Skip to main content
SpringerLink
Log in

Biodegradation of n-Alkanes in Oil-Contaminated Bottom Sediments under Bioelectrochemical Stimulation

  • EXPERIMENTAL ARTICLES
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

Degradation of oil hydrocarbons artificially introduced into bottom sediments in a bioelectrochemical system of a membrane-free (silt) type was studied. Passive bioelectrochemical stimulation by means of electrodes connected by an external circuit with a resistance of 1 kΩ, with an average electric current of ~85 µA was found to cause an increase in degradation during two months from 23.0 to 57.9%. Contamination of bottom sediments with oil (1.32 g/kg) slightly decreased the current in the external circuit of the bioelectrochemical system. The relationship was revealed between the degree of oil degradation and predominant utilization of the lighter n-alkanes in the C14H30–C30H62 series, compared with both the original oil and the residual hydrocarbons of the control. An increase in the representation of the alkB alkane monooxygenase genes relative to the 16S rRNA gene in the total DNA isolated from the sediments was induced by the introduction of hexadecane, both in the case of electrochemical stimulation and in the control. The results may be of interest for the development of new methods of bioelectrochemical removal of organic pollutants from anaerobic environments.

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.

Similar content being viewed by others

REFERENCES

  1. Bose, S., Hochell, M.F., Jr., Gorby, Y.A., Kennedy, D.W., McCready, D.E., Madden, A.S., and Lower, B.H., Bioreduction of hematite nanoparticles by the dissimilatory iron reducing bacterium Shewanella oneidensis MR-1, Geochim. Cosmochim. Acta, 2009, vol. 73, no. 4, pp. 962–976.

    Article  CAS  Google Scholar 

  2. Bukliarevich, H.A., Gurinovich, A.S., Filonov, A.E., and Titok, M.A., Molecular genetic and functional analysis of the genes encoding alkane 1-monooxygenase synthesis in members of the genus Rhodococcus, Microbiology (Moscow), 2023, vol. 92, no. 2, pp. 242–255.

    Article  CAS  Google Scholar 

  3. Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M.W., Shipley, G.L., Vandesompele, J., and Wittwer C.T., The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments, Clin. Chem., 2009, vol. 55, no. 4, pp. 611–622.

    Article  CAS  PubMed  Google Scholar 

  4. Cabrera, J., Irfan, M., Dai, Y., Zhang, P., Zong, Y., and Liu, X., Bioelectrochemical system as an innovative technology for treatment of produced water from oil and gas industry‒a review, Chemosphere, 2021, vol. 285, p. 131428.

    Article  CAS  PubMed  Google Scholar 

  5. Chandrasekhar, K. and Venkata Mohan, S., Bio-electrochemical remediation of real field petroleum sludge as an electron donor with simultaneous power generation facilitates biotransformation of PAH: effect of substrate concentration, Bioresour. Technol., 2012, vol. 110, pp. 517–525.

    Article  CAS  PubMed  Google Scholar 

  6. Idris, M.O., Kim, H.-C., Yaqoob, A.A., and Ibrahim, M.N.M., Exploring the effectiveness of microbial fuel cell for the degradation of organic pollutants coupled with bio-energy generation, Sustain. Energy Technol. Assess., 2022, vol. 52, p. 102183.

    Google Scholar 

  7. Khmelevtsova, L.E., Sazykin, I.S., Sazykina, M.A., and Seliverstova, E.Y., Prokaryotic cytochromes p450 (review), Appl. Biochem. Microbiol., 2017, vol. 53, no. 4, pp. 401–409.

    Article  CAS  Google Scholar 

  8. Kondaveeti, S., Govindarajan, D., Mohanakrishna, G., Thatikayala, D., Abu-Reesh, I.M., Min, B., Nambi, I.M., Al-Raoush, R.I., and Aminabhavi, T.M., Sustainable bioelectrochemical systems for bioenergy generation via waste treatment from petroleum industries, Fuel, 2023, vol. 331, p. 125632.

    Article  CAS  Google Scholar 

  9. Lan, J., Wen, F., Ren, Y., Liu, G., Jiang, Y., Wang, Z., and Zhu, X., An overview of bioelectrokinetic and bioelectrochemical remediation of petroleum-contaminated soils, Environ. Sci. Technol., 2023, vol. 16, p. 100278.

    CAS  Google Scholar 

  10. Liang, R., Davidova, I.A., Teske, A., and Suflita, J.M., Evidence for the anaerobic biodegradation of higher molecular weight hydrocarbons in the Guaymas Basin, Int. Biodeterior. Biodegrad., 2023, vol. 181, p. 105621.

    Article  CAS  Google Scholar 

  11. Li, W.-W. and Yu, H.-Q., Stimulating sediment bioremediation with benthic microbial fuel cells, Biotechnol. Adv., 2015, vol. 33, pp. 1–12.

