Skip to main content
SpringerLink
Log in

Experimental thawing events enhance petroleum hydrocarbons attenuation and enzymatic activities in polluted temperate soils

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

Abstract

Polluted soils in temperate regions are frequently exposed to seasonal freezing and thawing events during which the soil biological properties are expected to change in response to the associated temperature variations. In this study, we investigated the influence of freeze–thaw events on enzymatic activities and natural attenuation of petroleum hydrocarbons in temperate soils with varying pollution profiles. Four soils [clean natural, Diesel amended (DAS), Crude-oil amended (COAS), and aged oil polluted] were subjected to ten freeze–thaw temperature regimes ranging from − 20 to + 20 °C for 45 days. The soil enzymatic activities and fractional petroleum hydrocarbon analysis were conducted using spectrophotometry and gas chromatography–mass spectrometry, respectively. After the incubation period, freezing resulted in decreased enzyme (lipase and dehydrogenase) activities in both clean and polluted soils, while thawing events compensated for the enzymatic losses that occurred during the preceding freezing phase. Fractional hydrocarbon analysis revealed that there was a switch from active removal of light- to medium-chain hydrocarbons (C10–C23) in the short-term polluted soils (DAS and COAS) during the freezing phase to rapid degradation of the heavier nonvolatile hydrocarbon fractions (C23–C34) during the thawing phase, and the long-term polluted soil had lower hydrocarbon removal rates than the short-term polluted soils. The relationship between the natural attenuation of hydrocarbons in the oil polluted soils and incubation temperatures was linear in the short- and long-term petroleum polluted soils.

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

Similar content being viewed by others

References

  • Abellan MA, Baena CW, Morote FAG, Cordoba MIP, Perez DC (2011) Influence of the soil storage method on soil enzymatic activities in Mediterranean forest soils. Plant Soil Environ 20(3):379–388

    Google Scholar 

  • Abena MTB, Li T, Shah MN, Zhong W (2019) Biodegradation of total petroleum hydrocarbons (TPH) in highly contaminated soils by natural attenuation and bioaugmentation. Chemosphere 234:864–874

    Article  Google Scholar 

  • Aislabie J, Saul DJ, Foght JM (2006) Bioremediation of hydrocarbon-contaminated polar soils. Extremophiles 10(3):171–179

    Article  CAS  Google Scholar 

  • Alrumman SA, Standing DB, Paton GI (2015) Effects of hydrocarbon contamination on soil microbial community and enzyme activity. J King Saud UnivScie 27(1):31–41

    Article  Google Scholar 

  • Bajagain R, Gautam P, Jeong S (2020) Degradation of petroleum hydrocarbons in unsaturated soil and effects on subsequent biodegradation by potassium permanganate. Environ Geochem Health 42:1705–1714

    Article  CAS  Google Scholar 

  • Blagodatskaya E, Blagodatsky S, Khomyakov N (2016) Temperature sensitivity and enzymatic mechanisms of soil organic matter decomposition along an altitudinal gradient on Mount Kilimanjaro. Sci Rep 6:22240

    Article  CAS  Google Scholar 

  • Børresen MH, Barnes DL, Rike AG (2007) Repeated freeze-thaw cycles and their effects on mineralization of hexadecane and phenanthrene in cold climate soils. Cold RegSciTechnol 49(3):215–225

    Google Scholar 

  • Buddhadasa C, Barone S, Bigger S, Orbell J (2001) Extraction of hydrocarbons from clay soils by sonication and soxhlet techniques. Sekiyu Gakkaishi J Jpn Pet Inst 44(6):378–383

    Article  CAS  Google Scholar 

  • Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil BiolBiochem 58:216–234

    Article  CAS  Google Scholar 

  • Chandra S, Sharma R, Singh K, Sharma A (2013) Application of bioremediation technology in the environment contaminated with petroleum hydrocarbon. Ann Microbiol 63:417–431

