Strategies to Increase Bioavailability and Uptake of Hydrocarbons

  • J. J. Ortega-Calvo
Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)


The biodegradation of hydrocarbons in the environment is often slow due to restricted bioavailability. Research performed during the last 20 years has shown possible pathways to increase the bioavailability of hydrocarbons without necessarily increasing the risk to the environment. Pollutant solubilization through (bio)surfactants, microbial transport, and attachment to pollutant interfaces can increase bioavailability, which translates into an enhancement of biodegradation rates. These strategies can not only be integrated into optimized bioremediation protocols that lead to lower decontamination endpoints in soils and sediments but also help to improve biodegradation in other environmental contexts, such as wastewater treatment and natural attenuation.



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. Akbari A, Ghoshal S (2015) Bioaccessible porosity in soil aggregates and implications for biodegradation of high molecular weight petroleum compounds. Environ Sci Technol 49:14368–14375CrossRefPubMedGoogle Scholar
  2. Akbari A, Rahim AA, Ehrlicher AJ, Ghoshal S (2016) Growth and attchment-facilitated entry of bacteria into submicrometer pores can enhance bioremediation and oil recovery in low-permeability and microporous media. Environ Sci Technol Lett 3:399–403CrossRefGoogle Scholar
  3. Alexander M (1991) Research needs in bioremediation. Environ Sci Technol 25:1972–1973CrossRefGoogle Scholar
  4. Banat IM, Franzetti A, Gandolfi I, Bestetti G, Martinotti MG, Fracchia L, Smyth TJ, Marchant R (2010) Microbial biosurfactants production, applications and future potential. Appl Microbiol Biotechnol 87:427–444CrossRefPubMedGoogle Scholar
  5. Bueno-Montes M, Springael D, Ortega-Calvo JJ (2011) Effect of a non-ionic surfactant on biodegradation of slowly desorbing PAHs in contaminated soils. Environ Sci Technol 45:3019–3026CrossRefPubMedGoogle Scholar
  6. Congiu E, Ortega-Calvo J-J (2014) Role of desorption kinetics in the rhamnolipid-enhanced biodegradation of polycyclic aromatic hydrocarbons. Environ Sci Technol 48:10869–10877CrossRefPubMedGoogle Scholar
  7. Congiu E, Parsons JR, Ortega-Calvo J-J (2015) Dual partitioning and attachment effects of rhamnolipid on pyrene biodegradation under bioavailability restrictions. Environ Pollut 205:378–384CrossRefPubMedGoogle Scholar
  8. Degryse F, Smolders E, Merckx R (2006) Labile Cd complexes increase Cd availability to plants. Environ Sci Technol 40:830–836CrossRefPubMedGoogle Scholar
  9. Ehlers LJ, Luthy RG (2003) Contaminant bioavailability in soil and sediment. Environ Sci Technol 37:295A–302ACrossRefPubMedGoogle Scholar
  10. Furuno S, Pazolt K, Rabe C, Neu TR, Harms H, Wick LY (2010) Fungal mycelia allow chemotactic dispersal of polycyclic aromatic hydrocarbon-degrading bacteria in water-unsaturated systems. Environ Microbiol 12:1391–1398PubMedGoogle Scholar
  11. Garcia-Junco M, De Olmedo E, Ortega-Calvo JJ (2001) Bioavailability of solid and non-aqueous phase liquid (NAPL)-dissolved phenanthrene to the biosurfactant-producing bacterium Pseudomonas aeruginosa 19SJ. Environ Microbiol 3:561–569CrossRefPubMedGoogle Scholar
  12. Garcia-Junco M, Gomez-Lahoz C, Niqui-Arroyo JL, Ortega-Calvo JJ (2003) Biodegradation- and biosurfactant-enhanced partitioning of polycyclic aromatic hydrocarbons from nonaqueous-phase liquids. Environ Sci Technol 37:2988–2996CrossRefPubMedGoogle Scholar
  13. Garon D, Sage L, Wouessidjewe D, Seigle-Murandi F (2004) Enhanced degradation of fluorene in soil slurry by Absidia cylindrospora and maltosyl-cyclodextrin. Chemosphere 56:159–166CrossRefPubMedGoogle Scholar
  14. Haderlein A, Legros R, Ramsay B (2001) Enhancing pyrene mineralization in contaminated soil by the addition of humic acids or composted contaminated soil. Appl Microbiol Biotechnol 56:555–559CrossRefPubMedGoogle Scholar
  15. Haftka JJH, Parsons JR, Govers HAJ, Ortega-Calvo JJ (2008) Enhanced kinetics of solid-phase microextraction and biodegradation of polycyclic aromatic hydrocarbons in the presence of dissolved organic matter. Environ Toxicol Chem 27:1526–1532CrossRefPubMedGoogle Scholar
