Advertisement

The Application of Biosurfactants in Bioremediation of the Aged Sediment Contaminated with Polychlorinated Biphenyls

  • Katarína Lászlová
  • Hana Dudášová
  • Petra Olejníková
  • Gabriela Horváthová
  • Zuzana Velická
  • Hana Horváthová
  • Katarína Dercová
Article

Abstract

Currently, there is a considerable interest on application of bio-based surfactants as an alternative to conventional synthetic ones as well as in bioremediation technologies to decontaminate polluted sites more effectively. The work is focused on the study of the effects of two biosurfactants, non-ionic Saponin and anionic Rhamnolipids R-90 on the biodegradation of Delor 103, the industrial mixture of polychlorinated biphenyls (PCBs) by bioaugmented bacterial strains. The bacterial isolates used in this study were obtained from long-term PCB-contaminated sediments of the industrial waste Strážsky canal. Enhanced biodegradation of PCBs by Gram-negative strains Achromobacter xylosoxidans (93%) and Stenotrophomonas maltophilia (66%) was observed with the addition of (bio)surfactants Saponin, Rhamnolipids R-90, and Triton X-100 in defined liquid mineral media. The addition of biosurfactant Saponin and Rhamnolipids R-90 increased the PCB biodegradation (55 and 60%, respectively) in the bioaugmented PCB-contaminated sediment inoculated with bacterial strain A. xylosoxidans as well. Regarding to the inhibitory effect of used (bio)surfactants, the obtained IC50 values confirmed that the non-ionic phytogenic Saponin and synthetic surfactant Triton X-100 had a significantly lower toxicity toward bioluminescence of the standard bacteria Vibrio fischeri and used PCB-degrading bacterial strains than the anionic bacterial surfactant Rhamnolipids R-90.

Keywords

Bacteria Biodegradation Biosurfactants PCBs 

Notes

Funding information

The authors received financial support from the Scientific Grant Agency (project No. 1/0295/15) and from the Slovak Research and Development Agency (project No. APVV-0656-12) of the Ministry of Education, Research and Sport of the Slovak Republic.

References

  1. Akiyode, O., George, D., Getti, G., & Boateng, J. (2016). Systematic comparison of the functional physico-chemical characteristics and biocidal activity of microbial derived biosurfactants on blood-derived and breast cancer cells. Journal of Colloid and Interface Science, 479, 221–233.CrossRefGoogle Scholar
  2. Bezza, F. A., Beukes, M., & Nkhalambayausi Chirwa, E. M. (2015). Application of biosurfactant produced by Ochrobactrum intermedium CN3 for enhancing petroleum sludge bioremediation. Process Biochemistry, 50, 1911–1922.CrossRefGoogle Scholar
  3. Bharali, P., Saikiab, J. P., Raya, A., & Konwarc, B. K. (2013). Rhamnolipid (RL) from Pseudomonas aeruginosa OBP1: a novel chemotaxis and antibacterial agent. Colloids and Surfaces B: Biointerfaces, 103, 502–509.CrossRefGoogle Scholar
  4. Billingsley, K. A., Backus, S. M., & Ward, O. P. (1999). Effect of surfactant solubilization on biodegradation of polychlorinated biphenyl congeners by Pseudomonas LB400. Applied Microbiology and Biotechnology, 52, 255–260.CrossRefGoogle Scholar
  5. Blyth, W., Shahsavari, E., Morrison, P. D., & Ball, A. S. (2015). Biosurfactant from red ash trees enhances the bioremediation of PAH contaminated soil at a former gasworks site. Journal of Environmental Management, 162, 30–36.CrossRefGoogle Scholar
  6. Borja, J., Taleon, D. M., Auresenia, J., & Gallardo, S. (2005). Polychlorinated biphenyls and their biodegradation. Process Biochemistry, 40, 1999–2013.CrossRefGoogle Scholar
  7. Brázová, T., Hanzelová, V., & Miklisová, D. (2012). Bioaccumulation of six PCB indicator congeners in a heavily polluted water reservoir in eastern Slovakia: tissue-specific distribution in fish and their parasites. Parasitology Research, 111, 779–786.CrossRefGoogle Scholar
  8. Danielovič, I., Hecl, J., & Danilovič, M. (2014). Soil contamination by PCBs on a regional scale: the case of Strážske, Slovakia. Polish Journal of Environmental Studies, 23, 1547–1554.Google Scholar
  9. Denyer, S. P., & Maillard, J. Y. (2002). Cellular impermeability and uptake of biocides and antibiotics in gram-negative bacteria. Journal of Applied Microbiology, 92, 35–45.CrossRefGoogle Scholar
  10. Dercová, K., Čičmanová, J., Lovecká, P., Demnerová, K., Macková, M., Hucko, P., & Kušnír, P. (2008). Isolation and identification of PCB-degrading microorganisms from contaminated sediments. International Biodeterioration and Biodegradation, 62, 219–225.CrossRefGoogle Scholar
  11. Dercová, K., Šeligová, J., Dudášová, H., Mikulášová, M., Šilhárová, K., Tóthová, L., & Hucko, P. (2009). Characterization of the bottom sediments contaminated with polychlorinated biphenyls: evaluation of ecotoxicity and biodegradability. International Biodeterioration and Biodegradation, 63, 440–449.CrossRefGoogle Scholar
  12. Dercová, K., Lászlová, K., Dudášová, H., Murínová, S., Balaščáková, M., & Škarba, J. (2015). The hierarchy of bioremediation technology choices: prospects of using the potential of bacterial degraders. Chemické Listy, 109, 281–290.Google Scholar
  13. Dudášová, H., Lukáčová, L., Murínová, S., Puškárová, A., Pangallo, D., & Dercová, K. (2014). Bacterial strains isolated from PCB-contaminated sediments and their use for bioaugmentation strategy in microcosms. Journal of Basic Microbiology, 54, 253–260.CrossRefGoogle Scholar
  14. Dudášová, H., Lászlová, K., Lukáčová, L., Balaščáková, M., Murínová, S., & Dercová, K. (2016). Bioremediation of PCB-contaminated sediments and evaluation of pre- and post-treatment ecotoxicity. Chemical Papers, 70, 1049–1058.Google Scholar
  15. Edwards, K. R., Lepo, J. E., & Lewis, M. A. (2003). Toxicity comparison of biosurfactants and synthetic surfactants used in oil spill remediation to two estuarine species. Marine Pollution Bulletin, 46, 1309–1316.CrossRefGoogle Scholar
  16. Egorova, D. O., Demakov, V. A., & Plotnikova, E. G. (2013). Bioaugmentation of a PCB contaminated soil with two aerobic bacterial strains. Journal of Hazardous Materials, 261, 378–386.CrossRefGoogle Scholar
  17. Ehlers, L. J., & Luthy, R. G. (2003). Contaminant bioavailability in soil and sediment. Environmental Science and Technology, 37, 295A–302A.CrossRefGoogle Scholar
