Anaerobic phenanthrene biodegradation with four kinds of electron acceptors enriched from the same mixed inoculum and exploration of metabolic pathways

Abstract

Polycyclic aromatic hydrocarbons (PAHs) are widespread and persistent contaminants worldwide, especially in environments devoid of molecular oxygen. For lack of molecular oxygen, researchers enhanced anaerobic zones PAHs biodegradation by adding sulfate, bicarbonate, nitrate, and iron. However, microbial community reports of them were limited, and information of metabolites was poor except two-ring PAH, naphthalene. Here, we reported on four phenanthrene-degrading enrichment cultures with sulfate, bicarbonate, nitrate, and iron as electron acceptors from the same initial inoculum. The high-to-low order of the anaerobic phenanthrene biodegradation rate was the nitrate-reducing conditions>sulfate-reducing conditions>methanogenic conditions>iron-reducing conditions. The dominant bacteria populations were Desulfobacteraceae, Anaerolinaceae, and Thermodesulfobiaceae under sulfate-reducing conditions; Moraxellaceae, Clostridiaceae, and Comamonadaceae under methanogenic conditions; Rhodobacteraceae, Planococcaceae, and Xanthomonadaceae under nitrate-reducing conditions; and Geobacteraceae, Carnobacteriaceae, and Anaerolinaceae under iron-reducing conditions, respectively. Principal component analysis (PCA) indicated that bacteria populations of longtime enriched cultures with four electron acceptors all obtained significant changes from original inoculum, and bacterial communities were similar under nitrate-reducing and iron-reducing conditions. Archaea accounted for a high percentage under iron-reducing and methanogenic conditions, and Methanosarcinaceae and Methanobacteriaceae, as well as Methanobacteriaceae, were the dominant archaea populations under iron-reducing and methanogenic conditions. The key steps of phenanthrene biodegradation under four reducing conditions were carboxylation, further ring system reduction, and ring cleavage.

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

References

  1. Amann R, Fuchs B M (2008). Single-cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nature Reviews. Microbiology, 6(5): 339–348

    CAS  Google Scholar 

  2. Annweiler E, Michaelis W, Meckenstock R U (2002). Identical ring cleavage products during anaerobic degradation of naphthalene, 2-methylnaphthalene, and tetralin indicate a new metabolic pathway. Applied and Environmental Microbiology, 68(2): 852–858

    CAS  Article  Google Scholar 

  3. APHA (1998). Standard Methods for the Examination of Water and Wastewater. Baltimore MD: American Public Health Association

    Google Scholar 

  4. Bauer J E, Capone D G (1985). Degradation and mineralization of the polycyclic aromatic hydrocarbons anthracene and naphthalene in intertidal marine sediments. Applied and Environmental Microbiology, 50(1): 81–90

    CAS  Article  Google Scholar 

  5. 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  Article  Google Scholar 

  6. Chang B V, Chang S W, Yuan S Y (2003). Anaerobic degradation of polycyclic aromatic hydrocarbons in sludge. Advances in Environmental Research, 7(3): 623–628

    CAS  Article  Google Scholar 

  7. Coates J D, Anderson R T, Woodward J C, Phillips E J P, Lovley D R (1996). Anaerobic hydrocarbon degradation in petroleum-contaminated harbor sediments under sulfate-reducing and artificially imposed iron-reducing conditions. Environmental Science & Technology, 30(9): 2784–2789

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  9. 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

    Article  CAS  Google Scholar 

  10. Feng Z J, Zhu L Z (2018). Sorption of phenanthrene to biochar modified by base. Frontiers of Environmental Science & Engineering, 12 (2): 1

    CAS  Article  Google Scholar 

  11. 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  Article  Google Scholar 

  12. 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  Article  Google Scholar 

  13. Hambrick G A, Delaune R D, Patrick W H (1980). Effect of estuarine sediment pH and oxidation-reduction potential on microbial hydrocarbon degradation. Applied and Environmental Microbiology, 40(2): 365–369

    CAS  Article  Google Scholar 

  14. Himmelberg A M, Brüls T, Farmani Z, Weyrauch P, Barthel G, Schrader W, Meckenstock R U (2018). Anaerobic degradation of phenan-threne by a sulfate-reducing enrichment culture. Environmental Microbiology, 20(10): 3589–3600

    CAS  Article  Google Scholar 

  15. Kleemann R, Meckenstock R U (2011). Anaerobic naphthalene degradation by Gram-positive, iron-reducing bacteria. FEMS Microbiology Ecology, 78(3): 488–496

    CAS  Article  Google Scholar 

  16. 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 Desulfobac-teraceae from various anoxic aquifers. FEMS Microbiology Ecology, 91(3): 1–12: fiv006

    Article  CAS  Google Scholar 

  17. Langenhoff A A M, Zehnder A J B, Schraa G (1996). Behaviour of toluene, benzene and naphthalene under anaerobic conditions in sediment columns. Biodegradation, 7(3): 267–274

    CAS  Article  Google Scholar 

  18. Li J, Luo C, Song M, Dai Q, Jiang L, Zhang D, Zhang G (2017). Biodegradation of phenanthrene in polycyclic aromatic hydrocarbon-contaminated wastewater revealed by coupling cultivation-dependent and-independent approaches. Environmental Science & Technology, 51(6): 3391–3401

    CAS  Article  Google Scholar 

  19. Luo F, Gitiafroz R, Devine C E, Gong Y, Hug L A, Raskin L, Edwards E A (2014). Metatranscriptome of an anaerobic benzene-degrading, nitrate-reducing enrichment culture reveals involvement of carbox-ylation in benzene ring activation. Applied and Environmental Microbiology, 80(14): 4095–4107

    Article  CAS  Google Scholar 

  20. 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  Article  Google Scholar 