    Article  PubMed  Google Scholar 

  12. Lovley, D.R., Electrically conductive pili‒Biological function and potential applications in electronics, Curr. Opin. Electrochem., 2017, vol. 4, pp. 190–198.

    Article  CAS  Google Scholar 

  13. Marzocchi, U., Palma, E., Rossetti, S., Aulenta, F., and Scoma, A., Parallel artificial and biological electric circuits power petroleum decontamination‒the case of snorkel and cable bacteria, Water Res., 2020, vol. 173, p. 115520.

    Article  CAS  PubMed  Google Scholar 

  14. Mbadinga, S.M., Wang, L.-Y., Zhou, L., Liu, J.-F., Gu, J.-D., and Mu, B.-Z., Microbial communities involved in anaerobic degradation of alkanes, Int. Biodeterior. Biodegrad., 2011, vol. 65, pp. 1‒13.

    Article  CAS  Google Scholar 

  15. Mohanakrishna, G., Al-Raoush, R.I., and Abu-Reesh, I.M., Sewage enhanced bioelectrochemical degradation of petroleum hydrocarbons in soil environment through bioelectro-stimulation, Biotechnol. Rep., 2020, vol. 27, p. e00478.

    Article  Google Scholar 

  16. Nozhevnikova, A.N., Russkova, Y.I., Litti, Y.V., Parshina, S.N., Zhuravleva, E.A., and Nikitina, A.A., Syntrophy and interspecies electron transfer in methanogenic microbial communities, Microbiology (Moscow), 2020, vol. 89, no. 2, pp. 129–147.

    Article  CAS  Google Scholar 

  17. Paisse, S., Duran, R., Coulon, F., and Goni-Urriza, M., Are alkane hydroxylase genes (alkB) relevant to assess petroleum bioremediation processes in chronically polluted coastal sediments?, Appl. Microbiol. Biotechnol., 2011, vol. 92, pp. 835–844.

    Article  CAS  PubMed  Google Scholar 

  18. Powell, S.M., Ferguson, S.H., Bowman, J.P., and Snape, I., Using real-time PCR to assess changes in the hydrocarbon-degrading microbial community in antarctic soil during bioremediation, Microb. Ecol., 2006, vol. 52, pp. 523–532.

    Article  CAS  PubMed  Google Scholar 

  19. Prathiba, S., Kumar, P.S., and Vo, D.-V.N., Recent advancements in microbial fuel cells: A review on its electron transfer mechanisms, microbial community, types of substrates and design for bio-electrochemical treatment, Chemosphere, 2022, vol. 286, p. 131856.

    Article  CAS  PubMed  Google Scholar 

  20. Samkov, A.A., Chugunova, Yu.A., Kruglova, M.N., Moiseeva, E.V., Volchenko, N.N., Khudokormov, A.A., Samkova, S.M., and Karaseva, E.V., Decolorization of dyes in a bioelectrochemical system depending on the immobilization of Shewanella oneidensis MR-1 cells on the anode surface and electrical stimulation of an external circuit, Appl. Biochem. Microbiol., 2023, vol. 59, no. 2, pp. 198–205.

    Article  CAS  Google Scholar 

  21. Samkov, A.A., Dzhimak, S.S., Barishev, M.G., Volchenko, N.N., Khudokormov, A.A., Samkova, S.M., and Karaseva, E.V., The effect of water isotopic composition on Rhodococcus erythropolis biomass production, Biophysics, 2015, vol. 60, no. 1, pp. 107‒112.

    Article  CAS  Google Scholar 

  22. Shvets, D. and Vinogradova, S., Occurrence and genetic characterization of grapevine pinot gris virus in Russia, Plants, 2022, vol. 11 (8), no. 1061, pp. 1–15.

  23. Solyanikova, I.P. and Golovleva, L.A., Hexadecane and hexadecane-degrading bacteria: mechanisms of interaction, Microbiology (Moscow), 2019, vol. 88, no. 1, pp. 15–26.

    Article  CAS  Google Scholar 

  24. Tao, L., Song, M., and Jiang, G., Enhanced depolluting capabilities of microbial bioelectrochemical systems by synthetic biology, Synth. Syst. Biotechnol., 2023, vol. 8, pp. 341–348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Taylor, S., Wakem, M., Dijkman, G., Alsarraj, M., and Nguyen, M., A practical approach to RT-qPCR‒publishing data that conform to the MIQE guidelines, Methods, 2010, vol. 50, pp. S1–S5.

    Article  CAS  PubMed  Google Scholar 

  26. Tourova, T.P., Sokolova, D.Sh., Semenova, E.M., Poltaraus, A.B., and Nazina, T.N., Diversity of the AlkB genes of n-alkane biodegradation in thermophilic hydrocarbon-oxidizing bacteria of the Geobacillus, Parageobacillus, and Aeribacillus, Microbiology (Moscow), 2018, vol. 87, no. 3, pp. 301–307.