  16. Jimenez-Sanchez C, Wick LY, Ortega-Calvo JJ (2012) Chemical effectors cause different motile behavior and deposition of bacteria in porous media. Environ Sci Technol 46:6790–6797CrossRefPubMedGoogle Scholar
  17. Jimenez-Sanchez C, Wick LY, Cantos M, Ortega-Calvo JJ (2015) Impact of dissolved organic matter on bacterial tactic motility, attachment, and transport. Environ Sci Technol 49:4498–4505CrossRefPubMedGoogle Scholar
  18. Kohlmeier S, Smits THM, Ford RM, Keel C, Harms H, Wick LY (2005) Taking the fungal highway: mobilization of pollutant-degrading bacteria by fungi. Environ Sci Technol 39:4640–4646CrossRefPubMedGoogle Scholar
  19. Krell T, Lacal J, Reyes-Darías JA, Jimenez-Sanchez C, Sungthong R, Ortega-Calvo JJ (2013) Bioavailability of pollutants and chemotaxis. Curr Opin Biotechnol 24:451–456CrossRefPubMedGoogle Scholar
  20. Lahlou M, Harms H, Springael D, Ortega-Calvo JJ (2000) Influence of soil components on the transport of polycyclic aromatic hydrocarbon-degrading bacteria through saturated porous media. Environ Sci Technol 34:3649–3656CrossRefGoogle Scholar
  21. Martín VI, de la Haba RR, Ventosa A, Congiu E, Ortega-Calvo JJ, Moyá ML (2014) Colloidal and biological properties of cationic single-chain and dimeric surfactants. Colloids Surf B: Biointerfaces 114:247–254CrossRefPubMedGoogle Scholar
  22. Marx RB, Aitken MD (2000) Bacterial chemotaxis enhances naphthalene degradation in a heterogeneous aqueous system. Environ Sci Technol 34:3379–3383CrossRefGoogle Scholar
  23. Niqui-Arroyo JL, Ortega-Calvo JJ (2007) Integrating biodegradation and electroosmosis for the enhanced removal of polycyclic aromatic hydrocarbons from creosote-polluted soils. J Environ Qual 36:1444–1451CrossRefPubMedGoogle Scholar
  24. Niqui-Arroyo JL, Ortega-Calvo JJ (2010) Effect of electrokinetics on the bioaccessibility of polycyclic aromatic hydrocarbons in polluted soils. J Environ Qual 39:1993–1998CrossRefPubMedGoogle Scholar
  25. Niqui-Arroyo JL, Bueno-Montes M, Posada-Baquero R, Ortega-Calvo JJ (2006) Electrokinetic enhancement of phenanthrene biodegradation in creosote-polluted clay soil. Environ Pollut 142:326–332CrossRefPubMedGoogle Scholar
  26. Niqui-Arroyo JL, Bueno-Montes M, Ortega-Calvo JJ (2011) Biodegradation of anthropogenic organic compounds in natural environments. In: Xing B, Senesi N, Huang PM (eds) Biophysico-chemical processes of anthropogenic organic compounds in environmental systems, IUPAC series on Biophysico-chemical processes in environmental systems, vol 3. Wiley, Chichester, pp 483–501CrossRefGoogle Scholar
  27. Ortega-Calvo JJ, Alexander M (1994) Roles of bacterial attachment and spontaneous partitioning in the biodegradation of naphthalene initially present in nonaqueous-phase liquids. Appl Environ Microbiol 60:2643–2646PubMedPubMedCentralGoogle Scholar
  28. Ortega-Calvo JJ, Saiz-Jimenez C (1998) Effect of humic fractions and clay on biodegradation of phenanthrene by a Pseudomonas fluorescens strain isolated from soil. Appl Environ Microbiol 64:3123–3126PubMedPubMedCentralGoogle Scholar
  29. Ortega-Calvo JJ, Birman I, Alexander M (1995) Effect of varying the rate of partitioning of phenanthrene in nonaqueous-phase liquids on biodegradation in soil slurries. Environ Sci Technol 29:2222–2225CrossRefPubMedGoogle Scholar
  30. Ortega-Calvo JJ, Fesch C, Harms H (1999) Biodegradation of sorbed 2,4-dinitrotoluene in a clay-rich, aggregated porous medium. Environ Sci Technol 33:3737–3742CrossRefGoogle Scholar
  31. Ortega-Calvo JJ, Marchenko AI, Vorobyov AV, Borovick RV (2003) Chemotaxis in polycyclic aromatic hydrocarbon-degrading bacteria isolated from coal-tar- and oil-polluted rhizospheres. FEMS Microbiol Ecol 44:373–381CrossRefPubMedGoogle Scholar
  32. Ortega-Calvo JJ, Molina R, Jimenez-Sanchez C, Dobson PJ, Thompson IP (2011) Bacterial tactic response to silver nanoparticles. Environ Microbiol Rep 3:526–534CrossRefPubMedGoogle Scholar
