Skip to main content
Log in

Biodegradation of Various Aromatic Compounds by Enriched Bacterial Cultures: Part A–Monocyclic and Polycyclic Aromatic Hydrocarbons

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Present study focused on the screening of bacterial consortium for biodegradation of monocyclic aromatic hydrocarbon (MAH) and polycyclic aromatic hydrocarbons (PAHs). Target compounds in the present study were naphthalene, acenaphthene, phenanthrene (PAHs), and benzene (MAH). Microbial consortia enriched with the above target compounds were used in screening experiments. Naphthalene-enriched consortium was found to be the most efficient consortium, based on its substrate degradation rate and its ability to degrade other aromatic pollutants with significantly high efficiency. Substrate degradation rate with naphthalene-enriched culture followed the order benzene > naphthalene > acenaphthene > phenanthrene. Chryseobacterium and Rhodobacter were discerned as the predominant species in naphthalene-enriched culture. They are closely associated to the type strain Chryseobacterium arthrosphaerae and Rhodobacter maris, respectively. Single substrate biodegradation studies with naphthalene (PAH) and benzene (MAH) were carried out using naphthalene-enriched microbial consortium (NAPH). Phenol and 2-hydroxybenzaldehyde were identified as the predominant intermediates during benzene and naphthalene degradation, respectively. Biodegradation of toluene, ethyl benzene, xylene, phenol, and indole by NAPH was also investigated. Monod inhibition model was able to simulate biodegradation kinetics for benzene, whereas multiple substrate biodegradation model was able to simulate biodegradation kinetics for naphthalene.

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

  1. Wang, Y., Yan, G., Wang, Q., Chen, C., Li, M., & Guo, S. (2015). Refining wastewater treatment using EGSB-BAF system. Desalination and Water Treatment, 53(10), 2808–2815.

    Article  CAS  Google Scholar 

  2. EPA, U. S. (2000). Superfund Sites. Washington, D.C.: US Environmental Protection Agency.

    Google Scholar 

  3. Juhasz, A. L., & Naidu, R. (2000). Bioremediation of high-molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. International Biodeterioration and Biodegradation, 45, 57–88.

    Article  CAS  Google Scholar 

  4. Mueller, J., Lantz, S., Ross, D., Colvin, R., Middaugh, D., & Pritchard, P. (1993). Strategy using bioreactors and specially selected microorganisms for bioremediation of groundwater contaminated with creosote and pentachlorophenol. Environmental Science & Technology, 27, 691–698.

    Article  CAS  Google Scholar 

  5. Das, K., & Mukherjee, A. K. (2007). Crude petroleum-oil biodegradation efficiency of Bacillus subtilis and Pseudomonas aeruginosa strains isolated from a petroleum-oil contaminated soil from North-East India. Bioresource Technology, 98(7), 1339–45.

    Article  CAS  Google Scholar 

  6. Woo, O. T., Chung, W. K., Wong, K. H., Chow, A. T., & Wong, P. K. (2009). Photocatalytic oxidation of polycyclic aromatic hydrocarbons: intermediates identification and toxicity testing. Journal of Hazardous Materials, 168, 1192–9.

    Article  CAS  Google Scholar 

  7. Muff, J., & Søgaard, E. (2010). Electrochemical degradation of PAH compounds in process water: a kinetic study on model solutions and a proof of concept study on runoff water from harbour sediment purification. Water Science and Technology, 61, 2043–51.

    Article  CAS  Google Scholar 

  8. Vidal, C. B., Barros, A. L., Moura, C. P., De Lima, A. C. A., Dias, F. S., Vasconcellos, L. C. G., Fechine, P., & Nascimento, R. F. (2011). Adsorption of polycyclic aromatic hydrocarbons from aqueous solutions by modified periodic mesoporous organo silica. Journal of Colloid and Interface Science, 357(2), 466–473.

    Article  CAS  Google Scholar 

  9. Desai, A. M., Autenrieth, R. L., Dimeitriou-Christidis, P., & McDonald, T. J. (2008). Biodegradation kinetics of select polycyclic aromatic hydrocarbon (PAH) mixtures by Sphingomonas paucimobilis EPA505. Biodegradation, 19, 223–233.

    Article  CAS  Google Scholar 

  10. Jegan, J., Vijayaraghavan, K., Senthilkumar, R., & Velan, M. (2010). Naphthalene degradation kinetics of Micrococcus sp., isolated from activated sludge. Clean: Soil, Air, Water, 38, 837–842.

