Skip to main content

Advertisement

Springer Nature Link
Log in

New Biocomposite Materials Based on Hydrocarbon-Oxidizing Microorganisms and Their Potential for Oil Products Degradation

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

An Erratum to this article was published on 03 June 2022

This article has been updated

Abstract—

Increasing the stability of biopreparations of hydrocarbon-oxidizing bacteria (HOB), which are used for bioremediation of oil-contaminated environmental objects, is presently an important task. In the present work, new biocomposite materials were developed for HOB immobilization on the surface of microcapsules (MCs) from: pure and chitosan- or gelatin-modified polyurea; polylactic and polyglycolic acids; and cell incorporation into the gels of humic acids silanol derivatives. The tested organisms used were gram-negative HOB Acinetobacter seifertii WS1, Pseudomonas extremaustralis WS-1, P. aeruginosa OIS 4.8.1, gram-positive bacteria Rhodococcus qingshengii 367-6, and Dietzia maris 367-2, as well as yeasts Yarrowia lipolytica 367-2. HOB cultivation in liquid media with chitosan-polyurea-based MCs (but not MCs of pure or gelatin-modified polyurea) resulted in viable cell numbers (CFU/mL) 2‒5 times higher than in the control (without MCs) both in freshly grown cultures and in those stored at room temperature under access to air for a long time (up to 7 months). HOB cultivation together with polylactic acid MCs resulted in active surface growth. Surface growth was less pronounced in the variants with polyglycolic MC, as was confirmed microscopically. Survival of the R. qingshengii grown in the presence of polylactide MCs after storage for 1 month was three orders of magnitude higher than in the control (without MCs). HOB immobilization in the gels of humate silanol derivatives was the most efficient approach, which resulted in CFU titers up to 100 times higher than in the control variant after storage for 7‒12 months; respiration rates were also higher than in the control. The biopreparations with HOB immobilized in new biocomposite materials had high oil-oxidizing activity both in liquid media and oil-contaminated soil microcosms. After 4-month storage at room temperature, the rate of oil oxidation by these biopreparations was 2 to 4 times higher than in the control. The practically important features of new biocomposite materials are: prolonged HOB cell viability in the course of long-term storage (up to 12 months); homogeneity of the cultures at the time of application; and presence of additional growth substrates, which may be used for hydrocarbon co-oxidation.

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

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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.
Fig. 7.
Fig. 8.
Fig. 9.
Fig. 10.

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

Change history

REFERENCES

  1. Beier, S. and Bertilsson, S., Bacterial chitin degradation-mechanisms and ecophysiological strategies, Front. Microbiol., 2013, vol. 4, art. 149. https://doi.org/10.3389/fmicb.2013.00149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Benita, S., Microencapsulation. Methods and Industrial Application, 2nd ed., CRC, 2005.

    Book  Google Scholar 

  3. Biomaterials for Oral and Dental Tissue Engineering, Tayebi, L. and Moharamzadeh, K., Eds., Woodhead, 2018.

    Google Scholar 

  4. Chen, A.Y., Zhong, C., and Lu, T.K., Engineering living functional materials, ACS Synth. Biol., 2015, vol. 4, pp. 8‒11. https://doi.org/10.1021/sb500113b

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Dagurov, A.V., Stom, D.I., Vyatchina, O.F., Balayan, A.E., and Kushnarev, D.F., On the mechanism of the antidote action of humates in relation to oil products, Acta Biomedica Scientifica, 2005, vol. 6, no. 44, pp. 143‒145.

    Google Scholar 

  6. Daiguji, H., Takada, S., Jay, J., Cornejo, M., and Takemura, F., Fabrication of hollow poly(lactic acid) microcapsules from microbubble templates, J. Phys. Chem., 2009, vol. 113, pp. 15002–15009. https://doi.org/10.1021/jp9053956

    Article  CAS  Google Scholar 

  7. Das, N. and Chandran, P., Microbial degradation of petroleum hydrocarbon contaminants, Biotechnol. Res. Int., 2011, vol. 2011, art. 941810. https://doi.org/10.4061/2011/941810

    Article  CAS  PubMed  Google Scholar 

  8. Davoodi, S.M., Miri, S., Taheran, M., Brar, S.K., Galvez-Cloutier, R., and Martel, R., Bioremediation of unconventional oil contaminated ecosystems under natural and assisted conditions: a review, Environ Sci Technol., 2020, vol. 18, iss. 54(4), pp. 2054−2067. https://doi.org/10.1021/acs.est.9b00906

  9. Dorofeev, A.G. and Panikov, N.S., Growth effectivity of microorganisms of different ecological strategies at steady-state conditions. Microbiology (Moscow), 1988, vol. 57, no. 4, pp. 963−973.

