Skip to main content
Log in

Characterization of a phenanthrene-degrading methanogenic community

  • Research Article
  • Published:
Frontiers of Environmental Science & Engineering Aims and scope Submit manuscript

Abstract

Polycyclic aromatic hydrocarbons (PAHs) often occur in oil-contaminated soil, coke wastewater and domestic sludge; however, associated PAH degraders in these environments are not clear. Here we evaluated phenanthrene degradation potential in the mixed samples of above environments, and obtained a methanogenic community with different microbial profile compared to those from sediments. Phenanthrene was efficiently degraded (1.26 mg/L/d) and nonstoichiometric amount of methane was produced simultaneously. 16S rRNA gene sequencing demonstrated that bacterial populations were mainly associated with Comamonadaceae Nocardiaceae and Thermodesulfobiaceae, and that methanogenic archaea groups were dominated by Methanobacterium and Methanothermobacter. Substances such as hexane, hexadecane, benzene and glucose showed the most positive effects on phenanthrene degradation. Substrate utilization tests indicated that this culture could not utilize other PAHs. These analyses could offer us some suggestions on the putative phenanthrene-degrading microbes in such environments, and might help us develop strategies for the removal of PAHs from contaminated soil and sludge.

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.

Similar content being viewed by others

References

  • Aislabie J, McLeod M, Fraser R (1998). Potential for biodegradation of hydrocarbons in soil from the Ross Dependency, Antarctica. Applied Microbiology and Biotechnology, 49(2): 210–214

    CAS  Google Scholar 

  • Bengtsson G, Zerhouni P (2003). Effects of carbon substrate enrichment and DOC concentration on biodegradation of PAHs in soil. Journal of Applied Microbiology, 94(4): 608–617

    CAS  Google Scholar 

  • Berdugo-Clavijo C, Dong X, Soh J, Sensen C W, Gieg L M (2012). Methanogenic biodegradation of two-ringed polycyclic aromatic hydrocarbons. FEMS Microbiology Ecology, 81(1): 124–133

    CAS  Google Scholar 

  • Canul-Chan M, Sánchez-González M, González-Burgos A, Zepeda A, Rojas-Herrera R (2017). Population structures shift during the biodegradation of crude and fuel oil by an indigenous consortium. International Journal of Environmental Science and Technology, 15(1): 1–16

    Google Scholar 

  • Chang B V, Chang I T, Yuan S Y (2008a). Anaerobic degradation of phenanthrene and pyrene in mangrove sediment. Bulletin of Environmental Contamination and Toxicology, 80(2): 145–149

    CAS  Google Scholar 

  • Chang B V, Chang S W, Yuan S Y. Anaerobic degradation of polycyclic aromatic hydrocarbons in sludge. Adv Environ Res, 2003, 7(3): 623–628

    CAS  Google Scholar 

  • Chang B V, Shiung L C, Yuan S Y. Anaerobic biodegradation of polycyclic aromatic hydrocarbon in soil. Chemosphere, 2002, 48: 717–724

    CAS  Google Scholar 

  • Chang M W, Holoman T P, Yi H (2008b). Molecular characterization of surfactant-driven microbial community changes in anaerobic phenanthrene-degrading cultures under methanogenic conditions. Biotechnology Letters, 30(9): 1595–1601

    CAS  Google Scholar 

  • Chang W, Um Y, Hoffman B, Pulliam Holoman T R (2005). Molecular characterization of polycyclic aromatic hydrocarbon (PAH)-degrading methanogenic communities. Biotechnology Progress, 21(3): 682–688

    CAS  Google Scholar 

  • Chang W, Um Y, Holoman T R (2006). Polycyclic aromatic hydrocarbon (PAH) degradation coupled to methanogenesis. Biotechnology Letters, 28(6): 425–430

    CAS  Google Scholar 

  • Chen S, Aitken M D (1999). Salicylate stimulates the degradation of high-molecular weight polycyclic aromatic hydrocarbons by Pseudomonas saccharophila P15. Environmental Science & Technology, 33(3): 435–439

    CAS  Google Scholar 

  • Davidova I A, Gieg L M, Duncan K E, Suflita J M (2007). Anaerobic phenanthrene mineralization by a carboxylating sulfate-reducing bacterial enrichment. ISME Journal, 1(5): 436–442

    CAS  Google Scholar 

  • Fang T, Pan R, Jiang J, He F, Wang H (2016). Effect of salinity on community structure and naphthalene dioxygenase gene diversity of a halophilic bacterial consortium. Frontiers of Environmental Science & Engineering, 10(6): 16

