Skip to main content
SpringerLink
Log in

Evaluation of constraints in bioremediation of weathered hydrocarbon-contaminated arid soils through microcosm biopile study

  • Original Paper
  • Published:
International Journal of Environmental Science and Technology Aims and scope Submit manuscript

Abstract

This research investigated the factors influencing bioremediation (biopile) of arid soils contaminated by weathered hydrocarbons. Five soils were thoroughly characterised to determine total petroleum hydrocarbons (TPH), their physicochemical properties and microbial diversity. Identified biopile-limiting factors are to be elevated petroleum hydrocarbon concentrations, high electrical conductivity and the magnitude of the recalcitrant hydrocarbon fraction. To optimise the biopile parameters, microcosm study was conducted which showed significant TPH reduction in three of five soils (BP-1, BP-2 and BP-4) but not in other two (BP-3 and BP-5), where BP-3 had a very high hydrocarbon concentration (123,757 mg kg−1) and BP-5 had a high proportion of recalcitrant hydrocarbons (>70 % of C29). Highest TPH removal (68 %) occurred in soil BP-2 and the lowest (5 %) in soil BP-3 over 56 days. Surfactant (Triton) addition, nutrient amendment or the soil dilution did not improve TPH degradation in soils BP-3 and BP-5. Phylogenetic analysis conducted during the remediation process found that hydrocarbon concentration and hydrocarbon fraction exerted the main effect on bacterial abundance, diversity and assemblage composition. At lower concentrations (~1000–4000 mg kg−1), bacterial diversity and abundance increased significantly, whilst decreased in higher concentrations. Although high TPH content and detection of TPH degraders, TPH biodegradation is limited in soil (BP-5) due to the presence of less soluble hydrocarbon fraction which indicated low TPH bioavailability (~7 %). Biopile could be applied as a technology to remediate three soils (BP-1, BP-2 and BP-4) but further modification of the biopile treatments required for other two soils BP-3 and BP-5.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adetutu EM, Smith RJ, Weber J, Aleer S, Mitchell JG, Ball AS, Juhasz AL (2013) A polyphasic approach for assessing the suitability of bioremediation for the treatment of hydrocarbon-impacted soil. Sci Total Environ 450–451:51–58. doi:10.1016/j.scitotenv.2013.02.007

    Article  Google Scholar 

  • Admon S, Green M, Avnimelech Y (2001) Biodegradation kinetics of hydrocarbons in soil during land treatment of oily sludge. Biorernediation J 5:193–209

    Article  CAS  Google Scholar 

  • Alexander M (2000) Aging, bioavailability, and overestimation of risk from environmental pollutants. Environ Sci Technol 34:4259–4265

    Article  CAS  Google Scholar 

  • Atlas RM, Bartha R (eds) (1998) Fundamentals and Applications. Microbial ecology. Benjamin/Cummings Publishing Company, Inc, California, pp 523–530

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Batelle (2007) Sediment toxicity of hydrocarbon fractions. Massachusetts Department of Environmental Protection Battelle, Duxbury, MA, USA

  • Beazley MJ et al (2012) Microbial community analysis of a coastal salt marsh affected by the Deepwater Horizon oil spill. PLoS ONE 7:e41305

    Article  CAS  Google Scholar 

  • Bell TH, Yergeau E, Martineau C, Juck D, Whyte LG, Greer CW (2011) Identification of nitrogen-incorporating bacteria in petroleum-contaminated arctic soils by using [15 N]DNA-based stable isotope probing and pyrosequencing. Appl Environ Microbiol 77:4163–4171. doi:10.1128/aem.00172-11

    Article  CAS  Google Scholar 

  • Beolchini F, Rocchetti L, Regoli F, Dell’Anno A (2010) Bioremediation of marine sediments contaminated by hydrocarbons: experimental analysis and kinetic modeling. J Hazard Mater 182:403–407. doi:10.1016/j.jhazmat.2010.06.047

    Article  CAS  Google Scholar 

  • Bernoth L, Firth I, McAllister P, Rhodes S (2000) Biotechnologies for remediation and pollution control in the mining industry. Miner Metallurg Proc 17:105–111

    CAS  Google Scholar 

  • Bouchez Naïtali M, Rakatozafy H, Marchal R, Leveau JY, Vandecasteele JP (1999) Diversity of bacterial strains degrading hexadecane in relation to the mode of substrate uptake. J Appl Microbiol 86:421–428. doi:10.1046/j.1365-2672.1999.00678.x