    Article  CAS  Google Scholar 

  27. Tucci, M., Viggi, C.C., Núnez, A.E., Schievano, A., Rabaey, K., and Aulenta, F., Empowering electroactive microorganisms for soil remediation—Challenges in the bioelectrochemical removal of petroleum hydrocarbons, Chem. Eng. J., 2021, vol. 419, p. 130008.

    Article  CAS  Google Scholar 

  28. Venkidusamy, K., Megharaj, M., Marzorati, M., Lockington, R., and Naidu, R., Enhanced removal of petroleum hydrocarbons using a bioelectrochemical remediation system with pre-cultured anodes, Sci. Total Environ., 2016, vol. 539, pp. 61–69.

    Article  CAS  PubMed  Google Scholar 

  29. Vodyanitskii, Y.N., Trofimov, S.Y., and Shoba, S.A., The influence of Fe(III) on oil biodegradation in excessively moistened soils and sediments, Euras. Soil Sci., 2015, vol. 48, no. 7, pp. 764–772.

    Article  CAS  Google Scholar 

  30. Voeikova, T.A., Emel’yanova, L.K., Novikova, L.M., Shakulov, R.S., Sidoruk, K.V., Smirnov, I.A., Il’in, V.K., Soldatov, P.E., Tyurin-Kuz’min, A.Yu., Smolenskaya, T.S., and Debabov, V.G., Intensification of bioelectricity generation in microbial fuel cells using Shewanella oneidensis MR-1 mutants with increased reducing activity, Microbiology (Moscow), 2013, vol. 82, no. 4, pp. 410–414.

    Article  CAS  Google Scholar 

  31. Wang, H., Lu, L., Mao, D., Huang, Z., Cui, Y., Jin, S., Zuo, Y., and Ren, Z.J., Dominance of electroactive microbiomes in bioelectrochemical remediation of hydrocarbon-contaminated soils with different textures, Chemosphere, 2019a, vol. 235, pp. 776–784.

    Article  CAS  PubMed  Google Scholar 

  32. Wang, H., Xing, L., Zhang, H., Gui, C., Jin, S., Lin, H., Li, Q., and Cheng, C., Key factors to enhance soil remediation by bioelectrochemical systems (BESs): a review, Chem. Eng. J., 2021, vol. 419, p. 129600.

    Article  CAS  Google Scholar 

  33. Wang, X., Wan, G., Shi, L., Gao, X., Zhang, X., Li, X., Zhao, J., Sha, B., and Huang, Z., Direct micro-electric stimulation alters phenanthrene-degrading metabolic activities of Pseudomonas sp. strain DGYH-12 in modified bioelectrochemical system, Environ. Sci. Pollut. Res., 2019b, pp. 31449–31462.

  34. Wasmund, K., Burns, K.A., Kurtböke, D.I., and Bourne, D.G., Novel alkane hydroxylase gene (alkB) diversity in sediments associated with hydrocarbon seeps in the Timor Sea, Australia, Appl. Environ. Microbiol., 2009, vol. 75, pp. 7391–7398.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Yuan, J.S., Reed, A., Chen, F., and Stewart, C.N., Jr., Statistical analysis of real-time PCR data, BMC Bioinformatics, 2006, vol. 7, no. 85, pp. 1‒15.

    Article  Google Scholar 

  36. Zhuravleva, E., Kovalev, A., Kovalev, D., Kotova, I., Shekhurdina, S., Laikova, A., Krasnovsky, A., Pygamov, T., Vivekanand, V., Li, L., He, C., and Litti, Y., Does carbon cloth really improve thermophilic anaerobic digestion performance on a larger scale? Focusing on statistical analysis and microbial community dynamics, J. Environ. Manage., 2023, vol. 341, p. 118124.

    Article  CAS  PubMed  Google Scholar 

Download references

ACKNOWLEDGMENTS

Chromatographic studies were carried out at the Ecological Analytical Center for Collective Research, Kuban State University.

The authors are grateful to prof. E.V. Karasev for kindly providing the strain Rhodococcus erythropolis VKM Ac-2017D.

Funding

The study was supported by the Russian Science Foundation, grant no. 22-24-00401, https://rscf.ru/project/22-24-00401/.

Author information

Authors and Affiliations

  1. Kuban State University, 350040, Krasnodar, Russia

    A. A. Samkov, N. N. Volchenko, T. N. Musorina, M. N. Kruglova, S. M. Samkova & A. A. Khudokormov

Authors
  1. A. A. Samkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. N. Volchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. N. Musorina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. N. Kruglova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. M. Samkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. A. Khudokormov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. A. Samkov.

Ethics declarations

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

Additional information

Translated by A. Bulaev

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Samkov, A.A., Volchenko, N.N., Musorina, T.N. et al. Biodegradation of n-Alkanes in Oil-Contaminated Bottom Sediments under Bioelectrochemical Stimulation. Microbiology 93, 314–323 (2024). https://doi.org/10.1134/S0026261723602804

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261723602804

Keywords:

Search

Navigation