Bioavailability of Polycyclic Aromatic Hydrocarbons in Soil as Affected by Microorganisms and Plants

  • Jose Julio Ortega-CalvoEmail author
  • Rosa Posada-Baquero
  • José Luis Garcia
  • Manuel Cantos
Conference paper
Part of the Sustainability in Plant and Crop Protection book series (SUPP)


The bioavailability of polycyclic aromatic hydrocarbons (PAHs) in soil can be enhanced through a variety of microbial and plant functions, that can be incorporated into optimized bioremediation technologies. In this review, we examine the potential of (bio)surfactants, the chemotactic mobilization of pollutant-degrading bacteria, and the role of bacterial attachment, to enhance biodegradation of PAHs. Plants can also play an active role in enhancing bioavailability of PAHs through rhizosphere-related mechanisms associated to specific exudate components that affect bacterial chemotaxis, pollutant mobilization, and intra-aggregate bacterial growth.


Biodegradation Bioremediation Bioavailability Bioaccessibility PAHs Roots Biosurfactant Chemotaxis Attachment Desorption Exudates Bacteria Transport 



This study was supported by the Spanish Ministry of Science and Innovation (CGL2013-44554-R and CGL2016-77497-R), the Andalusian Government (RNM 2337), and the European Commission (LIFE15 ENV/IT/000396).


  1. Aprill, W., & Sims, R. C. (1990). Evaluation of the use of prairie grasses for stimulating polycyclic aromatic hydrocarbon treatment in soil. Chemosphere, 20, 253–265.CrossRefGoogle Scholar
  2. Badri, D. V., & Vivanco, J. M. (2009). Regulation and function of root exudates. Plant Cell and Environment, 32, 666–681.CrossRefGoogle Scholar
  3. Bertin, C., Yang, X. H., & Weston, L. A. (2003). The role of root exudates and allelochemicals in the rhizosphere. Plant and Soil, 256, 67–83.CrossRefGoogle Scholar
  4. Bottner, P., Pansu, M., & Sallih, Z. (1999). Modelling the effect of active roots on soil organic matter turnover. Plant and Soil, 216, 15–25.CrossRefGoogle Scholar
  5. Briones, A. M., Okabe, S., Umemiya, Y., Ramsing, N. B., Reichardt, W., & Okuyama, H. (2003). Ammonia-oxidizing bacteria on root biofilms and their possible contribution to N use efficiency of different rice cultivars. Plant and Soil, 250, 335–348.CrossRefGoogle Scholar
  6. Bueno-Montes, M., Springael, D., & Ortega-Calvo, J. J. (2011). Effect of a non-ionic surfactant on biodegradation of slowly desorbing PAHs in contaminated soils. Environmental Science and Technology, 45, 3019–3026.CrossRefPubMedGoogle Scholar
  7. Chen, Z. X., Ni, H. G., Jing, X., Chang, W. J., Sun, J. L., & Zeng, H. (2015). Plant uptake, translocation, and return of polycyclic aromatic hydrocarbons via fine root branch orders in a subtropical forest ecosystem. Chemosphere, 131, 192–200.CrossRefPubMedGoogle Scholar
  8. Chigbo, C., & Batty, L. (2013). Effect of combined pollution of chromium and benzo (a) pyrene on seed growth of Lolium perenne. Chemosphere, 90, 164–169.CrossRefPubMedGoogle Scholar
  9. Clode, P. L., Kilburn, M. R., Jones, D. L., Stockdale, E. A., Cliff, J. B., et al. (2009). In situ mapping of nutrient uptake in the rhizosphere using nanoscale secondary ion mass spectrometry. Plant Physiology, 151, 1751–1757.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Compant, S., Clement, C., & Sessitsch, A. (2010). Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization. Soil Biology and Biochemistry, 42, 669–678.CrossRefGoogle Scholar
  11. Congiu, E., & Ortega-Calvo, J. J. (2014). Role of desorption kinetics in the rhamnolipid-enhanced biodegradation of polycyclic aromatic hydrocarbons. Environmental Science and Technology, 48, 10869–10877.CrossRefPubMedGoogle Scholar
  12. Congiu, E., Parsons, J. R., & Ortega-Calvo, J. J. (2015). Dual partitioning and attachment effects of rhamnolipid on pyrene biodegradation under bioavailability restrictions. Environmental Pollution, 205, 378–384.CrossRefPubMedGoogle Scholar