    Article  Google Scholar 

  • Brassington KJ et al (2007) Weathered hydrocarbon wastes: a risk management primer. Crit Rev Environ Sci Technol 37:199–232

    Article  CAS  Google Scholar 

  • Bull A (2011) Actinobacteria of the extremobiosphere. In: Horikoshi K (ed) Extremophiles handbook. Springer, Japan, pp 1203–1240. doi:10.1007/978-4-431-53898-1_58

    Chapter  Google Scholar 

  • Cerniglia CE, Sutherland JB (2010) Degradation of polycyclic aromatic hydrocarbons by fungi. In: Timmis K (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 2079–2110. doi:10.1007/978-3-540-77587-4_151

    Chapter  Google Scholar 

  • Chaillan F, Chaîneau CH, Point V, Saliot A, Oudot J (2006) Factors inhibiting bioremediation of soil contaminated with weathered oils and drill cuttings. Environ Pollut 144:255–265. doi:10.1016/j.envpol.2005.12.016

    Article  CAS  Google Scholar 

  • CSIRO (2011) http://www.csiro.au/science/arid-land-sustainability

  • Ehlers LJ, Luthy RG (2003) Peer reviewed: contaminant bioavailability in soil and sediment. Environ Sci Technol 37:295A–302A. doi:10.1021/es032524f

    Article  CAS  Google Scholar 

  • Ferguson SH, Franzmann PD, Revill AT, Snape I, Rayner JL (2003) The effects of nitrogen and water on mineralisation of hydrocarbons in diesel-contaminated terrestrial Antarctic soils. Cold Reg Sci Technol 37:197–212. doi:10.1016/S0165-232X(03)00041-7

    Article  Google Scholar 

  • Friedman SP (2005) Soil properties influencing apparent electrical conductivity: a review. Comput Electron Agric 46:45–70. doi:10.1016/j.compag.2004.11.001

    Article  Google Scholar 

  • Gardner WH (1986) Water content. In: Klute A (ed) Methods of soil analysis. Part 1. Physical and mineralogical methods, 2nd edn. Soil Science Society of America, Inc., Madison, WI

    Google Scholar 

  • Gargouri B, Karray F, Mhiri N, Aloui F, Sayadi S (2013) Bioremediation of petroleum hydrocarbons-contaminated soil by bacterial consortium isolated from an industrial wastewater treatment plant. J Chem Technol Biotechnol. doi:10.1002/jctb.4188

    Google Scholar 

  • Godoy-Faúndez A, Antizar-Ladislao B, Reyes-Bozo L, Camaño A, Sáez-Navarrete C (2008) Bioremediation of contaminated mixtures of desert mining soil and sawdust with fuel oil by aerated in-vessel composting in the Atacama region (Chile). J Hazard Mater 151:649–657. doi:10.1016/j.jhazmat.2007.06.038

    Article  Google Scholar 

  • Greer CW, Whyte LG, Niederberger TD (2010) Microbial communities in hydrocarbon-contaminated temperate, tropical, alpine, and polar soils. In: Timmis K (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 2313–2328. doi:10.1007/978-3-540-77587-4_168

    Chapter  Google Scholar 

  • Griebler C, Lueders T (2009) Microbial biodiversity in groundwater ecosystems. Freshw Biol 54:649–677

    Article  Google Scholar 

  • Guerin TF (2002) Heavy equipment maintenance wastes and environmental management in the mining industry. J Environ Manage 66:185–199

    Article  Google Scholar 

  • Harmsen J, Naidu R (2013) Bioavailability as a tool in site management. J Hazard Mater. doi:10.1016/j.jhazmat.2012.12.044

    Google Scholar 

  • Hazen T, Tien A, Worsztynowicz A, Altman D, Ulfig K, Manko T (2003) Biopiles for remediation of petroleum-contaminated soils: a polish case study. In: Sasek V, Glaser JA, Baveye P (eds) The utilization of bioremediation to reduce soil contamination: problems and solutions. Springer, pp 229–246

  • Hazen TC et al (2010) Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330:204–208

    Article  CAS  Google Scholar 

  • Hua Z, Song R, Du G, Li H, Chen J (2007) Effects of EDTA and Tween60 on biodegradation of n-hexadecane with two strains of Pseudomonas aeruginosa. Biochem Eng J 36:66–71. doi:10.1016/j.bej.2006.06.008

    Article  CAS  Google Scholar 

  • Huesemann MH, Hausmann TS, Fortman TJ (2002) Microbial factors rather than bioavailability limit the rate and extent of PAH biodegradation in aged crude oil contaminated model soils. Bioremediation J 6:321–336

    Article  CAS  Google Scholar 

  • Laha S, Tansel B, Ussawarujikulchai A (2009) Surfactant–soil interactions during surfactant-amended remediation of contaminated soils by hydrophobic organic compounds: a review. J Environ Manage 90:95–100

    Article  CAS  Google Scholar 

  • Liu Z, Liu J (2013) Evaluating bacterial community structures in oil collected from the sea surface and sediment in the northern Gulf of Mexico after the Deepwater Horizon oil spill. MicrobiologyOpen. doi:10.1002/mbo3.89

    Google Scholar 

  • Makadia TH, Adetutu EM, Simons KL, Jardine D, Sheppard PJ, Ball AS (2011) Re-use of remediated soils for the bioremediation of waste oil sludge. J Environ Manage 92:866–871

    Article  CAS  Google Scholar 

  • Manz W, Amann R, Ludwig W, Vancanneyt M, Schleifer K-H (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga–flavobacter–bacteroides in the natural environment. Microbiology 142:1097–1106. doi:10.1099/13500872-142-5-1097

    Article  CAS  Google Scholar 

  • Masakorala K, Yao J, Chandankere R, Liu H, Liu W, Cai M, Choi MM (2013) A combined approach of physicochemical and biological methods for the characterization of petroleum hydrocarbon-contaminated soil. Environ Sci Pollut Res 21(1). doi:10.1007/s11356-013-1923-3

  • Mason OU et al (2012) Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to Deepwater Horizon oil spill. ISME J 6:1715–1727

    Article  CAS  Google Scholar 

  • Militon C et al (2010) Bacterial community changes during bioremediation of aliphatic hydrocarbon-contaminated soil. FEMS Microbiol Ecol 74:669–681

    Article  CAS  Google Scholar 

  • Miller W, Miller D (1987) A micro pipette method for soil mechanical analysis. Commun Soil Sci Plant Anal 19:1–15

    Article  Google Scholar 

  • Mulligan C, Yong R, Gibbs B (2001) Surfactant-enhanced remediation of contaminated soil: a review. Eng Geol 60:371–380

    Article  Google Scholar 

  • Naidu R et al (2013) Towards bioavailability-based soil criteria: past, present and future perspectives. Environ Sci Pollut Res. doi:10.1007/s11356-013-1617-x

  • Nikolopoulou M, Kalogerakis N (2009) Biostimulation strategies for fresh and chronically polluted marine environments with petroleum hydrocarbons. J Chem Technol Biotechnol 84:802–807. doi:10.1002/jctb.2182

    Article  CAS  Google Scholar 

  • Noordman WH, Wachter JHJ, de Boer GJ, Janssen DB (2002) The enhancement by surfactants of hexadecane degradation by Pseudomonas aeruginosa varies with substrate availability. J Biotechnol 94:195–212. doi:10.1016/S0168-1656(01)00405-9

    Article  CAS  Google Scholar 

  • Prince R (2010) Eukaryotic hydrocarbon degraders. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, pp 2065–2078

  • Reid BJ, Stokes JD, Jones KC, Semple KT (2000) Nonexhaustive cyclodextrin-based extraction technique for the evaluation of PAH bioavailability. Environ Sci Technol 34:3174–3179

    Article  CAS  Google Scholar 

  • Rhykerd R, Crews B, McInnes K, Weaver R (1999) Impact of bulking agents, forced aeration, and tillage on remediation of oil-contaminated soil. Bioresour Technol 67:279–285

    Article  CAS  Google Scholar 

  • Riding MJ, Doick KJ, Martin FL, Jones KC, Semple KT (2013) Chemical measures of bioavailability/bioaccessibility of PAHs in soil: fundamentals to application. J Hazard Mater. doi:10.1016/j.jhazmat.2013.03.033

    Google Scholar 

  • Risdon GC, Pollard SJ, Brassington KJ, McEwan JN, Paton GI, Semple KT, Coulon F (2008) Development of an analytical procedure for weathered hydrocarbon contaminated soils within a UK risk-based framework. Anal Chem 80:7090–7096