    Article  CAS  Google Scholar 

  • Chang W, Klemm S, Beaulieu C, Hawari J, Whyte L, Ghoshal S (2011) Petroleum hydrocarbon biodegradation under seasonal freeze-thaw soil temperature regimes in contaminated soils from a sub-arctic site. Environ SciTechnol 45(3):1061–1066

    Article  CAS  Google Scholar 

  • Chen W, Li J, Sun X, Min J, Hu X (2017) High efficiency degradation of alkanes and crude oil by a salt-tolerant bacterium Dietzia species CN-3. IntBiodeteriorBiodegrad 118:110–118

    CAS  Google Scholar 

  • Chikere CB, Okpokwasili GC, Chikere BO (2011) Monitoring of microbial hydrocarbon remediation in the soil. Biotech 1:117–138

    Google Scholar 

  • de Abreu-Mota MA, de MouraBarboza CA, Bícego MC, Martins CC (2016) Sedimentary biomarkers along a contamination gradient in a human-impacted sub-estuary in Southern Brazil: a multi-parameter approach based on spatial and seasonal variability. Chemosphere 103:156–163

    Article  Google Scholar 

  • Dong YW, Somero GN (2009) Temperature adaptation of cytosolic malate dehydrogenases of limpets (genus Lottia): differences in stability and function due to minor changes in sequences correlate with biogeographic and vertical distributions. J Exp Bio 212:169–177

    Article  CAS  Google Scholar 

  • Dzionek A, Dzik J, Wojcieszyńska D, Guzik U (2018) Fluorescein diacetate hydrolysis using the whole biofilm as a sensitive tool to evaluate the physiological state of immobilized bacterial cells. Catalysts 8:434

    Article  Google Scholar 

  • Ekperusi OA, Aigbodion FI (2015) Bioremediation of petroleum hydrocarbons from crude oil contaminated soil with the earthworm, Hyperiodrilus africanus. Biotech 3:957–965

    Google Scholar 

  • Eriksson M, Ka JO, Mohn WW (2001) Effects of low temperature and freeze-thaw cycles on hydrocarbon biodegradation in Arctic tundra soil. Appl Environ Microbiol 67(11):5107–5112

    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 RegSciTechnol 37:197–212

    Google Scholar 

  • Gheju M (2011) Kinetics of hexavalent chromium removal with scrap iron in continuous-flow system. Chemical Bulletin of Politehnica 56(70):1–7

    Google Scholar 

  • Gkorezis P, Daghio M, Franzetti A, Van Hamme JD, Sillen W, Vangronsveld J (2016) The interaction between plants and bacteria in the remediation of petroleum hydrocarbons: an environmental perspective. Front Microbiol 7:1836

    Article  Google Scholar 

  • Guo WL, Shi HB, Ma JJ, Zhang YJ, Wang J, Shu WJ, Zhang ZY (2013) Basic features of climate change in North China during 1961–2010. Adv Climate Change Res 4(2):73–83

    Article  Google Scholar 

  • Han L, Tsunekawa A, Tsubo M (2010) Monitoring near-surface soil freeze–thaw cycles in northern China and Mongolia from 1998 to 2007. Int J Appl Earth ObsGeoinf 12(5):375–384

    Google Scholar 

  • Henry A (2007) Soil freeze–thaw cycle experiments : Trends, methodological weaknesses and suggested improvements. Soil BiolBiochem 39:977–986

    Article  CAS  Google Scholar 

  • Holden P, LaMontagne M, Bruce A, Miller WG, Lindow SE (2002) Assessing the role of Pseudomonas aeruginosa surface-active gene expression in hexadecane biodegradation in sand. Appl Environ Microb 68:2509–2518

    Article  CAS  Google Scholar 

  • Joseph B, Shrivastava N, Ramteke PW (2012) Extracellular cold-active lipase of Microbacterium luteolum isolated from Gangotri glacier, western Himalaya: isolation, partial purification and characterization. J Genet EngBiotechnol 10(1):137–144

    CAS  Google Scholar 

  • Kaczyńska G, Borowik A, Wyszkowska J (2015) Soil Dehydrogenases as an indicator of contamination of the environment with petroleum products. Water Air Soil Pollut 226:372–376

    Article  Google Scholar 

  • Kim J, Lee AH, Chang W (2018) Enhanced bioremediation of nutrient-amended, petroleum hydrocarbon-contaminated soils over a cold-climate winter: the rate and extent of hydrocarbon biodegradation and microbial response in a pilot-scale biopile subjected to natural seasonal freeze-thaw. Sci Total Environ 612:903–913

    Article  CAS  Google Scholar 

  • Koshlaf E, Ball AS (2017) Soil bioremediation approaches for petroleum hydrocarbon polluted environments. AIMS Microbiol 3(1):25–49

    Article  CAS  Google Scholar 

  • Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54(3):305–315

    Article  CAS  Google Scholar 

  • Maletić SP, Dalmacija BD, Roncevic SD, Agbaba JR, Perovic SDU (2011) Impact of hydrocarbon type, concentration and weathering on its biodegradability in soil. J Environ Sci Health, Part A 46:1042–1049

    Article  Google Scholar 

  • Margesin R (2005) Determination of enzyme activities in contaminated soil. In: Margesin R, Schinner F (eds) Soil biology: manual for soil analysis, vol 5. Springer-Verlag, Berlin Heidelberg, pp 309–320

    Google Scholar 

  • Margesin R, Zimmerbauer A, Schinner F (2000) Monitoring of bioremediation by soil biological activities. Chemosphere 40(4):339–346

    Article  CAS  Google Scholar 

  • Margesin R, Feller G, Hämmerle M, Stegner U, Schinner F (2002) A colorimetric method for the determination of lipase activity in soil. Biotech Lett 24:27–33

    Article  CAS  Google Scholar 

  • Margesin R, Hammerle M, Tscherko D (2007) Micobial activity and community composition during bioremediation of diesel-oil contaminated soil: effects of hydrocarbon concentration, fertilizers and incubation time. MicrobEcol 55:259–269

    Google Scholar 

  • McKew BA, Coulon F, Osborn AM, Timmis KN, McGenity TJ (2007) Determining the identity and roles of oil-metabolizing marine bacteria from the Thames estuary. UK Environ Microbiol 9:165–176

    Article  CAS  Google Scholar 

  • Michael K, Wasswa J, Kasozi G (2016) Removal efficiency of total petroleum hydrocarbons from water by Pseudomonas aeruginosa: a case of lake albert. Uganda J BioremedBiodeg 7:337–341

    Google Scholar 

  • Miura M, Jones TG, Hill PW, Jones DL (2019) Freeze-thaw and dry-wet events reduce microbial extracellular enzyme activity, but not organic matter turnover in an agricultural grassland soil. Appl Soil Ecol 144:196–199

    Article  Google Scholar 

  • Mrozik A, Piotrowska-Seget Z (2010) Bioaugmentation as a strategy for cleaning up of soils contaminated with aromatic compounds. Microbiol Res 165(5):363–375

    Article  CAS  Google Scholar 

  • Naga Raju M, Golla N, Vengatampalli R (2016) Soil Physicochemical Properties Soil Enzymes 2016:5–10

    Google Scholar 

  • Nikrad MP, Kerkhof LJ, Max MH (2016) The subzeromicrobiome : microbial activity in frozen and thawing soils. FEMS MicrobiolEcol 92(6):1–16

    Google Scholar 

  • Razavi BS, Blagodatskaya E, Kuzyakov Y (2015) Nonlinear temperature sensitivity of enzyme kinetics explains canceling effect—a case study on loamy haplicLuvisol. Front Microbiol 6:1126

    Article  Google Scholar 

  • Robinson PK (2015) Enzymes: principles and biotechnological applications. Essays Biochem 59:1–41

    Article  Google Scholar 

  • Rončević S, Dalmacija B, Ivančev-Tumbas I, Tričković J, Petrović O, Klašnja M, Agbaba J (2005) Kinetics of degradation of hydrocarbons in the contaminated soil layer. Archives of Environ ContamToxicol 49(1):27–36