    Google Scholar 

  • Fuchedzhieva N, Karakashev D, Angelidaki I (2008). Anaerobic biodegradation of fluoranthene under methanogenic conditions in presence of surface-active compounds. Journal of Hazardous Materials, 153(1–2): 123–127

    CAS  Google Scholar 

  • Galushko A, Minz D, Schink B, Widdel F (1999). Anaerobic degradation of naphthalene by a pure culture of a novel type of marine sulphate-reducing bacterium. Environmental Microbiology, 1(5): 415–420

    CAS  Google Scholar 

  • Gómez R S G, Pandiyan T, Iris V E A, Luna-Pabello V, de Bazúa C D (2004). Spectroscopic determination of poly-aromatic compounds in petroleum contaminated soils. Water, Air, and Soil Pollution, 158(1): 137–151

    Google Scholar 

  • Goyal A K, Zylstra G J (1996). Molecular cloning of novel genes for polycyclic aromatic hydrocarbon degradation from Comamonas testosteroni GZ39. Applied and Environmental Microbiology, 62(1): 230–236

    CAS  Google Scholar 

  • Gray N D, Sherry A, Larter S R, Erdmann M, Leyris J, Liengen T, Beeder J, Head I M (2009). Biogenic methane production in formation waters from a large gas field in the North Sea. Extremophiles, 13(3): 511–519

    CAS  Google Scholar 

  • Haritash A K, Kaushik C P (2009). Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. Journal of Hazardous Materials, 169(1–3): 1–15

    CAS  Google Scholar 

  • Huang Y, Zhang J, Zhu L (2013). Evaluation of the application potential of bentonites in phenanthrene bioremediation by characterizing the biofilm community. Bioresource Technology, 134: 17–23

    CAS  Google Scholar 

  • Jiménez N, Viñas M, Bayona J M, Albaiges J, Solanas A M (2007). The Prestige oil spill: bacterial community dynamics during a field biostimulation assay. Applied Microbiology and Biotechnology, 77(4): 935–945

    Google Scholar 

  • Keith L H, Telliard W A (1979). Priority pollutants I—A perspective view. Environmental Science & Technology, 13(4): 416–423

    Google Scholar 

  • Kong X, Yu S, Xu S, Fang W, Liu J, Li H (2018). Effect of Fe0 addition on volatile fatty acids evolution on anaerobic digestion at high organic loading rates. Waste Management (New York, N.Y.), 71: 719–727

    CAS  Google Scholar 

  • Kryachko Y, Dong X, Sensen C W, Voordouw G (2012). Compositions of microbial communities associated with oil and water in a mesothermic oil field. Antonie van Leeuwenhoek, 101(3): 493–506

    Google Scholar 

  • Kümmel S, Herbst F A, Bahr A, Duarte M, Pieper D H, Jehmlich N, Seifert J, von Bergen M, Bombach P, Richnow H H, Vogt C (2015). Anaerobic naphthalene degradation by sulfate-reducing Desulfobacteraceae from various anoxic aquifers. FEMS Microbiology Ecology, 91(3): 1–13

    Google Scholar 

  • Li H, Chang J, Liu P, Fu L, Ding D, Lu Y (2015). Direct interspecies electron transfer accelerates syntrophic oxidation of butyrate in paddy soil enrichments. Environmental Microbiology, 17(5): 1533–1547

    Google Scholar 

  • Liang B, Wang L Y, Mbadinga S M, Liu J F, Yang S Z, Gu J D, Mu B Z (2015). Anaerolineaceae and Methanosaeta turned to be the dominant microorganisms in alkanes-dependent methanogenic culture after long-term of incubation. AMB Express, 5(1): 117

    Google Scholar 

  • Lladó S, Jiménez N, Viñas M, Solanas A M (2009). Microbial populations related to PAH biodegradation in an aged biostimulated creosote-contaminated soil. Biodegradation, 20(5): 593–601

    Google Scholar 

  • Luo J, Zhang J, Tan X, McDougald D, Zhuang G, Fane A G, Kjelleberg S, Cohen Y, Rice S A (2015). Characterization of the archaeal community fouling a membrane bioreactor. Journal of Environmental Sciences (China), 29: 115–123

    CAS  Google Scholar 

  • Musat F, Galushko A, Jacob J, Widdel F, Kube M, Reinhardt R, Wilkes H, Schink B, Rabus R (2009). Anaerobic degradation of naphthalene and 2-methylnaphthalene by strains of marine sulfate-reducing bacteria. Environmental Microbiology, 11(1): 209–219

    CAS  Google Scholar 

  • Pérez S, Guillamón M, Barceló D (2001). Quantitative analysis of polycyclic aromatic hydrocarbons in sewage sludge from wastewater treatment plants. Journal of Chromatography. A, 938(1–2): 57–65