    Google Scholar 

  10. Dzionek, A., Wojcieszyńska, D., and Guzik, U., Natural carriers in bioremediation, Electr. J. Biotechnol., 2016, vol. 23, pp. 28–36.

    Article  Google Scholar 

  11. Egozar’yan, N.S., Solyanikova, I.P., Suzina, N.E., Emel’yanova, E.V., Polivtseva, V.N., Mulyukin, A.L., El’-Registan, G.I., and Golovleva, L.A., Dormant cells of actinobacteria as the base of stable bioremediation preparations, Biotekhnologiya: sostoyanie i perspektivy razvitiya (Biotechnology: State and Prospects, 9th Int. Congress), Moscow, 2017, pp. 434‒436.

  12. Iqba, H.M.N. and Keshavarz, T., The challenge of biocompatibility evaluation of biocomposites, in Biomedical Composites, Woodhead Publ. Ser. Biomaterials, 2017, 2nd ed., pp. 303–334.

    Google Scholar 

  13. Ivshina, I.B., Mukhutdinova, A.N., Tyumina, H.A., Vikhareva, H.V., Suzina, N.E., El’-Registan, G.I., and Mulyukin, A.L., Drotaverine hydrochloride degradation using cyst-like dormant cells of Rhodococcus ruber, Curr. Microbiol., 2015, vol. 70, pp. 307–314.

    Article  CAS  Google Scholar 

  14. Kuran, P., Trögl, J., Nováková, J., Pilařová, V., Dáňová, P., Pavlorková, J., Kozler, J., Novák, F., and Popelka, J., Biodegradation of spilled diesel fuel in agricultural soil. Effect of humates, zeolite, and bioaugmentation, Sci. World J., 2014, vol. 2014, art. 642427. https://doi.org/10.1155/2014/642427

    Article  CAS  Google Scholar 

  15. Larionov, I.V., Rybal’chenko, O.V., Orlova, O.G., Potokin, I.L., Sushko, T.P., Khrushcheva, T.A., and Boldyrev, A.G., Adsorption of probiotic bacteria on cellulose sorbents, Sorbtsionnye i Khromatograficheskie Processy, 2011, vol. 11, pp. 792‒798.

    CAS  Google Scholar 

  16. Lia, Sh.-Sh., Hana, H., Zhua, X.-L., Jianga, X.-B., and Konga, X.Zh., Preparation and formation mechanism of porous polyurea by reaction of toluene diisocyanate with water and its application as adsorbent for anionic dye removal chinese, J. Polym. Sci., 2015, vol. 33, pp. 1196–1210.

    Google Scholar 

  17. Lipson, D.A., The complex relationship between microbial growth rate and yield and its implications for ecosystem processes, Frontiers in Microbiology, 2015, vol. 6, p. 615. https://doi.org/10.3389/fmicb.2015.00615

  18. Liu, S. and Xu, W., Engineered living materials-based sensing and actuation, Front. Sens., 2020. 1:586300. https://doi.org/10.3389/fsens.2020.586300

    Article  Google Scholar 

  19. Lupu, S., Balaure, P.C., Lete, C., and Mihailciuc, C., Biocomposite nanomaterials for electrochemical biosensors, in Handbook of Nanoelectrochemistry, Aliofkhazraei, M. and Makhlouf, A., Eds., Springer, Cham, 2015. https://doi.org/10.1007/978-3-319-15207-3_39-1

    Book  Google Scholar 

  20. Martens, R. and Domsch, K.H., Microbial degradation of polyurethane foams and isocyanate based polyureas in different media, Water Air Soil Pollut., 1981, vol. 15, pp. 503–509. https://doi.org/10.1007/BF00279430

    Article  CAS  Google Scholar 

  21. Mitropoulouet, G., Nedovic, V., Goyal, A., and Kourkoutas, Y., Immobilization technologies in probiotic food production, J. Nutrit. Metabolism, 2013, vol. 2013, art. 716861. https://doi.org/10.1155/2013/716861

    Article  Google Scholar 

  22. Nikolaev, Y.A., Demkina, E.V., Loiko, N.G., Borzenkov, I.A., Ivanona, A.E., El’-Registan, G.I., Perminova, I.V., and Konstantinov, A.I., Role of humic compounds in viability prolongation of the cells of hydrocarbon-oxidizing bacteria, Microbiology (Moscow), 2019, vol. 88, pp. 764‒768.