  18. Fava, F., & Di Gioia, D. (1998). Effects of triton X-100 and Quillaya Saponin on the ex situ bioremediation of a chronically polychlorobiphenyl-contaminated soil. Applied Microbiology and Biotechnology, 50, 623–630.CrossRefGoogle Scholar
  19. Fava, F., & Piccolo, A. (2001). Effects of humic substances on the bioavailabiolity and aerobic biodegradation of polychlorinated biphenyls in a model soil. Biotechnology and Bioengineering, 77, 204–2011.CrossRefGoogle Scholar
  20. Fava, F., & Picollo, A. (2002). Effects of humic substances on the bioavailability and aerobic biodegradation of polychlorinated biphenyls in a model soil. Biotechnology and Bioengineering, 77(2), 204–211.CrossRefGoogle Scholar
  21. Franzetti, A., Di Gennaro, P., Bevilacqua, A., Papacchini, M., & Bestetti, G. (2006). Environmental features of two commercial surfactants widely used in soil remediation. Chemosphere, 62, 1474–1480.CrossRefGoogle Scholar
  22. Furukawa, K., Suenaga, H., & Goto, M. (2004). Biphenyl dioxygenases: functional versatilities and directed evolution. Journal of Bacteriology, 186, 5189–5196.CrossRefGoogle Scholar
  23. Gomes, H. I., Dias-Ferreira, C., Ottosen, L. M., & Ribeiro, A. B. (2014). Electrodialytic remediation of polychlorinated biphenyls contaminated soil with iron nanoparticles and two different surfactants. Journal of Colloid and Interface Science, 433, 189–195.CrossRefGoogle Scholar
  24. Hiller, E., Zemanová, L., Sirotiak, M., & Jurkovič, Ľ. (2011). Concentrations, distributions, and sources of polychlorinated biphenyls and polycyclic aromatic hydrocarbons in bed sediments of the water reservoirs in Slovakia. Environmental Monitoring and Assessment, 173, 883–897.CrossRefGoogle Scholar
  25. Jensen, J. (1999). Fate and effects of linear alkylbenzene sulphonates (LAS) in the terrestrial environment. Science of the Total Environment, 226, 93–111.CrossRefGoogle Scholar
  26. Kaczorek, E., Sałek, K., Guzik, U., Dudzińska-Bajorek, B., & Olszanowski, A. (2013). The impact of long-term contact of Achromobacter sp. 4(2010) with diesel oil—changes in biodegradation, surface properties and hexadecane monooxygenase activity. International Biodeterioration and Biodegradation, 78, 7–16.CrossRefGoogle Scholar
  27. Kaczorek, E., Smułek, W., Zdarta, A., Sawczuk, A., & Zgoła-Grześkowiak, A. (2016). Influence of saponins on the biodegradation of halogenated phenols. Ecotoxicology and Environmental Safety, 131, 127–134.CrossRefGoogle Scholar
  28. Kobayashi, T., Kaminaga, H., Navarro, R. R., & Iimura, Y. (2012). Application of aqueous saponin on the remediation of polycyclic aromatic hydrocarbons-contaminated soil. Journal of Environmental Science and Health. Part A, Toxic/Hazardous Substances & Environmental Engineering, 47, 1138–1145.CrossRefGoogle Scholar
  29. Langer, P., Kočan, A., Tajtáková, M., Drobná, B., Chovancová, J., Rádiková, Z., et al. (2012). Environmental contamination with endocrine and metabolic disruptors and their impact on health of Slovakian resident. Monitor Medicíny SLS, 3–4, 5–12.Google Scholar
  30. Lászlová, K., Dercová, K., Horváthová, H., Murínová, S., Škarba, J., & Dudášová, H. (2016). Assisted bioremediation approaches—biostimulation and bioaugmentation—used in the removal of organochlorinated pollutants from the contaminated bottom sediments. International Journal of Environmental Research, 10, 367–378.Google Scholar
  31. Li, Y., Liang, F., Zhu, Y., & Wang, F. (2013). Phytoremediation of a PCB-contaminated soil by alfalfa and tall fescue single and mixed plants cultivation. Journal of Soils and Sediments, 13, 925–931.CrossRefGoogle Scholar
  32. Lima, T. M. S., Procópio, L. C., Brandão, F. D., Leão, B. A., Tótola, M. R., & Borges, A. C. (2011). Evaluation of bacterial surfactant toxicity towards petroleum degrading microorganisms. Bioresource Technology, 102, 2957–2964.CrossRefGoogle Scholar
  33. Liu, S., Guo, C., Liang, X., Wu, F., & Dang, Z. (2016). Nonionic surfactants induced changes in cell characteristics and phenanthrene degradation ability of Sphingomonas sp. GY2B. Ecotoxicology and Environmental Safety, 129, 210–218.CrossRefGoogle Scholar
  34. Makkar, R. S., & Rockne, K. J. (2003). Comparison of synthetic surfactants and biosurfactants in enhancing biodegradation of polycyclic aromatic hydrocarbons. Environmental Toxicology & Chemistry, 22, 2280–2292.CrossRefGoogle Scholar
  35. Maron, D. M., & Ames, B. J. (1983). Revised methods for Salmonella mutagenicity test. Mutation Research, 113, 173–215.CrossRefGoogle Scholar
  36. Martinéz, P., Agullo, L., Hernandez, M., & Seeger, M. (2007). Chlorobenzoate inhibits growth and induces stress proteins in the PCB-degrading bacterium Burkholderia xenovorans LB400. Microbiology, 188, 289–297.Google Scholar
  37. Mills, S. A., Thal, D. I., & Barney, J. (2007). A summary of the 209 PCB congener nomenclature. Chemosphere, 68, 1603–1612.CrossRefGoogle Scholar
  38. Mortelmans, K., & Zeiger, E. (2000). The Ames Salmonella/microsome mutagenicity assay. Mutation Research, 455, 29–60.CrossRefGoogle Scholar
  39. Mudgil, P. (2011). Biosurfactants for soil biology. In A. Singh, N. Parmar, & R. Kuhad (Eds.), Bioaugmentation, biostimulation, and biocontrol (pp. 203–206). Berlin: Springer.CrossRefGoogle Scholar
  40. Murínová, S., Dercová, K., & Dudášová, H. (2014). Degradation of polychlorinated biphenyls (PCBs) by four bacterial isolates obtained from the PCB-contaminated soil and PCB-contaminated sediment. International Biodeterioration & Biodegradation, 91, 52–59.CrossRefGoogle Scholar
  41. Ngigi, A., Dörfler, U., Scherb, H., Getenga, Z., Boga, H., & Schroll, R. (2011). Effect of fluctuating soil humidity on in situ bioavailability and degradation of atrazine. Chemosphere, 84, 369–375.CrossRefGoogle Scholar
  42. Pacwa-Płociniczak, M., Płaza, A. G., Piotrowska-Seget, Z., & Cameotra, S. (2011). Environmental applications of biosurfactants: recent advances. International Journal of Molecular Sciences, 12, 633–654.CrossRefGoogle Scholar
  43. Pieper, D. H. (2005). Aerobic degradation of polychlorinated biphenyls. Applied Microbiology and Biotechnology, 67, 170–191.CrossRefGoogle Scholar
  44. Pieper, H. D., & Seeger, M. (2008). Bacterial metabolism of polychlorinated biphenyls. Journal of Molecular Microbiology and Biotechnology, 15, 121–138.CrossRefGoogle Scholar
  45. Pijanowska, A., Kaczorek, E., Chrzanowski, Ł., & Olszanowski, A. (2007). Cell hydrophobicity of Pseudomonas spp. and Bacillus spp. bacteria and hydrocarbon biodegradation in the presence of Quillaya saponin. World Journal of Microbiology and Biotechnology, 23, 677–682.CrossRefGoogle Scholar
  46. Robinson, K. G., Ghosh, M. M., & Shi, Z. (1996). Mineralization enhancement of nonaqueous phase and soil bound PCB using biosurfactant. Water Science and Technology, 34, 303–309.CrossRefGoogle Scholar
  47. Schippers, C., Gessner, K., Mueller, T., & Scheper, T. (2000). Microbial degradation of phenanthrene by addition of a sophorolipid mixture. Journal of Biotechnology, 83, 189–198.CrossRefGoogle Scholar
  48. Seeger, M., Hernández, M., Méndez, V., Ponce, B., Córdova, M., & González, M. (2010). Bacterial degradation and bioremediation of chlorinated herbicides and biphenyls. Journal of Soil Science and Plant Nutrition, 10, 320–332.CrossRefGoogle Scholar
  49. Singer, A. C., Gilbert, E. S., Luepromchai, E., & Crowley, D. E. (2000). Bioremediation of polychlorinated biphenyl-contaminated soil using carvone and surfactant-grown bacteria. Applied Microbiology and Biotechnology, 54, 838–843.CrossRefGoogle Scholar
  50. Singh, A. K., & Cameotra, S. S. (2014). Influence of microbial and synthetic surfactant on the biodegradation of atrazine. Environmental Science and Pollution Research, 21, 2088–2097.CrossRefGoogle Scholar
  51. Slovak Office of Standards, Metrology and Testing (2006). Slovak standard: Water quality. Sampling. Part 12: Guidance on the design of sampling programmes and sampling techniques (757051). STN ISO 5667-12:2006. Bratislava, Slovakia.Google Scholar
  52. Slovak Office of Standards, Metrology and Testing (2007). Slovak standard: Water quality. Determination of the inhibitory effect of water samples on the light emission of Vibrio fischeri (Luminescent bacteria test). Part 2: Method using liquid-dried bacteria 757445-2007. STN ISO 11348-2:2007. Bratislava, Slovakia.Google Scholar
  53. Slovak Office of Standards, Metrology and Testing (2008). Slovak standard: Water quality (2008). Determination of the toxic effect of water constituents and waste water to duckweed (Lemna minor)—Duckweed growth inhibition test. (757747). STN ISO 20079. Bratislava, Slovakia.Google Scholar
