oren A (2002) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biotechnol 28:56–63Google Scholar
  22. Pelz O, Tesar M, Wittich RM, Moore ER, Timmis KN, Abraham WR (1999) Towards elucidation of microbial community metabolic pathways: unravelling the network of carbon sharing in a pollutant-degrading bacterial consortium by immunocapture and isotopic ratio mass spectrometry. Environ Microbiol 1(2):167–174CrossRefGoogle Scholar
  23. Peng RH, Xiong AS, Xue Y, Fu XY, Gao F, Zhao W, Tian YS, Yao QH (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955CrossRefGoogle Scholar
  24. Pieper D, Reineke W (2000) Engineering bacteria for bioremediation. Curr Opin Biotechnol 11:262–270CrossRefGoogle Scholar
  25. Sánchez O, Gasol JM, Massana R, Mas J, Pedrós-Alió C (2007) Comparison of different denaturing gradient gel electrophoresis primer sets for the study of marine bacterioplankton communities. Appl Environ Microbiol 73:5962–5967CrossRefGoogle Scholar
  26. Sanderman H, Strominger JL (1972) Purification and properties of C55-isoprenoid alcohol phosphokinase from Staphylococcus aureus. J Biol Chem 247:5123–5131Google Scholar
  27. Seo JS, Keum YS, Hu Y, Li QX (2009) Bacterial degradation of aromatic compounds. Int J Environ Res Public Health 6:278–309CrossRefGoogle Scholar
  28. Sutherland JB, Rafii F, Khan AA, Cerniglia CE (1995) Mechanisms of polycyclic aromatic hydrocarbon degradation. In: Young LY, Cerniglia CE (eds) Microbial transformation and degradation of toxic organic chemicals. Wiley-Liss, New York, pp 269–306Google Scholar
  29. Tapilatu YH, Grossi V, Acquaviva M, Militon C, Bertrand JC, Cuny P (2010) Isolation of hydrocarbon-degrading extremely halophilic archaea from an uncontaminated hypersaline pond (Camargue, France). Extremophiles 14:225–231CrossRefGoogle Scholar
  30. Whitehouse BG (1984) The effects of temperature and salinity on the aqueous solubility of polynuclear aromatic hydrocarbons. Mar Chem 14:319–332CrossRefGoogle Scholar
  31. Zhang XX, Cheng SP, Zhu CJ, Sun SL (2006) Microbial PAH-degradation in soil: degradation pathways and contributing factors. Pedosphere 16:555–565CrossRefGoogle Scholar
  32. Zhao B, Wang H, Mao X, Li R (2009) Biodegradation of phenanthrene by a halophilic bacterial consortium under aerobic conditions. Curr Microbiol 58:205–210CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Seyed Mohammad Mehdi Dastgheib
    • 1
  • Mohammad Ali Amoozegar
    • 2
  • Khosro Khajeh
    • 3
  • Mahmoud Shavandi
    • 4
  • Antonio Ventosa
    • 5
  1. 1.Department of Biotechnology, College of ScienceUniversity of TehranTehranIran
  2. 2.Extremophile Laboratory, Department of Microbiology, School of Biology, College of ScienceUniversity of TehranTehranIran
  3. 3.Department of Biochemistry, Faculty of Biological ScienceTarbiat Modares UniversityTehranIran
  4. 4.Biotechnology Research CenterResearch Institute of Petroleum IndustriesTehranIran
  5. 5.Department of Microbiology and Parasitology, Faculty of PharmacyUniversity of SevillaSevilleSpain

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