    Article  CAS  Google Scholar 

  23. Nikolaev, Y.A., Loiko, N.G., Demkina, E.V., El’-Registan, G.I., Konstantinov, A.I., Perminova, I.V., and Atroshchik, E.A., Functional activity of humic substances in survival prolongation of populations of hydrocarbon-oxidizing bacteria Acinetobacter junii, Microbiology (Moscow), 2020, vol. 89, pp. 74‒85.

    Article  CAS  Google Scholar 

  24. Nikovaev, Yu.A., Borzenkov, I.A., Bliznets, I.V., Loiko, H.G., Demkina, E.V., Ivanova, A.E., Kanapatskii, T.A., and El’-Registan, G.I., A method for obtaining biopreparations of living microorganisms with extended duration of the preservation of a high viable cell titer, RF Patent no. 2751360, 2020а.

  25. Opara, E.C., Cell Microencapsulation. Methods and Protocol, N.Y.: Springer Science + Business Media, 2017.

  26. Park, S., Kim, K.S., Kim, J.-T., Kang, D., and Sung, K., Effects of humic acid on phytodegradation of petroleum hydrocarbons in soil simultaneously contaminated with heavy metals, J. Environ. Sci., 2011, vol. 23, pp. 2034‒2041.

    Article  CAS  Google Scholar 

  27. Pilla, S., Handbook of Bioplastics and Biocomposites Engineering Applications, Wiley, 2011, р. 620.

    Book  Google Scholar 

  28. Qi, X., Ren, Y., and Wang, X., New advances in the biodegradation of poly(lactic) acid, Int. Biodeterior. Biodegrad., 2017, vol. 117, pp. 215–223. https://doi.org/10.1016/j.ibiod.2017.01.010

    Article  CAS  Google Scholar 

  29. Rudin, A. and Choi, Ph., Biopolymers. The Elements of Polymer Science & Engineering, Academic, 2013, 3rd ed., Ch. 13, pp. 521‒535.

    Google Scholar 

  30. Sakurai, D., Cornejo, J.J.M., Daiguji, H., and Takemura, F., Hollow polylactic acid microcapsules fabricated by gas/oil/water and bubble template methods, J. Mater. Chem. A., 2013, vol. 46, pp. 14562‒14568.

    Article  Google Scholar 

  31. Sawaguchi, A., Ono, S., Oomura, M., Inami, K., Kumeta, Y., Honda, K., Sameshima-Saito, R., Sakamoto, K., Ando, A., and Saito, A., Chitosan degradation and associated changes in bacterial community structures in two contrasting soils, Soil Sci. Plant Nutrit., 2015, vol. 61, pp. 471‒480. https://doi.org/10.1080/00380768.2014.1003965

    Article  CAS  Google Scholar 

  32. Sears, N.A., Pena-Galea, G., Cereceres, S.N., and Cosgriff-Hernandez, E., Hybrid polyurea elastomers with enzymatic degradation and tunable mechanical properties, J. Tissue Eng., 2016, vol. 7, art. 2041731416679363. https://doi.org/10.1177/2041731416679363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Sihag, S., Pathak, H., and Jaroli, D., Factors affecting the rate of biodegradation of polyaromatic hydrocarbons, Int. J. Pure App. Biosci., 2014, vol. 2, pp. 185‒202.

    Google Scholar 

  34. Solyanikova, I.P., Suzina, N.E., Egozarjan, N.S., Polivtseva, V.N., Golovleva, L.A., Mulyukin, A.L., El-Registan, G.I., and Egorova, D.O., Structural and functional rearrangements in the cells of actinobacteria Microbacterium foliorum BN52 during transition from vegetative growth to a dormant state and during germination of dormant forms, Microbiology (Moscow), 2017, vol. 86, pp. 476‒486.

