Low CO2 footprint remediation of oil-contaminated soil in a sediment microbial fuel cell

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Abstract

Abstract. Active study of electrocatalytic properties of prokaryotes in the last 30 years has led to the creation of a new field of biotechnology – electricity generation in microbial fuel or electrolytic cells, where microbial cells act as biocatalysts of anodic or cathodic processes consuming organic matter or forming biomass and substances with added value during electrotrophic fixation of CO2. The most economically promising is the use of microbial fuel cells (MFC) for wastewater treatment and in bioremediation processes. Recently, the prospects for the introduction of MFC or stimulation of electroactive microbial communities for the purification of oil-contaminated anaerobic layers of soils and marine sediments have been considered. However, this version of the technology has a number of significant technical limitations. We describe a laboratory sedimentary MFC with a bioanode and biocathode inoculated with oil-contaminated soil, which for 210 days of continuous operation was the only source of power supply for an autonomous sensor for monitoring ambient air parameters. Electric current generation in the MFC was accompanied by the destruction of hydrocarbons in contaminated soil and the formation of various microbial populations in the anaerobic soil layer, at the anode and at the cathode, in which potential oil destructors, electrogens and electrotrophs dominated, respectively. At the same time, the release of CO2 against the background of ambient air was minimal, which indicates the formation of an effective gas filter in the MFC. Short-term incubation of the MFC in field conditions revealed a significant effect of temperature fluctuations on the physicochemical parameters of the device, its performance and the composition of the cathode microbial population. We consider in detail the changes in the phylogenetic and physiological diversity of microbial populations of different zones of the sedimentary MFC during its operation, and also outline the prospects and problems of the practical application of such systems for bioremediation of oil-contaminated soil.

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About the authors

G. S. Klyushin

Federal Research Center of Biotechnology of the Russian Academy of Sciences

Email: sngavrilov@gmail.com

S.N. Winogradsky Institute of Microbiology

Russian Federation, 119071, Moscow

A. S. Gogov

Federal Research Center of Biotechnology of the Russian Academy of Sciences; National Research Center “Kurchatov Institute”

Email: sngavrilov@gmail.com

S.N. Winogradsky Institute of Microbiology

Russian Federation, 119071, Moscow; 123098, Moscow

A. E. Kolonsky

Federal Research Center of Biotechnology of the Russian Academy of Sciences; Skolkovo Institute of Science and Technology

Email: sngavrilov@gmail.com

S.N. Winogradsky Institute of Microbiology, Center for Molecular and Cellular Biology

