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Biodegradation of Polycyclic Aromatic Hydrocarbons in Mangrove Sediments Under Different Strategies: Natural Attenuation, Biostimulation, and Bioaugmentation with Rhodococcus erythropolis T902.1

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Abstract

Polycyclic aromatic hydrocarbons (PAHs) are pollutants that occur in mangrove sediments. Their removal by bacteria often depends on specific characteristics as the number of benzene rings they possess and their solubility. Their removal also depends on environmental factors, such as pH, temperature, oxygen, and the ability of the endogenous or exogenous microflora to metabolize hydrocarbons. With the aim of treating mangrove sediments polluted by hydrocarbons in a biological way, a biodegradation experiment was conducted using mangrove sediments artificially contaminated with a mixture of four PAHs. The study used Rhodococcus erythropolis as an exogenous bacterial strain in order to assess the biodegradation of the PAH mixture by natural attenuation, biostimulation, bioaugmentation, and a combination of biostimulation and bioaugmentation. The results showed that the last three treatments were more efficient than natural attenuation. The biostimulation/bioaugmentation combination proved to be the most effective PAH degradation treatment.

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References

  • Arino, S., Marchal, R., & Vandecasteele, J. P. (1996). Involvement of a rhamnolipid-producing strain of Pseudomonas aeruginosa in the degradation of polycyclic aromatic hydrocarbons by a bacterial community. Journal of Applied Microbiology, 84, 769–776.

    Article  Google Scholar 

  • Baker, K. H. (1994). Bioremediation of surface and subsurface soils. In K. H. Baker & D. S. Herson (Eds.), Bioremediation (pp. 203–259). New York, USA: McGraw-Hill Inc.

    Google Scholar 

  • Balba, M. T., Al-Awadhi, N., & Al-Daher, R. (1998). Bioremediation of oil-contaminated soil: microbiological methods for feasibility assessment and field evaluation. Journal Microbiology Methods, 32, 155–164.

    Article  CAS  Google Scholar 

  • Banerjee, D. K., Fedorak, P. M., Hashimoto, A., Masliyah, J. H., Pickard, M. A., & Gray, M. R. (1995). Monitoring the biological treatment of anthracene-contaminated soil in a rotating-drum bioreactor. Applied Microbiology and Biotechnology, 43, 521–528.

    Article  CAS  Google Scholar 

  • Bell, K. S., Philp, J. C., Aw, D. W. J., & Christofi, N. (1998). The genus Rhodococcus. Journal Applied Microbiology, 85, 195–210.

    Article  CAS  Google Scholar 

  • Brito, E. M. S., Guyoneaud, R., Goñi-Urriza, M., Ranchou-Peyruse, A., Verbaere, A., Crapez, M. A., Wasserman, J. C., & Duran, R. (2006). Characterization of hydrocarbonoclastic bacterial communities from mangrove sediments in Guanabara Bay, Brazil. Research in Microbiology, 157(8), 752–762.

    Article  CAS  Google Scholar 

  • Burd, G., & Ward, O. P. (1996). Involvement of a surface-active high molecular weight factor in degradation of polycyclic aromatic hydrocarbons by Pseudomonas marginalis. Canadian Journal of Microbiology, 42, 791–797.

    Article  CAS  Google Scholar 

  • Burns, K. A., Codi, S., Swannell, R. J. P., & Duke, N. C. (1999). Assessing the petroleum hydrocarbon potential of endogenous tropical marine wetland microorganisms: flask experiments. Mangroves and Salt Marshes, 3, 67–83.

    Article  Google Scholar 

  • Cai, Q. Y., Mo, C. H., Wu, Q. T., Wang, B. G., & Zhu, X. Z. (2002). Effect of municipal sludges and chemical fertiluers on the content of polycyclic aromatic hydrocarbons (PAHs) in paddy soil grown Ipomoea aquatica Fossk. Acta Pedologica Sinica (in Chinese), 39(6), 887–891.

    CAS  Google Scholar 

  • Cerniglia, C. E. (1993). Biodegradation of polycyclic aromatic hydrocarbons. Current Opinion Biotechnology, 4, 331–338.

    Article  CAS  Google Scholar 

  • Cerniglia, C. E. (1992). Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation, 3, 351–368.

    Article  CAS  Google Scholar 

  • Chen, J., Wong, M. H., Wong, Y. S., & Tam, N. F. Y. (2008). Multi-factors on biodegradation kinetics of polycyclic aromatic hydrocarbons (PAHs) by Sphingomonas sp. a bacterial strain isolated from mangrove sediment. Marine Pollution Bulletin, 57, 695–702.

    Article  CAS  Google Scholar 

  • de Carvalho, C. C. C. R. (2010). Adaptation of Rhodococcus to organic solvents. In H. M. Alvarez (Ed.), Biology of Rhodococcus (pp. 109–131). Berlin Heidelberg: Springer.

    Chapter  Google Scholar 

  • de Carvalho, C. C. C. R. (2012). Adaptation of Rhodococcus erythropolis cells for growth and bioremediation under extreme conditions. Resources Microbiology, 163, 125–136.

    Article  Google Scholar 

  • de Carvalho, C. C. C. R., Marques, M. P. C., Hachicho, N., & Heipieper, H. J. (2014). Rapid adaptation of Rhodococcus erythropolis cells to salt stress by synthesizing polyunsaturated fatty acids. Applied Microbiology Biotechnology, 98, 5599–5606.

    Google Scholar 

  • Deziel, E., Paquette, G., & Villemur, R. (1996). Biosurfactant production by a soil Pseudomonas strain growing on polycyclic aromatic hydrocarbons. Applied Environmental Microbiology, 62, 1908–1912.

    CAS  Google Scholar 

  • Dowty, R. A., Shaffer, G. P., Hester, M. W., Childers, G. W., Campo, F. M., & Greene, M. C. (2001). Phytoremediation of small-scale oil spills in fresh marsh environments: a mesocosm simulation. Marine Environmental Research, 52, 195–211.

    Article  CAS  Google Scholar 

  • Erickson, D. C., Loehr, R. C., & Neuhauser, E. F. (1993). PAH loss during bioremediation of manufactured gas plant site soil. Water Research, 27, 911–919.

    Article  CAS  Google Scholar 

  • Espinosa, E., Martinez, M. E., Torres, E. F., & Rojas, M. G. (2005). Improvement of the hydrocarbon phytoremediation rate by Cyperus laxus Lam. inoculated with a microbial consortium in a model system. Chemosphere, 59, 405–413.

    Article  Google Scholar 

  • Eun-Hee, L., Kang, L. K., & Cho, K.-S. (2011). Bioremediation of diesel-contaminated soils by natural attenuation, biostimulation and bioaugmentation employing Rhodococcus sp. EH831. Korean Journal of Microbiology Biotechnology, 39(1), 86–92.

    Google Scholar 

  • Fan, C. Y., & Krishnamurthy, M. (1995). Enzymes for enhancing bioremediation of petroleum-contaminated soils: a brief review. Air Waste Management Association, 45, 453–460.

    Article  CAS  Google Scholar 

  • Forsyth, J. V., Tsao, Y. M., & Bleam, R. D. (1995). Bioremediation: when is augmentation needed. In R. E. Hinchee, J. Fredrickson, & B. C. Alleman (Eds.), Bioaugmentation for Site Remediation (pp. 1–14). Columbus: Battelle Press.

    Google Scholar 

  • Gardner, W. S., Lee, R. F., Tenore, K. R., & Smith, L. W. (1979). Degradation of selected polycyclic aromatic hydrocarbons in coastal sediments: importance of microbes and polychaete worms. Water, Air, and Soil Pollution, 11, 339–347.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Herbs, S. E., & Schwall, L. R. (1978). Microbial transformation of polycyclic aromatic hydrocarbons in pristine and petroleum-contaminated sediments. Applied Environmental Microbiology, 35, 306–316.

    Google Scholar 

  • Hughes, J. B., Beckles, D. M., Chandra, S. D., & Ward, C. H. (1997). Utilization of bioremediation processes for the treatment of PAH-contaminated sediments. Journal of Industrial Microbiology and Biotechnology, 18, 152–160.

    Article  CAS  Google Scholar 

  • Iwamoto, T., & Nasu, M. (2001). Review: current bioremediation practice and perspective. Journal of Bioscience and Bioengineering, 92, 1–8.

    Article  CAS  Google Scholar 

  • Jia, L. Q., Qu, Z. Q., & Quyang, Z. Y. (2005). Ecological behavior of linear alkylbenzene sulfonate (LAS) in soil-plant systems. Pedosphere, 15(2), 216–224.