    Article  CAS  Google Scholar 

  35. Solyanikova, I.P., Suzina, N.E., Golovleva, L.A., Mulyukin, A.L., and El-Registan, G.I., Improved xenobiotic-degrading activity of Rhodococcus opacus strain 1cp after dormancy, J. Environ. Sci. Health. Part B: Pesticides. Food Contaminants and Agricultural Wastes, 2011, vol. 46, pp. 638‒647.

    CAS  Google Scholar 

  36. Tang, D., Chen, Z., Correa-Netto, F., Macosko, C.W., Hillmyer, M.A., and Zhang, G., Poly(urea ester): a family of biodegradable polymers with high melting temperatures, J. Polym. Sci. Part A: Polymer Chemistry, 2016, vol. 54, pp. 3795–3799. https://doi.org/10.1002/pola.28355

    Article  CAS  Google Scholar 

  37. Volikov, A.B., Ponomarenko, S.A., Gutsche, A., Nirschl, H., Hatfield, K., and Perminova, I.V., Targeted design of water-based humic substances-silsesquioxane soft materials for nature-inspired remedial, RSC Advances, 2016b, vol. 6, pp. 48222–48230.

    Article  CAS  Google Scholar 

  38. Volikov, A.B., Ponomarenko, S.A., Konstantinov, A.I., Hatfield, K., and Perminova, I.V., Silanized humic substances act as hydrophobic modifiers of soil separates inducing formation of water-stable aggregates in soils, Catena, 2016a, vol. 137, pp. 229–236.

    Article  CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

Electron microscopy was partially carried out using the equipment acquired within the framework of the Program of Development of Moscow State University up to 2020.

Funding

The work was supported by the Russian Foundation for Basic Research, project no. 18-29-05009/18 and partially by the State Assignment of the RF Ministry of Education and Science for the Biotechnology Research Center, Russian Academy of Sciences and, partially, by the Russian Science Foundation, project no. 21-14-00076.

Author information

Authors and Affiliations

  1. Winogradsky Institute of Microbiology, Research Centre of Biotechnology, Russian Academy of Sciences, 119071, Moscow, Russia

    Yu. A. Nikovaev, I. A. Borzenkov, E. V. Demkina, N. G. Loiko, T. A. Kanapatskii, N. V. Grigor’eva, V. V. Sorokin & G. I. El’-Registan

  2. Faculty of Chemistry, Moscow State University, 119191, Moscow, Russia

    I. V. Perminova & A. N. Khreptugova

  3. Faculty of Soil Science, Moscow State University, 119191, Moscow, Russia

    N. A. Manucharova & M. A. Kovalenko

  4. BNT Company (MSU Science and technology Park), Moscow, Russia

    I. V. Bliznets

Authors
  1. Yu. A. Nikovaev
    View author publications

    Search author on:PubMed Google Scholar

  2. I. A. Borzenkov
    View author publications

    Search author on:PubMed Google Scholar

  3. E. V. Demkina
    View author publications

    Search author on:PubMed Google Scholar

  4. N. G. Loiko
    View author publications

    Search author on:PubMed Google Scholar

  5. T. A. Kanapatskii
    View author publications

    Search author on:PubMed Google Scholar

  6. I. V. Perminova
    View author publications

    Search author on:PubMed Google Scholar

  7. A. N. Khreptugova
    View author publications

    Search author on:PubMed Google Scholar

  8. N. V. Grigor’eva
    View author publications

    Search author on:PubMed Google Scholar

  9. I. V. Bliznets
    View author publications

    Search author on:PubMed Google Scholar

  10. N. A. Manucharova
    View author publications

    Search author on:PubMed Google Scholar

  11. V. V. Sorokin
    View author publications

    Search author on:PubMed Google Scholar

  12. M. A. Kovalenko
    View author publications

    Search author on:PubMed Google Scholar

  13. G. I. El’-Registan
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Yu. A. Nikovaev.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by P. Sigalevich

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nikovaev, Y.A., Borzenkov, I.A., Demkina, E.V. et al. New Biocomposite Materials Based on Hydrocarbon-Oxidizing Microorganisms and Their Potential for Oil Products Degradation. Microbiology 90, 731–742 (2021). https://doi.org/10.1134/S0026261721060114

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261721060114

Keywords: