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Contribution of soil bacteria isolated from different regions into crude oil and oil product degradation

  • Irina F. Puntus
  • Oksana V. Borzova
  • Tatyana V. Funtikova
  • Nataliya E. Suzina
  • Nataliya S. Egozarian
  • Valentina N. Polyvtseva
  • Ekaterina S. Shumkova
  • Lenar I. Akhmetov
  • Ludmila A. Golovleva
  • Inna P. Solyanikova
SUITMA 9: Urbanization — Challenges and Opportunities for Soil Functions and Ecosystem Services

Abstract

Purpose

Crude oil and oil products are the most widespread environmental pollutants. The most efficient bioremediation is performed by using specific oil-degrading strains. Our objectives were to assess the role of soil bacteria, belonging to the following genera Arthrobacter, Microbacterium, Rhodococcus, Gordonia, and Acinetobacter in reduction of toxicity of environmental pollutants. Bacteria with different versatility were chosen: isolates from aromatic compounds or crude oil-contaminated soils and common representatives of the soil microflora.

Materials and methods

In this work, crude oil from the field Aschisay (Kazakhstan) of the following composition: alkanes 78%, naphthenes 6.7%, arenes 3.7%, and other compounds 11.6% was used as carbon source. To investigate the metabolic activity of microorganisms, they were cultured in flasks for 10 days under different conditions (variations in pH range, temperature, salinity, carbon source). Infrared spectrophotometry method was employed to determine the residual oil content after cultivation of bacteria. The ability of bacteria to produce biosurfactants was assessed by measuring surface tension and emulsifying activity (the Francey et al. method); localization of biosurfactants was detected.

Results and discussion

Forty-six strains from oil-spilled soils were isolated, with seven of these isolates showing the high degradation ability. Analysis of 16S-RNA gene sequences assigns these cultures to the genus Rhodococcus. Their degradation activity was then compared with the one of two rhodococci isolated from soil contaminated with chloroaromatics. The strains under study degraded crude oil, diesel fuel, and phenol; some of them destroyed benzene and naphthalene. The most active strains utilized up to 55–59% of crude oil hydrocarbons. The behavior of strains in the presence of petroleum components (benzene, toluene, nonane, decane, hexadecane) revealed bacterial persistence under severe conditions. Bacteria proved to be more sensitive to aromatic solvents than to aliphatic hydrocarbons. Most of the strains produced biosurfactants when grown on hydrophobic substrates.

Conclusions

The obtained results show that bacteria highly adapted to oil contaminations play an important role in the biodegradation of recalcitrant pollutants. Such strains may serve as the basis of bioaugmentation approach for soil remediation in sites with high contamination degree. Furthermore, this study highlights a significant role of common representatives of soil microflora in reducing pollution level in the soil owing to various, however, not necessary high destructive activities of soil strains.

Keywords

Bacteria Contamination Degradation Oil hydrocarbons Soil 

Notes

Funding information

This work was supported by Russian Science Foundation (grant no. 14-14-00368) and Kazakhstanian–Russian project No. 142 “Development of a concept for monitoring contaminated soil in the Aral Sea region, and technologies for their remediation using new bioproducts.”

Supplementary material

11368_2018_2003_MOESM1_ESM.docx (21.6 mb)
ESM 1 (DOCX 22104 kb)

References

  1. Ausbel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1995) Short protocols in molecular biology, 3rd edn. John Wiley and Sons, NYGoogle Scholar
  2. Bell KS, Philp JC, Aw DWJ, Christofi N (1998) The genus Rhodococcus. J Appl Microbiol 85:195–210CrossRefGoogle Scholar
  3. Bello-Akinosho M, Makofane R, Adeleke R, Thantsha M, Pillay M, Chirima GJ (2016) Potential of polycyclic aromatic hydrocarbon-degrading bacterial isolates to contribute to soil fertility. Biomed Res Int, Article ID 5798593, doi: https://doi.org/10.1155/2016/5798593
  4. Cameotra SS, Singh P (2008) Bioremediation of oil sludge using crude biosurfactants. Intern Biodeterior Biodegrad 62(3):274–280CrossRefGoogle Scholar
  5. Carhart G, Hegeman G (1975) Improved method of selection for mutants of Pseudomonas putida. Appl Microbiol 30:1046–1047Google Scholar
  6. Chaudhary DK (2016) Bioremediation: an eco-friendly approach for polluted agriculture soil. Emer Life Sci Res 2:73–75Google Scholar
  7. Cirigliano M, Carman GM (1984) Isolation of bioemulsifier from Candida lipolytica. Appl Environ Microbiol 48:747–750Google Scholar
  8. Coronelli TV, Kalyuzhnaya ТВ (1983) Change in the ultrastructure of cells of saprotrophic mycobacteria under the influence of isoniazid. Microbiology 522(2):278–281Google Scholar
  9. Cui CZ, Zeng C, Wan X, Chen D, Zhang JY, Shen P (2008) Effect of rhamnolipids on degradation of anthracene by two newly isolated strains, Sphingomonas sp. 12A and Pseudomonas sp. 12B. J Microbiol Biotechnol 18(1):63–66Google Scholar
  10. Dahal RH, Chaudhary DK, Kim J (2017) Acinetobacter halotolerans sp. nov., a novel halotolerant, alkalitolerant, and hydrocarbon degrading bacterium, isolated from soil. Arch Microbiol 199:701–710CrossRefGoogle Scholar
  11. Das N, Chandran P (2011) Microbial degradation of petroleum hydrocarbon contaminants: an overview. SAGE-Hindawi Access to Res Biotechnol Res Int Article ID 941810:1–13.  https://doi.org/10.4061/2011/941810 Google Scholar
  12. de Carvalho CCCR (2010) Adaptation of Rhodococcus to organic solvents. In: Alvarez HM (ed) Biology of Rhodococcus. Springer-Verlag, Berlin, Heidelberg, pp 110–131Google Scholar
  13. de Goes KCGP, da Silva JJ, Lovato GM, Iamanaka BT, Massi FP, Andrade DS (2017) Talaromyces sayulitensis, Acidiella bohemica and Penicillium citrinum in Brazilian oil shale by-products. Antonie Van Leeuwenhoek 110:1637–1646CrossRefGoogle Scholar
  14. Drzyzga O (2012) The strengths and weaknesses of Gordonia: a review of an emerging genus with increasing biotechnological potential. Crit Rev Microbiol 38(4):300–316CrossRefGoogle Scholar
  15. Evans CGT, Herbert D, Tempest DB (1970) The continuous cultivation of microorganisms. 2. Construction of a chemostat. Meth Microbiol 2:277–327Google Scholar
  16. Francy D, Thomas J, Raymond R, Ward C (1991) Emulsification of hydrocarbons by subsursurface bacteria. J Ind Microbiol 8(4):237–246CrossRefGoogle Scholar
  17. Franzetti A, Gandolfi I, Bestetti G, Smyth TJP, Banat IM (2010) Production and applications of trehalose lipid biosurfactants. Eur J Lipid Sci Technol 112:617–627CrossRefGoogle Scholar
  18. Fuentes S, Barra B, Caporaso JG, Seeger M (2016) From rare to dominant: a fine-tuned soil bacterial bloom during petroleum hydrocarbon bioremediation. Appl Environ Microbiol 82(3):888–896CrossRefGoogle Scholar
  19. Fuentes S, Méndez V, Aguila P, Seeger M (2014) Bioremediation of petroleum hydrocarbons: catabolic genes, microbial communities, and applications. Appl Microbiol Biotechnol 98:4781–4794CrossRefGoogle Scholar