    Article  Google Scholar 

  • Schnurer J, Rosswall T (1982) Fluorescein diacetate hydrolysis as a measure of total microbial activity in soil and litter. Appl Environ Microbiol 43:1256–1261

    Article  CAS  Google Scholar 

  • Sihag S, Pathak H, Jaroli DP (2014) Factor affecting the rate of biodegradation of polyaromatic hydrocarbons. Int J Pure ApplBiosci 2:185–202

    Google Scholar 

  • Smith JL, Halvorson JJ, Bolton H (2002) Soil properties and microbial activity across a 500m elevation gradient in a semi-arid environment. Soil BiolBiochem 34:1749–1757

    Article  CAS  Google Scholar 

  • Steinweg JM, Jagadamma S, Frerichs J, Mayes MA (2013) Activation energy of extracellular enzymes in soils from different biomes. PLoS ONE 8(3):e59943

    Article  CAS  Google Scholar 

  • Trasar-Cepeda C, Leiros MC, Seoane S, Gil-Sotres F (2000) Limitations of soil enzymes as indicators of soil pollution. Soil BiolBiochem 32:1867–1875

    Article  CAS  Google Scholar 

  • Truskewycz A, Gundry TD, Khudur LS, Kolobaric A, Taha M, Aburto-Medina A, Ball AS, Shahsavari E (2019) Petroleum hydrocarbon contamination in terrestrial ecosystems-fate and microbial responses. Molecules 24(18):3400

    Article  CAS  Google Scholar 

  • Varjani SJ, Upasani VN (2017) A new look on factors affecting microbial degradation of petroleum hydrocarbon pollutants. IntBiodeteriorBiodegrad 120:71–83

    CAS  Google Scholar 

  • Wu M, Dick WA, Li W, Wang X, Yang Q, Wang T, Chen L (2016) Bioaugmentation and biostimulation of hydrocarbon degradation and the microbial community in a petroleum-contaminated soil. IntBiodeteriorBiodegrad 107:158–164

    CAS  Google Scholar 

  • Yang SZ, Jin HJ, Wei Z, He RX, Ji YJ, Li XM (2009) Bioremediation of oil spills in cold environments: a review. Pedosphere 19(3):371–381

    Article  CAS  Google Scholar 

  • Yao Y, Huang GH, An CJ, Cheng GH, Wei J (2017) Effects of freeze-thawing cycles on desorption behaviors of PAH-contaminated soil in the presence of a biosurfactant a case study in western Canada. Environmental Science: Processes and Impacts 19(6):874–882

    CAS  Google Scholar 

  • Zekri A, Omar C (2005) Effect of temperature on biodegradation of crude oil. Energy Sources Part A 27:233–244

    Article  CAS  Google Scholar 

  • Zhou J, Huang R, Cheng S, Tang J, Fan H (2018) Effects of bacterial-feeding nematodes and organic matter on microbial activity and oil degradation in contaminated soil. Environ SciPollut Res 25:35614–35622

    Article  CAS  Google Scholar 

Download references

Acknowledgement

The authors are grateful for the financial support from the National Water Pollution Control and Treatment Science and Technology Major Project (No. 2018ZX07109-003) of China. The first author is grateful to the Petroleum Development Trust Fund, Nigeria, for the doctoral scholarship award.

Author information

Authors and Affiliations

  1. Key Laboratory of Groundwater Resources and Environment, Ministry of Education, College of New Energy and Environment, Jilin University, Changchun, 130021, China

    C. J. Okonkwo, N. Liu, J. Li & A. Ahmed

Authors
  1. C. J. Okonkwo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. Liu.

Additional information

Editorial responsibility: Samareh Mirkia.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 71 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Okonkwo, C.J., Liu, N., Li, J. et al. Experimental thawing events enhance petroleum hydrocarbons attenuation and enzymatic activities in polluted temperate soils. Int. J. Environ. Sci. Technol. 19, 1185–1196 (2022). https://doi.org/10.1007/s13762-021-03175-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13762-021-03175-8

Keywords

Search

Navigation