    Article  CAS  Google Scholar 

  • Riser R (1998) Remediation of petroleum contaminated soils: biological, physical and chemical processes. Lewis Publisher, United States

    Book  Google Scholar 

  • Røberg S, Østerhus J, Landfald B (2011) Dynamics of bacterial community exposed to hydrocarbons and oleophilic fertilizer in high-Arctic intertidal beach. Polar Biol 34:1455–1465. doi:10.1007/s00300-011-1003-4

    Article  Google Scholar 

  • Rocchetti L, Beolchini F, Ciani M, Dell’Anno A (2011) Improvement of bioremediation performance for the degradation of petroleum hydrocarbons in contaminated sediments. Appl Environ Soil Sci 2011:1–8. Art ID 319657. doi:10.1155/2011/319657

    Article  Google Scholar 

  • Ros M, Rodríguez I, García C, Hernández T (2010) Microbial communities involved in the bioremediation of an aged recalcitrant hydrocarbon polluted soil by using organic amendments. Bioresour Technol 101:6916–6923. doi:10.1016/j.biortech.2010.03.126

    Article  CAS  Google Scholar 

  • Sanscartier D, Reimer K, Koch I, Laing T, Zeeb B (2009) An investigation of the ability of a 14C-labeled hydrocarbon mineralization test to predict bioremediation of soils contaminated with petroleum hydrocarbons. Bioremediation J 13:92–101

    Article  CAS  Google Scholar 

  • Saul DJ, Aislabie JM, Brown CE, Harris L, Foght JM (2005) Hydrocarbon contamination changes the bacterial diversity of soil from around Scott Base, Antarctica. FEMS Microbiol Ecol 53:141–155. doi:10.1016/j.femsec.2004.11.007

    Article  CAS  Google Scholar 

  • Semple KT, Morriss A, Paton G (2003) Bioavailability of hydrophobic organic contaminants in soils: fundamental concepts and techniques for analysis. Eur J Soil Sci 54:809–818

    Article  CAS  Google Scholar 

  • Semple KT, Doick KJ, Jones KC, Burauel P, Craven A, Harms H (2004) Peer reviewed: defining bioavailability and bioaccessibility of contaminated soil and sediment is complicated. Environ Sci Technol 38:228–231

    Article  Google Scholar 

  • Shastri S, Kamper S, Sonigra T, Hill T, Beales J (2012) Australia’s mining thirst GTL solution

  • Stenuit B, Eyers L, Schuler L, Agathos SN, George I (2008) Emerging high-throughput approaches to analyze bioremediation of sites contaminated with hazardous and/or recalcitrant wastes. Biotechnol Adv 26:561–575. doi:10.1016/j.biotechadv.2008.07.004

    Article  CAS  Google Scholar 

  • Stroud JL, Paton GI, Semple KT (2008) Linking chemical extraction to microbial degradation of 14C-hexadecane in soil. Environ Pollut 156:474–481. doi:10.1016/j.envpol.2008.01.018

    Article  CAS  Google Scholar 

  • Sutton NB et al (2013) Impact of long-term diesel contamination on soil microbial community structure. Appl Environ Microbiol 79:619–630. doi:10.1128/aem.02747-12

    Article  CAS  Google Scholar 

  • Teng Y, Luo Y, Sun M, Liu Z, Li Z, Christie P (2010) Effect of bioaugmentation by Paracoccus sp. strain HPD-2 on the soil microbial community and removal of polycyclic aromatic hydrocarbons from an aged contaminated soil. Bioresour Technol 101:3437–3443. doi:10.1016/j.biortech.2009.12.088

    Article  CAS  Google Scholar 

  • Tibbett M, George SJ, Davie A, Barron A, Milton N, Greenwood PF (2011) Just add water and salt: the optimisation of petrogenic hydrocarbon biodegradation in soils from semi-arid barrow Island, Western Australia. Water Air Soil Pollut 216:513–525

    Article  CAS  Google Scholar 

  • USEPA (1998) Biopiles. Office of the Underground Storage Tank, US Environmental Protection Agency. Publication # EPA 510-B-95-007. http://www.epa.gov/swerust1/cat/biopiles.htm