    CAS  Google Scholar 

  • Johnsen, A. R., Wick, L. Y., & Harms, H. (2005). Principles of microbial PAH-degradation in soil. Environmental Pollution, 133, 71–84.

    Article  CAS  Google Scholar 

  • Joner, E. J., Corgie, S., Amellal, N., & Leyval, C. (2005). Nutritional constraints to PAH degradation in a rhizosphere model. Soil Biology Biochemistry, 34, 859–864.

    Article  Google Scholar 

  • 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 & Biodegradation, 45, 57–88.

    Article  CAS  Google Scholar 

  • Kastner, M., & Mahro, B. (1996). Microbial degradation of polycyclic aromatic hydrocarbons in soils affected by the organic matrix of compost. Applied Microbiology and Biotechnology, 44, 668–675.

    Article  CAS  Google Scholar 

  • Ke, L., Wang, W. Q., Wong, T. W. Y., Wong, Y. S., & Tam, N. F. Y. (2003). Removal of pyrene from contaminated sediments by mangrove microcosms. Chemosphere, 51, 25–34.

    Article  CAS  Google Scholar 

  • Kelley, I., Freeman, J. P., Evans, F. E., & Cerniglia, C. E. (1993). Identification of metabolites from the degradation of fluoranthene by Mycobacterium sp. Strain PYR-1. Applied Environmental Microbiology, 59, 800–806.

    CAS  Google Scholar 

  • Kinney, P. J., Button, D. K., & Schell, D. M. (1969). Kinetics of dissipation and biodegradation of crude oil in Alaska’s Cook Inlet. In Proceedings of 1969 Joint Conference on Prevention and Control of Oil Spills (pp. 333–340). Washington, D.C: American Petroleum Institute.

    Google Scholar 

  • Kuyukina, M. S., & Ivshina, I. B. (2010). Rhodococcus biosurfactants: biosynthesis, properties, and potential applications. In H. M. Alvarez (Ed.), Biology of Rhodococcus (pp. 291–313). Berlin Heidelberg: Springer.

    Chapter  Google Scholar 

  • Kuyukina, M. S., Ivshina, I. B., Makarov, S. O., Litvinenko, L. V., Cunningham, C. J., & Philp, J. C. (2005). Effect of biosurfactants on crude oil desorption and mobilization in a soil system. Environmental International, 31, 155–161.

    Article  CAS  Google Scholar 

  • Lang, S., & Philp, J. C. (1998). Surface-active lipids in rhodococci. Antonie van Leeuwenhoek, 74, 59–70.

    Article  CAS  Google Scholar 

  • Larkin, M. J., Kulakov, L. A., & Allen, C. C. R. (2010a). Rhodococcus. In K. N. Timmis (Ed.), Handbook of Hydrocarbon and Lipid Microbiology (pp. 1839–1852). Heidelberg: Springer-Verlag.

    Chapter  Google Scholar 

  • Larkin, M. J., Kulakov, L. A., & Allen, C. C. R. (2010b). Rhodococcus: genetics and functional genomics. In K. N. Timmis (Ed.), Handbook of Hydrocarbon and Lipid Microbiology (pp. 1345–1353). Heidelberg: Springer-Verlag.

    Chapter  Google Scholar 

  • Larkin, M. J., Kulakov, L. A., & Allen, C. C. R. (2005). Biodegradation and Rhodococcus – masters of catabolic versatility. Environmental. Biotechnology, 16, 282–290.

    CAS  Google Scholar 

  • Lu, H., Zhang, Y., Liu, B., Liu, J., Ye, J., & Yan, C. (2011). Rhizodegradation gradients of phenanthrene and pyrene in sediment of mangrove (Kandelia candel (L.) Druce). Journal of Hazardous Material, 196, 263–269.

    Article  CAS  Google Scholar 

  • Luan, T. G., Yu, K. S. H., Zhong, Y., Zhou, H. W., Lan, C. Y., & Tam, N. F. Y. (2006). Study of metabolites from the degradation of polycyclic aromatic hydrocarbons (PAHs) by bacterial consortium enriched from mangrove sediments. Chemosphere, 65, 2289–2296.

    Article  CAS  Google Scholar 

  • Marini, M., & Frapiccini, E. (2013). Persistence of polycyclic aromatic hydrocarbons in sediments in the deeper area of the Northern Adriatic Sea (Mediterranean Sea). Chemosphere, 90, 1839–1846.