  33. Ortega-Calvo JJ, Tejeda-Agredano MC, Jimenez-Sanchez C, Congiu E, Sungthong R, Niqui-Arroyo JL, Cantos M (2013) Is it possible to increase bioavailability but not environmental risk of PAHs in bioremediation? J Hazard Mater 261:733–745CrossRefPubMedGoogle Scholar
  34. Ortega-Calvo J-J, Harmsen J, Parsons JR, Semple KT, Aitken MD, Ajao C, Eadsforth C, Galay-Burgos M, Naidu R, Oliver R, Peijnenburg WJGM, Roembke J, Streck G, Versonnen B (2015) From bioavailability science to regulation of organic chemicals. Environ Sci Technol 49:10255–10264CrossRefPubMedGoogle Scholar
  35. Ortega-Calvo JJ, Jimenez-Sanchez C, Pratarolo P, Pullin H, Scott TB, Thompson IP (2016) Tactic response of bacteria to zero-valent iron nanoparticles. Environ Pollut 213:438–445CrossRefPubMedGoogle Scholar
  36. Reichenberg F, Mayer P (2006) Two complementary sides of bioavailability: accessibility and chemical activity of organic contaminants in sediments and soils. Environ Toxicol Chem 25:1239–1245CrossRefPubMedGoogle Scholar
  37. Resina-Pelfort O, García-Junco M, Ortega-Calvo JJ, 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 Microbiol Ecol 43:55–61PubMedGoogle Scholar
  38. Semple KT, Doick KJ, Jones KC, Burauel P, Craven A, Harms H (2004) Defining bioavailability and bioaccessibility of contaminated soil and sediment is complicated. Environ Sci Technol 38:228A–231ACrossRefPubMedGoogle Scholar
  39. Shi L, Harms H, Wick LY (2008) Electroosmotic flow stimulates the release of alginate-bound phenanthrene. Environ Sci Technol 42:2105–2110CrossRefPubMedGoogle Scholar
  40. Sungthong R, van West P, Cantos M, Ortega-Calvo JJ (2015) Development of eukaryotic zoospores within polycyclic aromatic hydrocarbon (PAH)-polluted environments: a set of behaviors that are relevant for bioremediation. Sci Total Environ 511:767–776CrossRefPubMedGoogle Scholar
  41. Sungthong R, Van West P, Heyman F, Jensen DF, Ortega-Calvo JJ (2016) Mobilization of pollutant-degrading bacteria by eukaryotic zoospores. Environ Sci Technol 50:7633–7640CrossRefPubMedGoogle Scholar
  42. Tejeda-Agredano MC, Gallego S, Niqui-Arroyo JL, Vila J, Grifoll M, Ortega-Calvo JJ (2011) Effect of interface fertilization on biodegradation of polycyclic aromatic hydrocarbons present in nonaqueous-phase liquids. Environ Sci Technol 45:1074–1081CrossRefPubMedGoogle Scholar
  43. Tejeda-Agredano MC, Gallego S, Vila J, Grifoll M, Ortega-Calvo JJ, Cantos M (2013) Influence of sunflower rhizosphere on the biodegradation of PAHs in soil. Soil Biol Biochem 57:830–840CrossRefGoogle Scholar
  44. Tejeda-Agredano MC, Mayer P, Ortega-Calvo JJ (2014) The effect of humic acids on biodegradation of polycyclic aromatic hydrocarbons depends on the exposure regime. Environ Pollut 184:435–442CrossRefPubMedGoogle Scholar
  45. Uyttebroek M, Breugelmans P, Janssen M, Wattiau P, Joffe B, Karlson U, Ortega-Calvo JJ, Bastiaens L, Ryngaert A, Hausner M, Springael D (2006a) Distribution of the Mycobacterium community and polycyclic aromatic hydrocarbons (PAHs) among different size fractions of a long-term PAH-contaminated soil. Environ Microbiol 8:836–847CrossRefPubMedGoogle Scholar
  46. Uyttebroek M, Ortega-Calvo JJ, Breugelmans P, Springael D (2006b) Comparison of mineralization of solid-sorbed phenanthrene by polycyclic aromatic hydrocarbon (PAH)-degrading Mycobacterium spp. and Sphingomonas spp. Appl Microbiol Biotechnol 72:829–836CrossRefPubMedGoogle Scholar
  47. Velasco-Casal P, Wick LY, Ortega-Calvo JJ (2008) Chemoeffectors decrease the deposition of chemotactic bacteria during transport in porous media. Environ Sci Technol 42:1131–1137CrossRefPubMedGoogle Scholar
  48. Yi H, Crowley DE (2007) Biostimulation of PAH degradation with plants containing high concentrations of linoleic acid. Environ Sci Technol 41:4382–4388CrossRefPubMedGoogle Scholar
  49. Zhang M, Shen XF, Zhang HY, Cai F, Chen WX, Gao Q, Ortega-Calvo JJ, Tao S, Wang XL (2016) Bioavailability of phenanthrene and nitrobenzene sorbed on carbonaceous materials. Carbon 110:404–413CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Instituto de Recursos Naturales y Agrobiologia de Sevilla, CSICSevillaSpain

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