  20. Gorlatov SN, Maltseva OV, Shevchenko VI, Golovleva LA (1989) Degradation of chlorophenols by a culture of Rhodococcus erythropolis. Mikrobiologiya (Moscow) 58:647–651Google Scholar
  21. Hong SH, Ryu H, Kim J, Cho KS (2011) Rhizoremediation of diesel-contaminated soil using the plant growth-promoting rhizobacterium Gordonia sp. S2RP-17. Biodegradation 22(3):593–601CrossRefGoogle Scholar
  22. Ishige T, Tani A, Saki Y, Kato N (2000) Long-chain aldehyde dehydrogenase that participates in n-alkane utilization and wax ester synthesis in Acinetobacter sp. strain M−1. Appl Environ Microbiol 66:3481–3486CrossRefGoogle Scholar
  23. Ivshina IB, Pshenichnov RA, Oborin AA (1987) Propane-oxidizing rodococci. Sverdlovsk, UNSC of the USSR Academy of Sciences (in Russian)Google Scholar
  24. Joshi MN, Dhebar SV, Dhebar SV, Bhargava P, Pandit A, Patel RP, Saxena A, Bagatharia SB (2014) Metagenomics of petroleum muck: revealing microbial diversity and depicting microbial syntrophy. Arch Microbiol 196:531–544CrossRefGoogle Scholar
  25. Kaczorek E, Jesionowski T, Giec A, Olszanowski A (2012) Cell surface properties of Pseudomonas stutzeri in the process of diesel oil biodegradation. Biotechnol Lett 34:857–862CrossRefGoogle Scholar
  26. Kang SK, Jung J, Jeon CO, Park W (2011) Acinetobacter oleivorans sp. nov. is capable of adhering to and growing on diesel-oil. J Microbiol 49:29–34CrossRefGoogle Scholar
  27. Kvenvolden KA, Cooper CK (2003) Natural seepage of crude oil into the marine environment. Geo-Mar Lett 23:140–146.  https://doi.org/10.1007/s00367-003-0135-0 CrossRefGoogle Scholar
  28. Larkin MJ, Kulakov LA, Allen CC (2005) Biodegradation and Rhodococcus—masters of catabolic versatility. Curr Opin Biotech 16(3):282–290CrossRefGoogle Scholar
  29. Lin T-C, Pan P-T, Cheng S-S (2010) Ex situ bioremediation of oil-contaminated soil. J Hazard Mater 176:27–34CrossRefGoogle Scholar
  30. Liu S, Liu W, Yang M, Zhou L, Liang H (2016b) The genetic diversity of soil bacteria affected by phytoremediation in a typical barren rare earth mined site of South China. Spring 5(1):1131CrossRefGoogle Scholar
  31. Liu Y, Hu X, Liu H (2016a) Industrial-scale culturing of the crude oil-degrading marine Acinetobacter sp. strain HC8-3S. Intern Biodeter Biodegr 107:56–61CrossRefGoogle Scholar
  32. Lo Piccolo L, De Pasquale C, Fodale R, Puglia AM, Quatrini P (2011) Involvement of an alkane hydroxylase system of Gordonia sp. strain SoCg in degradation of solid n-alkanes. Appl Environ Microbiol 77(4):1204–1213CrossRefGoogle Scholar
  33. Martínková L, Uhnáková B, Pátek M, Nešvera J, Křen V (2009) Biodegradation potential of the genus Rhodococcus. Environm Internation 35(1):162–177Google Scholar
  34. Oberoi AS, Philip L, Bhallamudi SM (2015) Biodegradation of various aromatic compounds by enriched bacterial cultures: part A—monocyclic and polycyclic aromatic hydrocarbons. Appl Biochem Biotech 176:1870–1888CrossRefGoogle Scholar
  35. Pacwa-Plociniczak M (2011) Environmental applications of biosurfactants: recent advances. Int J Mol Sci 12:633–654CrossRefGoogle Scholar
  36. Petrikov KV, Delegan YA, Surin A, Ponamoreva ON, Puntus IF, Filonov AE, Boronin AM (2013) Glycolipids of Pseudomonas and Rhodococcus oil-degrading bacteria used in bioremediation preparations: formation and structure. Process Biochem 48:931–935CrossRefGoogle Scholar
  37. Plotnikova EG, Rybkina DO, Anan’ina LN, Yastrebova OV, Demakov VA (2006) Characterization of microorganisms isolated from technogenic soils of the Kama region. Russ J Ecol 4:261–268Google Scholar
  38. Rapp P, Gabriel-Jurgens LH (2003) Degradation of alkanes and highly chlorinated benzenes, and production of biosurfactants, by a psychrophilic Rhodococcus sp. and genetic characterization of its chlorobenzene dioxygenase. Microbiology 149:2879–2890CrossRefGoogle Scholar
  39. Romanowska I, Kwapisz E, Mitka M, Bielecki S (2010) Isolation and preliminary characterization of a respiratory nitrate reductase from hydrocarbon-degrading bacterium Gordonia alkanivorans S7. J Ind Microbiol Biotechnol 37(6):625–629CrossRefGoogle Scholar
  40. Sajna KV, Sukumaran RK, Gottumukkala LD, Pandey A (2015) Crude oil biodegradation aided by biosurfactants from Pseudozyma sp. NII 08165 or its culture broth. Bioresour Technol 191:133–139CrossRefGoogle Scholar
  41. Satpute SK, Banpurkar AG, Dhakephalkar PK, Banat IM, Chopade BA (2010) Methods for investigating biosurfactants and bioemulsifiers: a review. Crit Rev Biotechnol 30(1):127–144CrossRefGoogle Scholar
  42. Sikkema J, de Bont JA, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rew 59(2):201–222Google Scholar
  43. Solyanikova IP, Emelyanova EV, Shumkova ES, Egorova DO, Korsakova ES, Plotnikova EG, Golovleva LA (2015) Peculiarities of the degradation of benzoate and its chloro- and hydroxy-substituted analogs by actinobacteria. Int Biodeter Biodegr 100:155–164CrossRefGoogle Scholar
  44. Solyanikova IP, Golovlev EL, Lisnyak OV, Golovleva LA (1999) Isolation and characterization of catechol 1,2-dioxygenases from Rhodococcus rhodnii strain 135 and Rhodococcus rhodochrous strain 89: comparison with analogous enzymes of the ordinary and modified ortho-cleavage pathways. Biokhimiya (Moscow) 64:824–831Google Scholar
  45. Solyanikova IP, Suzina NE, Egozarjan NS, Polivtseva VN, Mulyukin AL, Egorova DO, El-Registan GI, Golovleva LA (2017a) 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. Mikrobiologiya (Moscow) 86(4):463–475CrossRefGoogle Scholar
  46. Solyanikova IP, Suzina NE, Egozarjan NS, Polivtseva VN, Mulyukin AL, Egorova DO, El-Registan GI, Golovleva LA (2017b) The response of soil-dwelling Arthrobacter agilis Lush13 to stress impact: transition between vegetative growth and dormancy state. J Environm Sci Health Part B 52(10):745–751CrossRefGoogle Scholar
  47. Takihara H, Ogihara J, Yoshida T, Okuda S, Nakajima M, Iwabuchi N, Sunairi M (2014) Enhanced translocation and growth of Rhodococcus erythropolis PR4 in the alkane phase of aqueous-alkane two phase cultures were mediated by GroEL2 overexpression. Microbes Environ 29(4):346–352CrossRefGoogle Scholar
  48. Tanase A-M, Ionescu R, Chiciudean I, Vassu T, Stoica I (2013) Characterization of hydrocarbon-degrading bacterial strains isolated from oil-polluted soil. Intern Biodeter Biodegrad 84:150–154CrossRefGoogle Scholar
  49. Tiirola MA, Mannisto MK, Puhakka JA, Kulomaa MS (2002) Isolation and characterization of Novosphingobium sp. strain MT1, a dominant polychlorophenol-degrading strain in a groundwater bioremediation system. Appl Environ Microbiol 68:173–180CrossRefGoogle Scholar
  50. Throne-Holst M, Markussen S, Winnberg A, Ellingsen TE, Kotlar HK, Zotchev SB (2006) Utilization of n-alkanes by a newly isolated strain of Acinetobacter venetianus: the role of two AlkB-type alkane hydroxylases. Appl Microbiol Biotechnol 72:353–360CrossRefGoogle Scholar
  51. Tokumoto Y, Nomura N, Uchiyama H, Imura T, Morita T, Fukuoka T, Kitamoto D (2009) Structural characterization and surface-active properties of a succinoyl trehalose lipid produced by Rhodococcus sp. SD-74. J Oleo Sci 58(2):97–102CrossRefGoogle Scholar
  52. Tuleva B, Christova N, Cohen R, Stoev G, Stoineva I (2008) Production and structural elucidation of trehalose tetraesters (biosurfactants) from a novel alkanothrophic Rhodococcus wratislaviensis strain. J Appl Microbiol 104(6):1703–1710CrossRefGoogle Scholar
  53. Varjani SJ, Rana DP, Bateja S, Sharma MC, Upasani VN (2014) Screening and identification of biosurfactant (bioemulsifier) producing bacteria from crude oil contaminated sites of Gujarat, India. Int J Innovative Res Sci Eng Technol 3(2):9205–9213Google Scholar
  54. Varjani SJ, Upasani VN (2017) A new look on factors affecting microbial degradation of petroleum hydrocarbon pollutants. Intern Biodeter Biodegr 120:71–83CrossRefGoogle Scholar
  55. Varjani SJ, Rana DP, Jain AK, Bateja S, Upasani VN (2015) Synergistic ex situ biodegradation of crude oil by halotolerant bacterial consortium of indigenous strains isolated from on shore sites of Gujarat, India. Int Biodeterior Biodegrad 103:116–124CrossRefGoogle Scholar
  56. Varjani SJ, Upasani VN (2016a) Core flood study for enhanced oil recovery through ex-situ bioaugmentation with thermo- and halo-tolerant rhamnolipid produced by Pseudomonas aeruginosa NCIM 5514. Bioresour Technol 220:175–182CrossRefGoogle Scholar
  57. Varjani SJ, Upasani VN (2016b) Carbon spectrum utilization by an indigenous strain of Pseudomonas aeruginosa NCIM 5514: production, characterization and surface active properties of biosurfactant. Bioresour Technol 221:510–516CrossRefGoogle Scholar
  58. Varjani SJ, Upasani VN (2016c) Biodegradation of petroleum hydrocarbons by oleophilic strain of Pseudomonas aeruginosa NCIM 5514. Bioresour Technol 222:195–201CrossRefGoogle Scholar
  59. van Hamme JD, Singh A, Ward OP (2003) Recent advances in petroleum microbiology. Microbiol Mol Biol Rev 67(4):503–549CrossRefGoogle Scholar
  60. White DA, Hird LC, Ali ST (2013) Production and characterization of a trehalolipid biosurfactants produced by the novel marine bacterium Rhodococcus sp., strain PML026. J Appl Microbiol 115(3):744–755CrossRefGoogle Scholar
  61. Yamahira K, Hirota K, Nakajima K, Morita N, Nodasaka Y, Yumoto I (2008) Acinetobacter sp. strain Ths, a novel psychrotolerant and alkalitolerant bacterium that utilizes hydrocarbon. Extremophiles 12:729–734CrossRefGoogle Scholar
  62. Zhukov DV, Murygina VP, Kalyuzhny SV (2006) Mechanisms of petroleum hydrocarbons degradation by microorganisms. Successes of modern. Biology 126(3):285–296Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Irina F. Puntus
    • 1
  • Oksana V. Borzova
    • 1
    • 2
  • Tatyana V. Funtikova
    • 1
  • Nataliya E. Suzina
    • 1
  • Nataliya S. Egozarian
    • 1
  • Valentina N. Polyvtseva
    • 1
  • Ekaterina S. Shumkova
    • 3
  • Lenar I. Akhmetov
    • 1
  • Ludmila A. Golovleva
    • 1
    • 2
  • Inna P. Solyanikova
    • 1
  1. 1.G.K. Skryabin Institute of Biochemistry and Physiology of MicroorganismsRussian Academy of SciencesPushchinoRussia
  2. 2.Pushchino State Natural Science InstitutePushchinoRussia
  3. 3.Bach Institute of Biochemistry, Research Center of BiotechnologyRussian Academy of SciencesMoscowRussia

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