    CAS  Google Scholar 

  11. Xu, P., Ma, W., Han, H., Hou, B., & Jia, S. (2014). Characterization of naphthalene degradation by Streptomyces sp. QWE-5 isolated from active sludge. Water Science and Technology, 70(6), 1129–34.

    Article  CAS  Google Scholar 

  12. Lin, C., Gan, L., & Chen, Z. (2010). Biodegradation of naphthalene by strain Bacillus fusiformis (BFN). J Hazardous Materials, 182(1-3), 771–777.

    Article  CAS  Google Scholar 

  13. You, Y., Shim, J., Cho, C.-H., Ryu, M.-H., Shea, P. J., Kamala-Kannan, S., Chae, J. C., & Oh, B. T. (2013). Biodegradation of BTEX mixture by Pseudomonas putida YNS1 isolated from oil- contaminated soil. Journal of Basic Microbiology, 53(2013), 469–75.

    Article  CAS  Google Scholar 

  14. Chang, Y.-I., Cheng, H.-P., Lai, S.-H., & Ning, H. (2014). Biodegradation of naphthalene in the oil re-finery wastewater by enriched activated sludge. International Biodeterioration & Biodegradation, 86(Part C), 272–277.

    Article  CAS  Google Scholar 

  15. Yuan, S., Wei, S., & Chang, B. (2000). Biodegradation of polycyclic aromatic hydrocarbons by a mixed culture. Chemosphere, 41, 1463–1468.

    Article  CAS  Google Scholar 

  16. Huang, Y., & Li, L. (2014). Biodegradation characteristics of naphthalene and benzene, toluene, ethyl benzene, and xylene (BTEX) by bacteria enriched from activated sludge. Water Environment Research, 86, 277–284.

    Article  CAS  Google Scholar 

  17. Zhang, L., Zhang, C., Cheng, Z., Yao, Y., & Chen, J. (2013). Biodegradation of benzene, toluene, ethylbenzene, and o-xylene by the bacterium Mycobacterium cosmeticum byf-4. Chemosphere, 90, 1340–1347.

    Article  CAS  Google Scholar 

  18. Baboshin, M., Akimov, V., Baskunov, B., Born, T. L., Khan, S. U., & Golovleva, L. (2008). Conversion of polycyclic aromatic hydrocarbons by Sphingomonas sp. VKM B-2434. Biodegradation, 19, 567–576.

    Article  CAS  Google Scholar 

  19. Jalilnejad, E., & Vahabzadeh, F. (2013). Models for the biodegradation kinetics of naphthalene by Ralstonia eutropha. Polycyclic Aromatic Compounds, 33, 451–466.

    Article  CAS  Google Scholar 

  20. Lin, C. W., & Cheng, Y. W. (2007). Biodegradation kinetics of benzene, methyl tert-butyl ether, and toluene as a substrate under various substrate concentrations. Journal of Chemical Technology and Biotechnology, 82, 51–57.

    Article  CAS  Google Scholar 

  21. Priya, V. S., & Philip, L. (2013). Biodegradation of dichloromethane along with other VOCs from pharmaceutical wastewater. Applied Biochemistry and Biotechnology, 169, 1197–1218.

    Article  CAS  Google Scholar 

  22. Datta, A., Philip, L., & Murty, B. S. (2014). Modeling the biodegradation kinetics of aromatic and aliphatic volatile pollutant mixture in liquid phase. Chemical Engineering Journal, 241, 288–300.

    Article  CAS  Google Scholar 

  23. Bauer, J. E., & Capone, D. G. (1988). Effects of co-occurring aromatic hydrocarbons on degradation of individual polycyclic aromatic hydrocarbons in marine sediment slurries. Applied and Environmental Microbiology, 54(7), 1649–1655.

    CAS  Google Scholar 

  24. Kelley, I., & Cerniglia, C. E. (1995). Degradation of a mixture of high-molecular-weight polycyclic aromatic hydrocarbons by a Mycobacterium strain PYR-1. Journal of Soil Contamination, 4, 44–91.

    Google Scholar 

  25. Leblond, J. D., Schultz, T. W., & Sayler, G. S. (2001). Observations on the preferential biodegradation of selected components of polyaromatic hydrocarbon mixtures. Chemosphere, 42, 333–343.