  54. Soberón-Chávez, G., Lépine, F., & Déziel, E. (2005). Production of rhamnolipids by Pseudomonas aeruginosa. Applied Microbiology and Biotechnology, 68(6), 718–725.CrossRefGoogle Scholar
  55. Sotirova, A. V., Spasova, D. I., Galabova, D. N., Karpenko, E., & Shulga, A. (2008). Rhamnolipid–biosurfactant permeabilizing effects on gram-positive and gram-negative bacterial strains. Current Microbiology, 56, 639–644.CrossRefGoogle Scholar
  56. Sparg, S. G., Light, M. E., & van Staden, J. (2004). Biological activities and distribution of plant saponins. Journal of Ethnopharmacology, 94, 219–243.CrossRefGoogle Scholar
  57. Sütterlin, H., Alexy, R., & Kümmerer, K. (2008). The toxicity of the quaternary ammonium compound benzalkonium chloride alone and in mixtures with other anionic compounds to bacteria in test systems with Vibrio fischeri and Pseudomonas putida. Ecotoxicology and Environmental Safety, 71, 498–505.CrossRefGoogle Scholar
  58. Taniyasu, S., Kannan, K., Holoubek, I., Ansorgova, A., Horii, Y., Hanari, N., et al. (2003). Isomer-specific analysis of chlorinated biphenyls, naphthalenes and dibenzofurans in Delor: polychlorinated biphenyl preparations from the former Czechoslovakia. Environmental Pollution, 126, 169–178.CrossRefGoogle Scholar
  59. Tian, W., Yao, J., Liu, R., Zhu, M., Wang, F., Wu, X., et al. (2016). Effect of natural and synthetic surfactants on crude oil biodegradation by indigenous strains. Ecotoxicology and Environmental Safety, 129, 171–179.CrossRefGoogle Scholar
  60. Vasilyeva, G. K., Strijakova, E. R., Nikolaeva, S. N., Lebedev, A. T., & Shea, P. J. (2010). Dynamics of PCB removal and detoxification in historically contaminated soils amended with activated carbon. Environmental Pollution, 158, 770–777.CrossRefGoogle Scholar
  61. Viisimaa, M., Karpenko, O., Novikov, V., Trapido, M., & Goi, A. (2013). Influence of biosurfactant on combined chemical-biological treatment of PCB-contaminated soil. Chemical Engineering Journal, 220, 352–359.CrossRefGoogle Scholar
  62. Viney, I., & Bewley, R. J. F. (1990). Preliminary studies on the development of a microbiological treatment for polychlorinated biphenyls. Archives of Environmental Contamination and Toxicology, 19, 789–796.CrossRefGoogle Scholar
  63. Volkering, F., Breure, A. M., Andel, J., & Rulkens, W. H. (1995). Influence of non-ionic surfactants on bioavailability and biodegradation of polycyclic aromatic hydrocarbons. Applied and Environmental Microbiology, 61, 1699–1705.Google Scholar
  64. Volkering, F., Breure, A. M., & Rulkens, W. H. (1998). Microbiological aspects of surfactant use for biological soil remediation. Biodegradation, 8, 401–417.CrossRefGoogle Scholar
  65. Vrana, B., Dercová, K., Baláž, Š., & Ševčíková, A. (1996). Effect of chlorobenzoates on the degradation of polychlorinated biphenyls (PCB) by Pseudomonas stutzeri. World Journal of Microbiology and Biotechnology, 12, 323–326.CrossRefGoogle Scholar
  66. Wang, L., Li, F., Zhan, Y., & Zhu, L. (2016). Shifts in microbial community structure during in situ surfactant-enhanced bioremediation of polycyclic aromatic hydrocarbon-contaminated soil. Environmental Science and Pollution Research, 23, 14451–14461.CrossRefGoogle Scholar
  67. Wang, X., Sun, L., Wang, L., Wu, H., Chen, S., & Zheng, X. (2017). Surfactant-enhanced bioremediation of DDTs and PAHs in contaminated farmland soil. Environmental Technology, 9, 1–12.Google Scholar
  68. Zhang, D., & Zhu, L. Z. (2012). Controlling technology of interfacial behaviors of organic pollutants and its application. Frontiers of Environmental Science & Engineering, 8, 305–315.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Katarína Lászlová
    • 1
  • Hana Dudášová
    • 2
  • Petra Olejníková
    • 3
  • Gabriela Horváthová
    • 4
  • Zuzana Velická
    • 4
  • Hana Horváthová
    • 1
  • Katarína Dercová
    • 1
  1. 1.Faculty of Chemical and Food Technology, Institute of BiotechnologySlovak University of TechnologyBratislavaSlovak Republic
  2. 2.Slovac Academy of Science, Institute of ChemistryBratislavaSlovak Republic
  3. 3.Faculty of Chemical and Food Technology, Institute of Biochemistry and MicrobiologySlovak University of TechnologyBratislavaSlovak Republic
  4. 4.Water Research InstituteBratislavaSlovak Republic

Personalised recommendations