    Article  CAS  Google Scholar 

  • Martinkova, L., Uhnakova, B., Patek, M., Nesvera, J., & Kren, V. (2009). Biodegradation potential of the genus Rhodococcus. Environmental International, 35, 162–177.

    Article  CAS  Google Scholar 

  • Masy, T., Demaneche, S., Tromme, O., Thonart, P., Jacques, P., Hiligsmann, S., & Vogel, T. M. (2016). Hydrocarbon biostimulation and bioaugmentation in organic carbon and clay-rich soils. Soil Biology & Biochemistry, 99, 66–74.

    Article  CAS  Google Scholar 

  • Mills, M. A., Bonner, J. S., McDonald, T. J., Page, C. A., & Autenrieth, R. L. (2003). Intrinsic bioremediation of a petroleum-impacted wetland. Marine Pollution Bulletin, 46, 887–899.

    Article  CAS  Google Scholar 

  • Mueller, J. G., Lantz, S. E., Blattmann, B. O., & Chapman, P. J. (1991). Bench-scale evaluation of alternative biological treatment process for the remediation of pentachlorophenol and creosote contaminated materials: solid phase bioremediation. Environmental Science and Technology, 25, 1045–1055.

    Article  CAS  Google Scholar 

  • Moreira, I. T. A., Oliveira, O. M. C., Triguis, J. A., Dos Santos, A. M. P., Queiroz, A. F. S., Martins, C. M. S., Silva, C. S., & Jesus, R. S. (2011). Phytoremediation using Rhizophora mangle L. in mangrove sediments contaminated by persistent total petroleum hydrocarbons (TPH’s). Microchemistry Journal, 29, 376–382.

    Article  Google Scholar 

  • Neff, J. M. (1979). Polycyclic aromatic hydrocarbons in the aquatic environment: sources, fate and biological effects. Essex, England: Applied Science Publishers, Ltd.

    Google Scholar 

  • Park, K. S., Sims, R. C., & Dupont, R. (1990). Transformations of PAHs in soil systems. Journal Environmental Engineering, 116, 632–640.

    Article  CAS  Google Scholar 

  • Puri, R. K., Ye, Q. P., Kapila, S., Lower, W. R., & Puri, V. (1997). Plant uptake and metabolism of polychlorinated biphenyls PCBs. In W. Wang, J. W. Gorsuch, & J. S. Hughes (Eds.), Plants for Environmental Studies (pp. 482–513). New York: CRC Press LLC.

    Google Scholar 

  • Ramsay, M. A., Swannell, R. P. J., Shipton, W. A., Duke, N. C., & Hill, R. T. (2000). Effect of bioremediation community in oiled mangrove sediments. Marine Pollution Bulletin, 41, 413–419.

    Article  CAS  Google Scholar 

  • Riser-Roberts, E. (1998). Remediation of petroleum contaminated soils: biological, physical, and chemical processes (pp. 5–313). Boca Raton: Lewis Publishers.

    Book  Google Scholar 

  • Samanta, S. K., Singh, O. V., & Jain, R. K. (2002). Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnology, 20, 243–248.

    Article  CAS  Google Scholar 

  • Sims, R. C., & Overcash, M. R. (1983). Fate of polynuclear aromatic compounds (PNAs) in soil-plant systems. Residue Review, 1, 2–68.

    Google Scholar 

  • Song, H. G., Wang, X., & Bartha, R. (1990). Bioremediation potential of terrestrial fuel spills. Applied Environmental Microbiology, 56, 652–656.

    CAS  Google Scholar 

  • Tam, N. F. Y., Guo, C. L., Yau, W., & Wong, Y. S. (2002). Preliminary study on biodegradation of phenanthrene by bacteria isolated from mangrove sediments in Hong Kong. Marine Pollution Bulletin, 45, 316–324.

    Article  CAS  Google Scholar 

  • Tam, N. F. Y., & Wong, Y. S. (2008). Effectiveness of bacterial inoculum and mangrove plants on remediation of sediment contaminated with polycyclic aromatic hydrocarbons. Marine Pollution Bulletin, 57, 716–726.