  21. Martirani-Von Abercron S M, Pacheco D, Benito-Santano P, Marín P, Marqués S (2016). Polycyclic aromatic hydrocarbon-induced changes in bacterial community structure under anoxic nitrate reducing conditions. Frontiers in Microbiology, 7: 1–16

    Article  Google Scholar 

  22. Meckenstock R U, Annweiler E, Michaelis W, Richnow H H, Schink B (2000). Anaerobic naphthalene degradation by a sulfate-reducing enrichment culture. Applied and Environmental Microbiology, 66(7): 2743–2747

    CAS  Article  Google Scholar 

  23. Mihelcic J R, Luthy R G (1988). Degradation of polycyclic aromatic hydrocarbon compounds under various redox conditions in soil-water systems. Applied and Environmental Microbiology, 54(5): 1182–1187

    CAS  Article  Google Scholar 

  24. Morris B E, Gissibl A, Kümmel S, Richnow H H, Boll M (2014). A PCR-based assay for the detection of anaerobic naphthalene degradation. FEMS Microbiology Letters, 354(1): 55–59

    CAS  Article  Google Scholar 

  25. Mouttaki H, Johannes J, Meckenstock R U (2012). Identification of naphthalene carboxylase as a prototype for the anaerobic activation of non-substituted aromatic hydrocarbons. Environmental Microbiology, 14(10): 2770–2774

    CAS  Article  Google Scholar 

  26. Müller J B, Ramos D T, Larose C, Fernandes M, Lazzarin H S, Vogel T M, Corseuil H X (2017). Combined iron and sulfate reduction biostimulation as a novel approach to enhance BTEX and PAH source-zone biodegradation in biodiesel blend-contaminated ground-water. Journal of Hazardous Materials, 326: 229–236

    Article  CAS  Google Scholar 

  27. 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  Article  Google Scholar 

  28. Obi C C, Adebusoye S A, Amund O O, Ugoji E O, Ilori M O, Hedman C J, Hickey W J (2017). Structural dynamics of microbial communities in polycyclic aromatic hydrocarbon-contaminated tropical estuarine sediments undergoing simulated aerobic biotreatment. Applied Microbiology and Biotechnology, 101(10): 4299–4314

    CAS  Article  Google Scholar 

  29. Rockne K J, Strand S E (2001). Anaerobic biodegradation of naphthalene, phenanthrene, and biphenyl by a denitrifying enrichment culture. Water Research, 35(1): 291–299

    CAS  Article  Google Scholar 

  30. 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  Article  Google Scholar 

  31. Sharak Genthner B R, Townsend G T, Lantz S E, Mueller J G (1997). Persistence of polycyclic aromatic hydrocarbon components of creosote under anaerobic enrichment conditions. Archives of Environmental Contamination and Toxicology, 32(1): 99–105

    CAS  Article  Google Scholar 

  32. Smith M R (1990). The biodegradation of aromatic hydrocarbons by bacteria. Biodegradation, 1(2-3): 191–206

    CAS  Article  Google Scholar 

  33. Tor J M, Lovley D R (2001). Anaerobic degradation of aromatic compounds coupled to Fe(III) reduction by Ferroglobus placidus. Environmental Microbiology, 3(4): 281–287

    CAS  Article  Google Scholar 

  34. Trably E, Patureau D, Delgenes J P (2003). Enhancement of polycyclic aromatic hydrocarbons removal during anaerobic treatment of urban sludge. Water Science and Technology, 48(4): 53–60

    CAS  Article  Google Scholar 

  35. Weyrauch P, Zaytsev A V, Stephan S, Kocks L, Schmitz O J, Golding B T, Meckenstock R U (2017). Conversion of cis-2-carboxycyclohex-ylacetyl-CoA in the downstream pathway of anaerobic naphthalene degradation. Environmental Microbiology, 19(7): 2819–2830

    CAS  Article  Google Scholar 

  36. Xu M, He Z, Zhang Q, Liu J, Guo J, Sun G, Zhou J (2015). Responses of aromatic-degrading microbial communities to elevated nitrate in sediments. Environmental Science & Technology, 49(20): 12422–12431

    CAS  Article  Google Scholar 

  37. 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  Article  Google Scholar 

  38. Ye Q H, Wang C Y, Wang Y, Wang H (2018). Characterization of a phenanthrene-degrading methanogenic community. Frontiers of Environmental Science & Engineering, 12 (5): 4

    Article  CAS  Google Scholar 

  39. 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  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  41. Zhang X, Sullivan E R, Young L Y (2000). Evidence for aromatic ring reduction in the biodegradation pathway of carboxylated naphthalene by a sulfate reducing consortium. Biodegradation, 11(2/3): 117–124

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This study was funded by the National Natural Science Foundations of China (Grant Nos. 41573065 and 41773082), the Key Project of Natural Science Foundation of China (No. 21337001) and the Mega-projects of Science Research for Water Environment Improvement (No. 2017ZX07202002).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Hui Wang.

Additional information

Highlights

• Anaerobic phenanthrene biodegradation enriched process was described in detail.

• The enriched bacterial communities were characterized under four redox conditions.

• The enriched archaeal communities were stated under high percentage conditions.

• Relatively intact pathways of anaerobic phenanthrene biodegradation were proposed.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhang, Z., Wang, C., He, J. et al. Anaerobic phenanthrene biodegradation with four kinds of electron acceptors enriched from the same mixed inoculum and exploration of metabolic pathways. Front. Environ. Sci. Eng. 13, 80 (2019). https://doi.org/10.1007/s11783-019-1164-x

Download citation

Keywords

  • Phenanthrene
  • Anaerobic biodegradation
  • Bacterial populations
  • Archaea populations
  • Metabolic pathway