    Google Scholar 

  • Pinyakong O, Tiangda K, Iwata K, Omori T (2012). Isolation of novel phenanthrene-degrading bacteria from seawater and the influence of its physical factors on the degradation of phenanthrene. Science Asia, 38(1): 36–43

    CAS  Google Scholar 

  • Safinowski M, Meckenstock R U (2006). Methylation is the initial reaction in anaerobic naphthalene degradation by a sulfate-reducing enrichment culture. Environmental Microbiology, 8(2): 347–352

    CAS  Google Scholar 

  • Sekiguchi Y, Kamagata Y, Syutsubo K, Ohashi A, Harada H, Nakamura K (1998). Phylogenetic diversity of mesophilic and thermophilic granular sludges determined by 16S rRNA gene analysis. Microbiology-Uk, 144(Pt 9): 2655–2665

    CAS  Google Scholar 

  • Sullivan E R, Zhang X, Phelps C, Young L Y (2001). Anaerobic mineralization of stable-isotope-labeled 2-methylnaphthalene. Applied and Environmental Microbiology, 67(9): 4353–4357

    CAS  Google Scholar 

  • Tøndervik A, Bruheim P, Berg L, Ellingsen T E, Kotlar H K, Valla S, Throne-Holst M (2012). Ralstonia sp. U2 naphthalene dioxygenase and Comamonas sp. JS765 nitrobenzene dioxygenase show differences in activity towards methylated naphthalenes. Journal of Bioscience and Bioengineering, 113(2): 173–178

    Google Scholar 

  • Wan R, Zhang S, Xie S (2012). Microbial community changes in aquifer sediment microcosm for anaerobic anthracene biodegradation under methanogenic condition. Journal of Environmental Sciences (China), 24(8): 1498–1503

    CAS  Google Scholar 

  • Yarza P, Yilmaz P, Pruesse E, Glöckner F O, Ludwig W, Schleifer K H, Whitman W B, Euzéby J, Amann R, Rosselló-Móra R (2014). Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nature Reviews. Microbiology, 12(9): 635–645

    CAS  Google Scholar 

  • Ye Q, Zhang Z, Huang Y, Fang T, Cui Q, He C, Wang H (2018). Enhancing electron transfer by magnetite during phenanthrene anaerobic methanogenic degradation. International Biodeterioration & Biodegradation, 129: 109–116

    CAS  Google Scholar 

  • Yin Q, Miao J, Li B, Wu G (2017). Enhancing electron transfer by ferroferric oxide during the anaerobic treatment of synthetic wastewater with mixed organic carbon. International Biodeterioration & Biodegradation, 119: 104–110

    CAS  Google Scholar 

  • Yuan S Y, Chang B V (2007). Anaerobic degradation of five polycyclic aromatic hydrocarbons from river sediment in Taiwan. Journal of Environmental Science and Health. Part. B, Pesticides, Food Contaminants, and Agricultural Wastes, 42(1): 63–69

    CAS  Google Scholar 

  • Zhang S, Wang Q, Xie S (2012a). Stable isotope probing identifies anthracene degraders under methanogenic conditions. Biodegradation, 23(2): 221–230

    Google Scholar 

  • Zhang S Y, Wang Q F, Xie S G (2012b). Molecular characterization of phenanthrene-degrading methanogenic communities in leachatecontaminated aquifer sediment. International Journal of Environmental Science and Technology, 9(4): 705–712

    CAS  Google Scholar 

  • Zhang X, Young L Y (1997). Carboxylation as an initial reaction in the anaerobic metabolism of naphthalene and phenanthrene by sulfidogenic consortia. Applied and Environmental Microbiology, 63(12): 4759–4764

    CAS  Google Scholar 

  • Zhou S, Xu J, Yang G, Zhuang L (2014). Methanogenesis affected by the co-occurrence of iron(III) oxides and humic substances. FEMS Microbiology Ecology, 88(1): 107–120

    CAS  Google Scholar 

  • Zhuang L, Tang J, Wang Y, Hu M, Zhou S (2015). Conductive iron oxide minerals accelerate syntrophic cooperation in methanogenic benzoate degradation. Journal of Hazardous Materials, 293: 37–45

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant Nos. 41573065 and 41773082), the Key Project of Natural Science Foundation of China (Grant No. 21337001) and the National Water Pollution Control and Treatment Science and Technology Major Project (Grant No. 2017ZX07202002).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hui Wang.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ye, Q., Liang, C., Wang, C. et al. Characterization of a phenanthrene-degrading methanogenic community. Front. Environ. Sci. Eng. 12, 4 (2018). https://doi.org/10.1007/s11783-018-1083-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11783-018-1083-2

Keywords

Navigation