  13. Degryse, F., Smolders, E., & Merckx, R. (2006). Labile Cd complexes increase Cd availability to plants. Environmental Science and Technology, 40, 830–836.CrossRefPubMedGoogle Scholar
  14. D'Orazio, V., Ghanem, A., & Senesi, N. (2013). Phytoremediation of pyrene contaminated soils by different plant species. Clean-Soil Air Water, 41, 377–382.CrossRefGoogle Scholar
  15. Ehlers, L. J., & Luthy, R. G. (2003). Contaminant bioavailability in soil and sediment. Environmental Science and Technology, 37, 295A–302A.CrossRefPubMedGoogle Scholar
  16. Garcia-Junco, M., De Olmedo, E., & Ortega-Calvo, J. J. (2001). Bioavailability of solid and non-aqueous phase liquid (NAPL)-dissolved phenanthrene to the biosurfactant-producing bacterium Pseudomonas aeruginosa 19SJ. Environmental Microbiology, 3, 561–569.CrossRefPubMedGoogle Scholar
  17. Garcia-Junco, M., Gomez-Lahoz, C., Niqui-Arroyo, J. L., & Ortega-Calvo, J. J. (2003). Biodegradation- and biosurfactant-enhanced partitioning of polycyclic aromatic hydrocarbons from nonaqueous-phase liquids. Environmental Science and Technology, 37, 2988–2996.CrossRefPubMedGoogle Scholar
  18. Grayston, S. J., Vaughan, D., & Jones, D. (1997). Rhizosphere carbon flow in trees, in comparison with annual plants: The importance of root exudation and its impact on microbial activity and nutrient availability. Applied Soil Ecology, 5, 29–56.CrossRefGoogle Scholar
  19. Haderlein, A., Legros, R., & Ramsay, B. (2001). Enhancing pyrene mineralization in contaminated soil by the addition of humic acids or composted contaminated soil. Applied Microbiology and Biotechnology, 56, 555–559.CrossRefPubMedGoogle Scholar
  20. Haftka, J. J. H., Parsons, J. R., Govers, H. A. J., & Ortega-Calvo, J. J. (2008). Enhanced kinetics of solid-phase microextraction and biodegradation of polycyclic aromatic hydrocarbons in the presence of dissolved organic matter. Environmental Toxicology and Chemistry, 27, 1526–1532.CrossRefPubMedGoogle Scholar
  21. Hegde, R. S., & Fletcher, J. S. (1996). Influence of plant growth stage and season on the release of root phenolics by mulberry as related to development of phytoremediation technology. Chemosphere, 32, 2471–2479.CrossRefGoogle Scholar
  22. Hughes, M., Donnelly, C., Crozier, A., & Wheeler, C. T. (1999). Effects of the exposure of roots of Alnus glutinosa to light on flavonoids and nodulation. Canadian Journal of Botany, 77, 1311–1315.CrossRefGoogle Scholar
  23. Jimenez-Sanchez, C., Wick, L. Y., & Ortega-Calvo, J. J. (2012). Chemical effectors cause different motile behavior and deposition of bacteria in porous media. Environmental Science and Technology, 46, 6790–6797.CrossRefPubMedGoogle Scholar
  24. Jimenez-Sanchez, C., Wick, L. Y., Cantos, M., & Ortega-Calvo, J. J. (2015). Impact of dissolved organic matter on bacterial tactic motility, attachment, and transport. Environmental Science and Technology, 49, 4498–4505.CrossRefPubMedGoogle Scholar
  25. Krell, T., Lacal, J., Reyes-Darías, J. A., Jimenez-Sanchez, C., Sungthong, R., & Ortega-Calvo, J. J. (2013). Bioavailability of pollutants and chemotaxis. Current Opinion in Biotechnology, 24, 451–456.CrossRefPubMedGoogle Scholar
  26. Kummerova, M., Kmentova, E., & Koptikova, J. (2001). Effect of fluoranthene on growth and primary processes of photosynthesis in faba bean and sunflower. Rostlinna Vyroba, 47, 344–351.Google Scholar
  27. Kuzyakov, Y., & Domanski, G. (2000). Carbon input by plants into the soil. Review. Journal of Plant Nutrition and Soil Science-Zeitschrift Fur Pflanzenernahrung Und Bodenkunde, 163, 421–431.CrossRefGoogle Scholar
  28. Liste, H. H., & Alexander, M. (2000). Plant-promoted pyrene degradation in soil. Chemosphere, 40, 7–10.CrossRefPubMedGoogle Scholar