Russian Federation, 119071, Moscow; 121205, Moscow

A. R. Stroeva

Lomonosov Moscow State University

Email: sngavrilov@gmail.com

Faculty of Biology

Russian Federation, 119234, Moscow

I. M. Elizarov

Federal Research Center of Biotechnology of the Russian Academy of Sciences

Email: sngavrilov@gmail.com

S.N. Winogradsky Institute of Microbiology

Russian Federation, 119071, Moscow

A. A. Klyukina

Federal Research Center of Biotechnology of the Russian Academy of Sciences

Email: sngavrilov@gmail.com

S.N. Winogradsky Institute of Microbiology

Russian Federation, 119071, Moscow

S. N. Gavrilov

Federal Research Center of Biotechnology of the Russian Academy of Sciences

Author for correspondence.
Email: sngavrilov@gmail.com

S.N. Winogradsky Institute of Microbiology

Russian Federation, 119071, Moscow

References

  1. Атлас почв Российской Федерации. https://soil-db.ru/soilatlas/razdel-3-pochvy-rossiyskoy-federacii/chernozemy-vyshchelochennye-i-opodzolennye?ysclid=m2ask93lwv52646867. Accessed November 8, 2024.
  2. Губернский Ю. Д., Калинина Н. В., Гапонова Е. Б., Банин И. М. Обоснование допустимого уровня содержания диоксида углерода в воздухе помещений жилых и общественных зданий // Гигиена и санитария. 2014. Т. 6. С. 37–41.
  3. Кулагина Г. М., Кулагин С. С., Ключникова М. Ю. Мониторинг нефтяного загрязнения Винновской рощи // Успехи современного естествознания. 2012. № 10. С. 90.
  4. Меркель А. Ю., Тарновецкий И. Ю., Подосокорская О. А., Тощаков С. В. Анализ систем праймеров на ген 16S рРНК для профилирования термофильных микробных сообществ // Микробиология. 2019. Т. 88. С. 671–680. https://doi.org/10.1134/S0026365619060119
  5. Merkel A. Y., Tarnovetskii I. Y., Podosokorskaya O. A., Toshchakov S. V. Analysis of 16S rRNA primer systems for profiling of thermophilic microbial communities // Microbiology (Moscow). 2019. V. 88. P. 671–680. https://doi.org/10.1134/S0026261719060110
  6. Соколова Т. А., Толпешта И. И., Трофимов С. Я. Почвенная кислотность. Кислотно-основная буферность почв. Соединения алюминия в твердой фазе почвы и в почвенном растворе. Тула: Гриф и К, 2012. 124 с.
  7. Фёдорова Ю. А., Ахметова Г. И., Коржова Л. Ф., Ягафарова Г. Г. Изучение биодеструкции органических поллютантов ароматического ряда // Вестн. технологического университета. 2017. Т. 20. С. 143–146.
  8. Ambaye T. G., Vaccari M., Franzetti A., Prasad S., Formicola F., Rosatelli A., Hassani A., Aminabhavi T. M., Rtimi S. Microbial electrochemical bioremediation of petroleum hydrocarbons (PHCs) pollution: Recent advances and outlook // Chem. Engin. J. 2023. V. 452. Art. 139372. https://doi.org/10.1016/j.cej.2022.139372
  9. Anaerobic utilization of hydrocarbons, oils, and lipids. Handbook of hydrocarbon and lipid microbiology / Ed. Boll M. Springer, Cham. 2020. https://doi.org/10.1007/978-3-319-50391-2.
  10. Braun A., Spona-Friedl M., Avramov M., Elsner M., Baltar F., Reinthaler T., Herndl G. J., Griebler C. Reviews and syntheses: heterotrophic fixation of inorganic carbon – significant but invisible flux in environmental carbon cycling // Biogeosci. 2021. V. 18. P. 3689–3700. https://doi.org/10.5194/bg-18-3689-2021
  11. Carlson H. K., Iavarone A. T., Gorur A., Yeo B. S., Tran R., Melnyk R. A., Mathies R. A., Auer M., Coates J. D. Surface multiheme c-type cytochromes from Thermincola potens and implications for respiratory metal reduction by Gram-positive bacteria // Proc. Natl. Acad. Sci. USA. 2012. V. 109. P. 1702–1707. https://doi.org/10.1073/pnas.1112905109
  12. Chen H., Simoska O., Lim K., Grattieri M., Yuan M., Dong F., Lee Y. S., Beaver K., Weliwatte S., Gaffney E. M., Minteer S. D. Fundamentals, applications, and future directions of bioelectrocatalysis // Chem. Rev. 2020. V. 120. P. 12903–12993. https://doi.org/10.1021/acs.chemrev.0c00472
  13. Douglas G. M., Maffei V. J., Zaneveld J. R., Yurgel S. N., Brown J. R., Taylor C. M., Huttenhower C., Langille M. G.I. PICRUSt2 for prediction of metagenome functions // Nat. Biotechnol. 2020. V. 38. P. 685–688. https://doi.org/10.1038/s41587-020-0548-6
  14. Erable B., Etcheverry L., Bergel A. From microbial fuel cell (MFC) to microbial electrochemical snorkel (MES): maximizing chemical oxygen demand (COD) removal from wastewater // Biofouling. 2011. V. 27. P. 319–326. https://doi.org/10.1080/08927014.2011.564615
  15. Gohl D. M., MacLean A., Hauge A., Becker A., Walek D., Beckman K. B. An optimized protocol for high- throughput amplicon-based microbiome profiling // Protoc. Exch. 2016. https://doi.org/10.1038/protex.2016.030
  16. Hugerth L. W., Wefer H. A., Lundin S., Jakobsson H. E., Lindberg M., Rodin S., Engstrand L., Andersson A. F. DegePrime, a program for degenerate primer design for broad-taxonomic-range PCR in microbial ecology studies // Appl. Environ. Microbiol. 2014. V. 80. P. 5116–5123. https://doi.org/10.1128/AEM.01403-14
  17. Karstens L., Asquith M., Davin S., Fair D., Gregory W. T., Wolfe A. J., Braun J., McWeeney S. Controlling for contaminants in low-biomass 16S rRNA gene sequencing experiments // mSystems. 2019. V. 4. Art. e00290-19. https://doi.org/10.1128/mSystems.00290-19