    Article  CAS  Google Scholar 

  26. Abu Hamed, T., Bayaktar, E., Mehmetoglu, T., & Mehmetoglu, U. (2003). Substrate interactions during the biodegradation of benzene, toluene and phenol mixtures. Process Biochemistry, 39, 27–35.

    Article  Google Scholar 

  27. Abuhamed, T., Bayraktar, E., Mehmetoglu, T., & Mehmetoglu, U. (2004). Kinetics model for growth of Pseudomonas putida F1 during benzene, toluene and phenol biodegradation. Process Biochemistry, 39, 983–8.

    Article  CAS  Google Scholar 

  28. Chang, B. V., Wu, W. B., & Yuan, S. Y. (1997). Biodegradation of benzene, toluene, and other aromatic compounds by Pseudomonas sp. D8. Chemosphere, 35, 2807–2815.

    Article  CAS  Google Scholar 

  29. Trigueros, D. E. G., Modenes, A. N., & Ravagnani, M. A. S. S. (2010). Biodegradation kinetics of benzene and toluene as single and mixed substrate: estimation of biokinetics parameters by applying particle swarm optimization. Latin American Applied Research, 40, 219–226.

    CAS  Google Scholar 

  30. Tao, Y., Fishman, A., Bentley, W., & Wood, T. (2004). Oxidation of benzene to phenol, catechol, and 1, 2, 3-trihydroxybenzene by toluene 4-monooxygenase of Pseudomonas mendocina KR-1 and toluene 3-monooxygenase of Ralstoniapickettii PKO1. Applied and Environmental Microbiology, 70, 3814–3820.

    Article  CAS  Google Scholar 

  31. Kobetičová, K., Simek, Z., Brezovský, J., & Hofman, J. (2011). Toxic effects of nine polycyclic aromatic compounds on Enchytraeus crypticus in artificial soil in relation to their properties. Ecotoxicology and Environmental Safety, 74(6), 1727–33.

    Article  Google Scholar 

  32. Habe, H., & Omori, T. (2003). Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Bioscience, Biotechnology, and Biochemistry, 67, 225–243.

    Article  CAS  Google Scholar 

  33. Pumphrey, G. M., & Madsen, E. L. (2007). Naphthalene metabolism and growth inhibition by naphthalene in Polaromonas naphthalenivorans strain CJ2. Microbiology, 153, 3730–3738.

    Article  CAS  Google Scholar 

  34. Sharma, N. K., Philip, L., & Bhallamudi, S. M. (2012). Aerobic degradation of phenolics and aromatic hydrocarbons in presence of cyanide. Bioresource Technology, 121, 263–273.

    Article  CAS  Google Scholar 

  35. Ramos, J. L., Duque, E., Gallegos, M. T., Godoy, P., Ramos-Gonzalez, M. I., Rojas, A., Teran, W., & Segura, A. (2002). Mechanisms of solvent tolerance in gram-negative bacteria. Annual Review of Microbiology, 56, 743–768.

    Article  CAS  Google Scholar 

  36. Owsianiak, M., Szulc, A., Chrzanowski, L., Cyplik, P., Bogacki, M., Olejnik Schmidt, A. K., & Heipieper, H. J. (2009). Biodegradation and surfactant-mediated biodegradation of diesel fuel by 218 microbial consortia are not correlated to cell surface hydrophobicity. Applied Microbiology and Biotechnology, 84, 545–553.

    Article  CAS  Google Scholar 

  37. Fahy, A., McGenity, T. J., Timmis, K. N., & Ball, A. S. (2006). Heterogeneous aerobic benzene-degrading communities in oxygen-depleted groundwaters. FEMS Microbiology Ecology, 58, 260–270.

    Article  CAS  Google Scholar 

  38. Maliyekkal, S. M., Reneb, E. R., Philip, L., & Swaminathan, T. (2004). Performance of BTX degraders under substrate versatility conditions. Journal of Hazardous Materials, 109, 201–211.

    Article  CAS  Google Scholar 

  39. Kim, D. J., Choi, J. W., Choi, N. C., Mahendran, B., & Lee, C. E. (2005). Modeling of growth kinetics for Pseudomonas sp during benzene degradation. Applied Microbiology and Biotechnology, 69, 456–462.

    Article  CAS  Google Scholar 

  40. Legates, D. R., & McCabe, G. J. (1999). Evaluating the use of” goodness-of-fit” measures in hydrologic and hydro climatic model validation. Water Resources Research, 35(1), 233–241.