  • USEPA (2004) Treatment technologies for site cleanup annual status report (11th edn). Rep. No. EPA-542-R-03-009, Office of Solid Waste and Emergency Response US EPA, Washington, DC. http://www.epa.gov/tio/download/remed/asr/12/asr12_full_document.pdf

  • Voelkerding KV, Dames SA, Durtschi JD (2009) Next-generation sequencing: from basic research to diagnostics. Clin Chem 55:641–658

    Article  CAS  Google Scholar 

  • Volke-Sepúlveda TL, Gutiérrez-Rojas M, Favela-Torres E (2003) Biodegradation of hexadecane in liquid and solid-state fermentations by Aspergillus niger. Bioresour Technol 87:81–86. doi:10.1016/S0960-8524(02)00207-9

    Article  Google Scholar 

  • Walworth J, Woolard C, Braddock J, Reynolds C (1997) Enhancement and inhibition of soil petroleum biodegradation through the use of fertilizer nitrogen: an approach to determining optimum levels. Soil Sediment Contam 6:465–480

    Article  CAS  Google Scholar 

  • Wu J, Ju L-K (1998) Extracellular particles of polymeric material formed in n-hexadecane fermentation by Pseudomonas aeruginosa. J Biotechnol 59:193–202. doi:10.1016/S0168-1656(97)00150-8

    Article  CAS  Google Scholar 

  • Xu J, Deng H, Huang T, Song S (2014) Enhanced biodegradation of crude oil in contaminated soil by inoculation of hydrocarbon-degraders. Desalin Water Treat 52:5126–5135. doi:10.1080/19443994.2014.898433

    Article  CAS  Google Scholar 

  • Yeh C, Lin L-C (2003) Sorption and desorption kinetics of surfactants TX-100 and DPC on different fractions of soils. J Environ Sci Health A Tox Hazard Subst Environ Eng 38:1145

    Article  Google Scholar 

  • Yergeau E, Lawrence JR, Sanschagrin S, Waiser MJ, Korber DR, Greer CW (2012) Next-generation sequencing of microbial communities in the Athabasca River and its tributaries in relation to oil sands mining activities. Appl Environ Microbiol 78:7626–7637

    Article  CAS  Google Scholar 

  • Yeung AT, Gu Y-Y (2011) A review on techniques to enhance electrochemical remediation of contaminated soils. J Hazard Mater 195:11–29. doi:10.1016/j.jhazmat.2011.08.047

    Article  CAS  Google Scholar 

  • Zhang L, Xu Z (2008) Assessing bacterial diversity in soil. J Soils Sediments 8:379–388

    Article  CAS  Google Scholar 

  • Zhang G, Hu H, Sun W, Ni J (2009) Sorption of Triton X-100 on soil organic matter fractions: kinetics and isotherms. J Environ Sci 21:795–800. doi:10.1016/S1001-0742(08)62343-8

    Article  Google Scholar 

  • Zhang D-C, Mörtelmaier C, Margesin R (2012) Characterization of the bacterial archaeal diversity in hydrocarbon-contaminated soil. Sci Total Environ 421–422:184–196. doi:10.1016/j.scitotenv.2012.01.043

    Article  Google Scholar 

Download references

Acknowledgments

This research was funded and supported by BHP BIO Iron Ore, Western Australia through the Cooperative Research Centre for Contamination Assessment and Remediation of the Environment (CRC CARE), Adelaide, Australia.

Author information

Authors and Affiliations

  1. Centre for Environmental Risk Assessment and Remediation, University of South Australia, Mawson Lakes, SA, 5095, Australia

    K. Ramadass, E. Smith, T Palanisami, G. Mathieson, M. Megharaj & R. Naidu

  2. Cooperative Research Centre for Contamination Assessment and Remediation of the Environment, Mawson Lakes, SA, 5095, Australia

    P. Srivastava, M. Megharaj & R. Naidu

Authors
  1. K. Ramadass
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T Palanisami
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. G. Mathieson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. Srivastava
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Megharaj
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. R. Naidu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. Ramadass.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramadass, K., Smith, E., Palanisami, T. et al. Evaluation of constraints in bioremediation of weathered hydrocarbon-contaminated arid soils through microcosm biopile study. Int. J. Environ. Sci. Technol. 12, 3597–3612 (2015). https://doi.org/10.1007/s13762-015-0793-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13762-015-0793-2

Keywords

Search

Navigation