    Article  CAS  Google Scholar 

  • Tian, Y., Liu, H. J., Zheng, T. L., Kwon, K. K., Kim, S. J., & Yan, C. L. (2008). PAHs contamination and bacterial communities in mangrove surface sediments of the Jiulong River Estuary. China Marine Pollution Bulletin, 57, 707–715.

    Article  CAS  Google Scholar 

  • Trzesicka-Mlynarz, D., & Ward, O. P. (1995). Degradation of polycyclic aromatic hydrocarbons (PAHs) by a mixed culture and its components pure cultures, obtained from PAH-contaminated soil. Canadian Journal of Microbiology, 41, 470–476.

    Article  CAS  Google Scholar 

  • Uthe, J. F. (1991). Polycyclic aromatic hydrocarbons in the environment. Canadian Chemistry News, 43(7), 25–27.

    CAS  Google Scholar 

  • Vogel, T. M. (1996). Bioaugmentation as a soil bioremediation approach. Current. Opinion and Biotechnology, 7, 311–316.

    Article  CAS  Google Scholar 

  • Walker, J. D., & Colwell, R. R. (1975). Degradation of hydrocarbons and mixed hydrocarbon substrate by microorganisms from Chesapeake Bay. Progress Water Technology, 7, 83–91.

    Google Scholar 

  • Wannoussa, W., Masy, T., Lambert, S. D., Heinrichs, B., Tasseroul, L., Al-Ahmad, A., Weekers, F., Thonart, P., & Hiligsmann, S. (2015). Effect of iron nanoparticles synthesized by a sol–gel process on Rhodococcus erythropolis T902.1 for biphenyl degradation. Journal of Water Resource and Protection, 7, 264–277.

    Article  CAS  Google Scholar 

  • Weekers, F., Jacques, P., Springael, D., Mergeay, M., Diels, L., & Thonart, P. (1999). Improving the catabolic functions of desiccation-tolerant soil bacteria. In B. H. Davison & M. Finkelstein (Eds.), Twentieth Symposium on Biotechnology for Fuels and Chemicals (pp. 251–266). Gatlinburg, Tennesee: Humana Press.

    Chapter  Google Scholar 

  • Whyte, L. G., Slagman, S. J., Pietrantonio, F., Bourbonni_ere, L., Koval, S. F., Lawrence, J. R., Inniss, W. E., & Greer, C. W. (1999). Physiological adaptations involved in alkane assimilation at a low temperature by Rhodococcus sp. strain Q15. Applied Environmental Microbiology, 65, 2961–2968.

    CAS  Google Scholar 

  • Wild, S. R., Berrow, M. L., & Jones, K. C. (1991). The persistence of polynuclear aromatic hydrocarbons (PAHs) in sewage sludge-amended agricultural soils. Environmental Pollution, 72, 141–57.

    Article  CAS  Google Scholar 

  • Yan, J., Cheng, S. P., Zhang, X. X., Shi, L., & Zhu, J. (2004). Effect of four metals on the degradation of purified terephthalic acid wastewater by Phanaerochaete chrysosporium and strain Fhhh. Bulletin of Environmental Contamination Toxicology, 72, 387–393.

    Article  CAS  Google Scholar 

  • Yu, K. S. H., Wong, A. H. Y., Yau, K. W. Y., Wong, Y. S., & Tam, N. F. Y. (2005). Natural attenuation, biostimulation and bioaugmentation on biodegradation of polycyclic aromatic hydrocarbons (PAHs) in mangrove sediments. Marine Pollution Bulletin, 51, 1071–1077.

    Article  CAS  Google Scholar 

  • Zhang, X. X., Cheng, S. P., Zhu, C. J., & Sun, S. L. (2006). Microbial PAH-degradation in soil: degradation pathways and contributing factors. Pedosphere, 16(5), 555–565.

    Article  CAS  Google Scholar 

  • Zhou, Q. X., & Hua, T. (2004). Bioremediation: a review of applications and problems to be resolved. Progress Natural Science, 14(11), 937–944.

    Article  CAS  Google Scholar 

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Lang, F.S., Destain, J., Delvigne, F. et al. Biodegradation of Polycyclic Aromatic Hydrocarbons in Mangrove Sediments Under Different Strategies: Natural Attenuation, Biostimulation, and Bioaugmentation with Rhodococcus erythropolis T902.1. Water Air Soil Pollut 227, 297 (2016). https://doi.org/10.1007/s11270-016-2999-4

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