    Article  Google Scholar 

Download references

Compliance with Ethical Standards

Authors are declaring that there is no potential conflict of interest involved and this work is in compliance with ethical standards.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ligy Philip.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig S1

Substrate degradation profile during the initial phase of acclimatization. Concentration of target pollutants increased in stepwise manner (DOCX 94 kb)

Fig S2

Substrate degradation and bacterial growth kinetics during the biodegradation of various PAHs and benzene with different enriched cultures (initial pollutant concentration = 50 mg/L) (DOCX 439 kb)

Fig S3

Specific (mg/g/h) and maximum degradation rate (mg/h) for various PAHs and benzene with different enriched cultures (DOCX 182 kb)

Fig S4

Acetone degradation profile during the time course degradation of various PAHs: a naphthalene, b scenaphthene, and c phenanthrene with different enriched cultures (DOCX 288 kb)

Fig S5

TOC removal pattern during the biodegradation of various PAHs and benzene with different enriched cultures a naphthalene, b acenaphthene, c phenanthrene, d benzene (DOCX 225 kb)

Fig S6

Fragmentation pattern of different intermediates identified during biodegradation of benzene and naphthalene (DOCX 86 kb)

Fig S7

Experimental and model predicted (generalized model) results for acetone degradation during the biodegradation of different initial concentration of naphthalene (DOCX 97 kb)

Fig S8

Biodegradation of different substrates by naphthalene enriched culture for different initial concentrations (DOCX 81 kb)

Fig S9

Neighbor-joining phylogenetic tree based on 16S rRNA gene sequences showing the relationship between isolated strain NAP1 with closely related members in GenBank during BLAST analysis. Bootstrap percentages (based on 1000 replicates) are given at the branching points. NCBI accession numbers for the sequences used in the analysis are given in parentheses. Bar 0.005 nucleotide substitutions per site (DOCX 37 kb)

Fig S10

Neighbor-joining phylogenetic tree based on 16S rRNA gene sequences showing the relationship between isolated strain NAP2 with closely related members in GenBank during BLAST analysis. Bootstrap percentages (based on 1000 replicates) are given at the branching points. NCBI accession numbers for the sequences used in the analysis are given in parentheses. Bar 0.001 nucleotide substitutions per site (DOCX 33 kb)

Fig S11

Neighbor-joining phylogenetic tree, based on 16S rRNA gene sequences, showing the relationship between isolated strain NAP1 and previously known species of the genus Chryseobacterium. Bootstrap percentages (based on 1000 replicates) are given at the branching points. NCBI accession numbers for the sequences used in the analysis are given in parentheses. Bar 0.005 nucleotide substitutions per site (DOCX 19 kb)

Fig S12

Neighbor-joining phylogenetic tree, based on 16S rRNA gene sequences, showing the relationship between isolated strain NAP2 and previously known species of the genus Rhodobacter. Bootstrap percentages (based on 1000 replicates) are given at the branching points. NCBI accession numbers for the sequences used in the analysis are given in parentheses. Bar 0.005 nucleotide substitutions per site (DOCX 19 kb)

Table S1

Various kinetic models and corresponding governing Equations (DOCX 30 kb)

Table S2

Mass spectral details of characteristic fragment ion peaks of metabolites identified during the degradation of benzene and naphthalene (DOCX 15 kb)

Table S3

Comparison of biokinetic parameters obtained from Monod inhibition model with Haldane and Monod model for benzene (DOCX 15 kb)

Table S4

Values of growth kinetic parameters reported in the literature evaluated from different biokinetic models (DOCX 17 kb)

Table S5

Modified coefficients of efficiency (E) obtained while evaluating performance of Monod inhibition model for benzene (DOCX 16 kb)

Table S6

Modified coefficients of efficiency (E) obtained while evaluating performance of generalized model for naphthalene (DOCX 16 kb)

Table S7

Comparison of modified coefficients of efficiency (E) obtained while evaluating performance of Monod inhibition Model with Haldane and Monod model for benzene degradation (DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oberoi, A.S., Philip, L. & Bhallamudi, S.M. Biodegradation of Various Aromatic Compounds by Enriched Bacterial Cultures: Part A–Monocyclic and Polycyclic Aromatic Hydrocarbons. Appl Biochem Biotechnol 176, 1870–1888 (2015). https://doi.org/10.1007/s12010-015-1684-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-015-1684-1

Keywords

Navigation