  29. Macci, C., Doni, S., Peruzzi, E., Bardella, S., Filippis, G., et al. (2013). A real-scale soil phytoremediation. Biodegradation, 24, 521–538.CrossRefPubMedGoogle Scholar
  30. Macci, C., Peruzzi, E., Doni, S., Poggio, G., & Masciandaro, G. (2016). The phytoremediation of an organic and inorganic polluted soil: A real scale experience. International Journal of Phytoremediation, 18, 378–386.CrossRefPubMedGoogle Scholar
  31. Maliszewska-Kordybach, B., & Smreczak, B. (2000). Ecotoxicological activity of soils polluted with polycyclic aromatic hydrocarbons (PAHS) – Effect on plants. Environmental Technology, 21, 1099–1110.CrossRefGoogle Scholar
  32. Marschner, P., Crowley, D., & Rengel, Z. (2011). Rhizosphere interactions between microorganisms and plants govern iron and phosphorus acquisition along the root axis – Model and research methods. Soil Biology and Biochemistry, 43, 883–894.CrossRefGoogle Scholar
  33. Martín, V. I., de la Haba, R. R., Ventosa, A., Congiu, E., Ortega-Calvo, J. J., & Moyá, M. L. (2014). Colloidal and biological properties of cationic single-chain and dimeric surfactants. Colloids and Surfaces B: Biointerfaces, 114, 247–254.CrossRefPubMedGoogle Scholar
  34. Micallef, S. A., Channer, S., Shiaris, M. P., & Colon-Carmona, A. (2009). Plant age and genotype impact the progression of bacterial community succession in the Arabidopsis rhizosphere. Plant Signaling and Behavior, 4, 777–780.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Miya, R. K., & Firestone, M. K. (2001). Enhanced phenanthrene biodegradation in soil by slender oat root exudates and root debris. Journal of Environmental Quality, 30, 1911–1918.CrossRefPubMedGoogle Scholar
  36. Nannipieri, P. (2006). Role of stabilised enzymes in microbial ecology and enzyme extraction from soil with potential applications in soil proteomics. Nucleic Acids and Proteins in Soil, 8, 75–94.CrossRefGoogle Scholar
  37. Newman, L. A., & Reynolds, C. M. (2004). Phytodegradation of organic compounds. Current Opinion in Biotechnology, 15, 225–230.CrossRefPubMedGoogle Scholar
  38. Nguyen, C. (2003). Rhizodeposition of organic C by plants: Mechanisms and controls. Agronomie, 23, 375–396.CrossRefGoogle Scholar
  39. Niqui-Arroyo, J. L., & Ortega-Calvo, J. J. (2007). Integrating biodegradation and electroosmosis for the enhanced removal of polycyclic aromatic hydrocarbons from creosote-polluted soils. Journal of Environmental Quality, 36, 1444–1451.CrossRefPubMedGoogle Scholar
  40. Niqui-Arroyo, J. L., & Ortega-Calvo, J. J. (2010). Effect of electrokinetics on the bioaccessibility of polycyclic aromatic hydrocarbons in polluted soils. Journal of Environmental Quality, 39, 1993–1998.CrossRefPubMedGoogle Scholar
  41. Niqui-Arroyo, J. L., Bueno-Montes, M., Posada-Baquero, R., & Ortega-Calvo, J. J. (2006). Electrokinetic enhancement of phenanthrene biodegradation in creosote-polluted clay soil. Environmental Pollution, 142, 326–332.CrossRefPubMedGoogle Scholar
  42. Niqui-Arroyo, J. L., Bueno-Montes, M., & Ortega-Calvo, J. J. (2011). Biodegradation of anthropogenic organic compounds in natural environments. In B. Xing, N. Senesi, & P. M. Huang (Eds.), Biophysico-chemical processes of anthropogenic organic compounds in environmental systems, IUPAC Series on Biophysico-Chemical Processes in Environmental Systems (Vol. 3, pp. 483–501). Chichester: Wiley.CrossRefGoogle Scholar
  43. Olson, P. E., Castro, A., Joern, M., DuTeau, N. M., Pilon-Smits, E. A. H., & Reardon, K. F. (2007). Comparison of plant families in a greenhouse phytoremediation study on an aged polycyclic aromatic hydrocarbon-contaminated soil. Journal of Environmental Quality, 36, 1461–1469.CrossRefPubMedGoogle Scholar
  44. Ortega-Calvo, J. J., & Alexander, M. (1994). Roles of bacterial attachment and spontaneous partitioning in the biodegradation of naphthalene initially present in nonaqueous-phase liquids. Applied and Environmental Microbiology, 60, 2643–2646.PubMedPubMedCentralGoogle Scholar
  45. Ortega-Calvo, J. J., & Saiz-Jimenez, C. (1998). Effect of humic fractions and clay on biodegradation of phenanthrene by a Pseudomonas fluorescens strain isolated from soil. Applied and Environmental Microbiology, 64, 3123–3126.PubMedPubMedCentralGoogle Scholar
  46. Ortega-Calvo, J. J., Marchenko, A. I., Vorobyov, A. V., & Borovick, R. V. (2003). Chemotaxis in polycyclic aromatic hydrocarbon-degrading bacteria isolated from coal-tar- and oil-polluted rhizospheres. FEMS Microbiology Ecology, 44, 373–381.CrossRefPubMedGoogle Scholar
  47. Ortega-Calvo, J. J., Molina, R., Jimenez-Sanchez, C., Dobson, P. J., & Thompson, I. P. (2011). Bacterial tactic response to silver nanoparticles. Environmental Microbiology Reports, 3, 526–534.CrossRefPubMedGoogle Scholar
  48. Ortega-Calvo, J. J., Tejeda-Agredano, M. C., Jimenez-Sanchez, C., Congiu, E., Sungthong, R., et al. (2013). Is it possible to increase bioavailability but not environmental risk of PAHs in bioremediation? Journal of Hazardous Materials, 261, 733–745.CrossRefPubMedGoogle Scholar
  49. Ortega-Calvo, J. J., Harmsen, J., Parsons, J. R., Semple, K. T., Aitken, M. D., et al. (2015). From bioavailability science to regulation of organic chemicals. Environmental Science and Technology, 49, 10255–10264.CrossRefPubMedGoogle Scholar
  50. Pandya, S., Iyer, P., Gaitonde, V., Parekh, T., & Desai, A. (1999). Chemotaxis of Rhizobium SP.S2 towards Cajanus cajan root exudate and its major components. Current Microbiology, 38, 205–209.CrossRefPubMedGoogle Scholar
  51. Parrish, Z. D., Banks, M. K., & Schwab, A. P. (2004). Effectiveness of phytoremediation as a secondary treatment for polycyclic aromatic hydrocarbons (PAHs) in composted soil. International Journal of Phytoremediation, 6, 119–137.CrossRefPubMedGoogle Scholar
  52. Parrish, Z. D., Banks, M. K., & Schwab, A. P. (2005). Effect of root death and decay on dissipation of polycyclic aromatic hydrocarbons in the rhizosphere of yellow sweet clover and tall fescue. Journal of Environmental Quality, 34, 207–216.CrossRefPubMedGoogle Scholar
  53. Paterson, E. (2003). Importance of rhizodeposition in the coupling of plant and microbial productivity. European Journal of Soil Science, 54, 741–750.CrossRefGoogle Scholar
  54. Phillips, L. A., Greer, C. W., & Germida, J. J. (2006). Culture-based and culture-independent assessment of the impact of mixed and single plant treatments on rhizosphere microbial communities in hydrocarbon contaminated flare-pit soil. Soil Biology and Biochemistry, 38, 2823–2833.CrossRefGoogle Scholar
  55. Reichenauer, T. G., & Germida, J. J. (2008). Phytoremediation of organic contaminants in soil and groundwater. ChemSusChem, 1, 708–717.CrossRefPubMedGoogle Scholar
  56. Reichenberg, F., & Mayer, P. (2006). Two complementary sides of bioavailability: Accessibility and chemical activity of organic contaminants in sediments and soils. Environmental Toxicology and Chemistry, 25, 1239–1245.CrossRefPubMedGoogle Scholar
  57. Rentz, J. A., Alvarez, P. J. J., & Schnoor, J. L. (2005). Benzo a pyrene co-metabolism in the presence of plant root extracts and exudates: Implications for phytoremediation. Environmental Pollution, 136, 477–484.CrossRefPubMedGoogle Scholar
  58. Resina-Pelfort, O., García-Junco, M., Ortega-Calvo, J. J., Comas-Riu, J., & Vives-Rego, J. (2003). Flow cytometry discrimination between bacteria and clay humic acid particles during growth-linked biodegradation of phenanthrene by Pseudomonas aeruginosa 19SJ. FEMS Microbiology Ecology, 43, 55–61.PubMedGoogle Scholar
  59. Ryan, P. R., Delhaize, E., & Jones, D. L. (2001). Function and mechanism of organic anion exudation from plant roots. Annual Review of Plant Physiology and Plant Molecular Biology, 52, 527–560.CrossRefPubMedGoogle Scholar
  60. Schachtman, D. P., & Shin, R. (2007). Nutrient sensing and signaling: NPKS. Annual Review of Plant Biology, 58, 47–69.CrossRefPubMedGoogle Scholar
  61. Semple, K. T., Doick, K. J., Jones, K. C., Burauel, P., Craven, A., & Harms, H. (2004). Defining bioavailability and bioaccessibility of contaminated soil and sediment is complicated. Environmental Science and Technology, 38, 228A–231A.CrossRefPubMedGoogle Scholar
  62. Sungthong, R., van West, P., Cantos, M., & Ortega-Calvo, J. J. (2015). Development of eukaryotic zoospores within polycyclic aromatic hydrocarbon (PAH)-polluted environments: A set of behaviors that are relevant for bioremediation. Science of the Total Environment, 511, 767–776.CrossRefPubMedGoogle Scholar
  63. Sungthong, R., Van West, P., Heyman, F., Jensen, D. F., & Ortega-Calvo, J. J. (2016). Mobilization of pollutant-degrading bacteria by eukaryotic zoospores. Environmental Science and Technology, 50, 7633–7640.CrossRefPubMedGoogle Scholar
  64. Suo, B., Chen, Q., Wu, W., Wu, D., Tian, M., et al. (2016). Chemotactic responses of Phytophthora sojae zoospores to amino acids and sugars in root exudates. Journal of General Plant Pathology, 82, 142–148.CrossRefGoogle Scholar
  65. Tejeda-Agredano, M. C., Gallego, S., Niqui-Arroyo, J. L., Vila, J., Grifoll, M., & Ortega-Calvo, J. J. (2011). Effect of interface fertilization on biodegradation of polycyclic aromatic hydrocarbons present in nonaqueous-phase liquids. Environmental Science and Technology, 45, 1074–1081.CrossRefPubMedGoogle Scholar
  66. Tejeda-Agredano, M. C., Gallego, S., Vila, J., Grifoll, M., Ortega-Calvo, J. J., & Cantos, M. (2013). Influence of sunflower rhizosphere on the biodegradation of PAHs in soil. Soil Biology and Biochemistry, 57, 830–840.CrossRefGoogle Scholar
  67. Tejeda-Agredano, M. C., Mayer, P., & Ortega-Calvo, J. J. (2014). The effect of humic acids on biodegradation of polycyclic aromatic hydrocarbons depends on the exposure regime. Environmental Pollution, 184, 435–442.CrossRefPubMedGoogle Scholar
  68. Velasco-Casal, P., Wick, L. Y., & Ortega-Calvo, J. J. (2008). Chemoeffectors decrease the deposition of chemotactic bacteria during transport in porous media. Environmental Science and Technology, 42, 1131–1137.CrossRefPubMedGoogle Scholar
  69. Vranova, V., Rejsek, K., Skene, K. R., Janous, D., & Formanek, P. (2013). Methods of collection of plant root exudates in relation to plant metabolism and purpose: A review. Journal of Plant Nutrition and Soil Science, 176, 175–199.CrossRefGoogle Scholar
  70. Walker, T. S., Bais, H. P., Grotewold, E., & Vivanco, J. M. (2003). Root exudation and rhizosphere biology. Plant Physiology, 132, 44–51.CrossRefPubMedPubMedCentralGoogle Scholar
  71. Yang, Q., Wang, X., & Shen, Y. (2013). Comparison of soil microbial community catabolic diversity between rhizosphere and bulk soil induced by tillage or residue retention. Journal of Soil Science and Plant Nutrition, 13, 187–199.Google Scholar
  72. Yi, H., & Crowley, D. E. (2007). Biostimulation of PAH degradation with plants containing high concentrations of linoleic acid. Environmental Science and Technology, 41, 4382–4388.CrossRefPubMedGoogle Scholar
  73. Zheng, X. Y., & Sinclair, J. B. (1996). Chemotactic response of Bacillus megaterium strain B153-2-2 to soybean root and seed exudates. Physiological and Molecular Plant Pathology, 48, 21–35.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Jose Julio Ortega-Calvo
    • 1
    Email author
  • Rosa Posada-Baquero
    • 1
  • José Luis Garcia
    • 1
  • Manuel Cantos
    • 1
  1. 1.Instituto de Recursos Naturales y Agrobiologia de Sevilla, CSICSevillaSpain

Personalised recommendations