Skip to main content
Log in

Biodegradation of polycyclic aromatic hydrocarbons by a halophilic microbial consortium

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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 76:324–330

    Google Scholar 

  • Arulazhagan P, Vasudevan N, Yeom IT (2010) Biodegradation of polycyclic aromatic hydrocarbon by bacterial consortium isolated from marine environment. Int J Environ Sci Tech 7:639–652

    CAS  Google Scholar 

  • Cerniglia CE (1993) Biodegradation of polycyclic aromatic hydrocarbons. Curr Opin Biotechnol 3:331–338

    Article  Google Scholar 

  • Dastgheib SM, Amoozegar MA, Khajeh K, Ventosa A (2011) A halotolerant Alcanivorax sp. strain with potential application in saline soil remediation. Appl Microbiol Biotechnol 90:305–312

    Article  CAS  Google Scholar 

  • García MT, Ventosa A, Mellado E (2005) Catabolic versatility of aromatic compound-degrading halophilic bacteria. FEMS Microbiol Ecol 1:97–109

    Article  Google Scholar 

  • Haritash AK, Kaushik CPJ (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15

    Article  CAS  Google Scholar 

  • Hart DJ, Vreeland RH (1988) Changes in the hydrophobic–hydrophilic cell surface character of Halomonas elongata in response to NaCl. J Bacteriol 170:132–135

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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 68:5625–5633

    Article  CAS  Google Scholar 

  • Le Borgne S, Paniagua D, Vasquez-Duhalt R (2008) Biodegradation of organic pollutants by halophilic bacteria and archaea. J Mol Microbiol Biotechnol 15:74–92

    Article  Google Scholar 

  • 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 16:57–65

    Article  CAS  Google Scholar 

  • 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 55:1181–1186

    Article  CAS  Google Scholar 

  • 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 153:2104–2115

    Article  CAS  Google Scholar 

  • Margesin R, Schinner F (2001) Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 5:73–78

    Article  CAS  Google Scholar 

  • 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 53:1383–1387

    Article  Google Scholar 

  • McGenity TJ, Gramain A (2010) Cultivation of halophilic hydrocarbon degraders. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin

    Google Scholar 

  • 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 9:165–176

    Article  CAS  Google Scholar 

  • 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 68:2858–2868

    Article  CAS  Google Scholar 

  • Menzie CA, Potocki BB, Santodonato J (1992) Exposure to carcinogenic PAH in the environment. Environ Sci Technol 26:1278–1284

    Article  CAS  Google Scholar 

  • 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 66:678–683

    Article  CAS  Google Scholar 

  • Oren A (2002) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biotechnol 28:56–63

    CAS  Google Scholar 

  • 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):167–174

    Article  CAS  Google Scholar 

  • 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 32:927–955

    Article  CAS  Google Scholar 

  • Pieper D, Reineke W (2000) Engineering bacteria for bioremediation. Curr Opin Biotechnol 11:262–270

    Article  CAS  Google Scholar 

  • 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 73:5962–5967

    Article  Google Scholar 

  • Sanderman H, Strominger JL (1972) Purification and properties of C55-isoprenoid alcohol phosphokinase from Staphylococcus aureus. J Biol Chem 247:5123–5131

    Google Scholar 

  • Seo JS, Keum YS, Hu Y, Li QX (2009) Bacterial degradation of aromatic compounds. Int J Environ Res Public Health 6:278–309

    Article  CAS  Google Scholar 

  • 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 269–306

    Google Scholar 

  • 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 14:225–231

    Article  CAS  Google Scholar 

  • Whitehouse BG (1984) The effects of temperature and salinity on the aqueous solubility of polynuclear aromatic hydrocarbons. Mar Chem 14:319–332

    Article  CAS  Google Scholar 

  • Zhang XX, Cheng SP, Zhu CJ, Sun SL (2006) Microbial PAH-degradation in soil: degradation pathways and contributing factors. Pedosphere 16:555–565

    Article  CAS  Google Scholar 

  • Zhao B, Wang H, Mao X, Li R (2009) Biodegradation of phenanthrene by a halophilic bacterial consortium under aerobic conditions. Curr Microbiol 58:205–210

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Dr. Massoud Houshmand and Elham Khalili (Special Medical Center, Iran) for providing DGGE facilities and for their useful comments. We would also like to thank Dr. Majid Zeinali and Parviz Soleimani (Iranian Research Institute of Petroleum Industries) for their helpful remarks on GC–MS analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mohammad Ali Amoozegar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dastgheib, S.M.M., Amoozegar, M.A., Khajeh, K. et al. Biodegradation of polycyclic aromatic hydrocarbons by a halophilic microbial consortium. Appl Microbiol Biotechnol 95, 789–798 (2012). https://doi.org/10.1007/s00253-011-3706-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-011-3706-4

Keywords

Navigation