  18. Lahti L., Shetty S. Microbiome R package. https://bioconductor.org/packages/release/bioc/html/microbiome.html. Accessed August, 2024.
  19. Logan B. E., Rossi R., Ragab A., Saikaly P. E. Electroactive microorganisms in bioelectrochemical systems // Nat. Rev. Microbiol. 2019. V. 17. P. 307–319. https://doi.org/10.1038/s41579-019-0173-x
  20. Lovley D. R., Holmes D. E. Electromicrobiology: the ecophysiology of phylogenetically diverse electroactive microorganisms // Nat. Rev. Microbiol. 2022. V. 20. P. 5–19. https://doi.org/10.1038/s41579-021-00597-6
  21. Lovley D. R., Holmes D. E., Nevin K. P. Dissimilatory Fe(III) and Mn(IV) reduction // Adv. Microb. Physiol. 2004. V. 49. P. 219–286. https://doi.org/10.1016/S0065-2911(04)49005-5
  22. Lusk B. G. Thermophiles; or, the modern Prometheus: the importance of extreme microorganisms for understanding and applying extracellular electron transfer // Front. Microbiol. 2019. V. 10. Art. 818. https://doi.org/10.3389/fmicb.2019.00818
  23. Marshall C. W., May H. D. Electrochemical evidence of direct electrode reduction by a thermophilic Gram-positive bacterium, Thermincola ferriacetica // Energy Environ. Sci. 2009. V. 2. P. 699–705. https://doi.org/10.1039/b823237g
  24. Matturro B., Viggi C. C., Aulenta F., Rossetti S. Cable bacteria and the bioelectrochemical snorkel: the natural and engineered facets playing a role in hydrocarbons degradation in marine sediments // Front. Microbiol. 2017. V. 8. Art. 952. https://doi.org/10.3389/fmicb.2017.00952
  25. Ntarlagiannis D., Atekwana E. A., Hill E. A., Gorby Y. Microbial nanowires: is the subsurface ‘‘hardwired’’? // Geophys. Res. Lett. 2007. V. 34. Art. L17305. https://doi.org/10.1029/2007GL030426
  26. Oksanen J. Vegan: Community Ecology Package. R package. https://cran.r-project.org/web/packages/vegan. Accessed August 17, 2024.
  27. Package ‘ggvenn’. https://cran.r-project.org/web/packages/ggvenn/ggvenn.pdf. Accessed August 17, 2024.
  28. Peters K. E., Moldowan J. M. The Biomarker Guide: Interpreting molecular fossils in petroleum and ancient sediment. Prentice Hall: Englewood Cliffs, NJ. 1993. P. 40–45.
  29. Rogińska J., Perdicakis M., Midoux C., Bouchez T., Despas C., Liu L., Tian J.-H., Chaumont C., Jorand F. P.A., Tournebize J., Etienne M. Electrochemical analysis of a microbial electrochemical snorkel in laboratory and constructed wetlands // Bioelectrochem. 2021. V. 142. Art. 107895. https://doi.org/10.1016/j.bioelechem.2021.107895
  30. Shi L., Dong H., Reguera G., Beyenal H., Lu A., Liu J., Yu H. Q., Fredrickson J. K. Extracellular electron transfer mechanisms between microorganisms and minerals // Nat. Rev. Microbiol. 2016. V. 14. P. 651–662. https://doi.org/10.1038/nrmicro.2016.93
  31. Wang L. Y., Nevin K. P., Woodard T. L., Mu B. Z., Lovley D. R. Expanding the diet for DIET: electron donors supporting direct interspecies electron transfer (DIET) in defined co-cultures // Front. Microbiol. 2016. V. 7. Art. 236. https://doi.org/10.3389/fmicb.2016.00236
  32. Yamamoto M., Takaki Y., Kashima H., Tsuda M., Tanizaki A., Nakamura R., Takai K. In situ electrosynthetic bacterial growth using electricity generated by a deep-sea hydrothermal vent // ISME J. 2023. V. 17. P. 12–20. https://doi.org/10.1038/s41396-022-01316-6

Supplementary files

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1. JATS XML
2. Fig. 1. Large -scale scheme of the sedimentary MTE device.

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3. Fig. 2. The parameters of the generated electric current and voltage in the first 77 days of incubation (a) and the concentration of CO2 in the gas phase of MTE during the experiment (b).

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4. Fig. 3. The structure of microbial populations of oil -heated soil, the anode and cathode of the MTE according to the results of profiling according to the hypervariabular section of the V4 Gene 16s RRNA at the level of the Philums (A), families and childbirth (b).

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5. Fig. 4. Differences in the representation of potential carriers of the oxidredus (a) and genes that determine the anaerobic oxidation of hydrocarbons (b) in the microbial populations of MTE at the beginning (S0, C0) and at the end of the incubation (S3, A3, C1, C3) according to the results of the Picrust2 analysis.

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6. Fig. 5. Physiological groups in MTE microbial populations, predicted on the basis of an analysis of literary data on cultivated microorganisms, the closestly related Philotypes: a - all targeted physiological groups; b - the ratio of various groups of microorganisms capable of extracellular transfer of electrons; B - representation of microorganisms capable of heterotrophic fixation of CO2, in a cathode population.

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7. Additional materials
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