Skip to main content
Log in

Biodegradation of diesel oil by a novel microbial consortium: comparison between co-inoculation with biosurfactant-producing strain and exogenously added biosurfactants

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Bioremediation, involving the use of microorganisms to detoxify or remove pollutants, is the most interesting strategy for hydrocarbon remediation. In this aim, four hydrocarbon-degrading bacteria were isolated from oil-contaminated soil in Tunisia. They were identified by the 16S rDNA sequence analysis, as Lysinibacillus bronitolerans RI18 (KF964487), Bacillus thuringiensis RI16 (KM111604), Bacillus weihenstephanensis RI12 (KM094930), and Acinetobacter radioresistens RI7 (KJ829530). Moreover, a lipopeptide biosurfactant produced by Bacillus subtilis SPB1, confirmed to increase diesel solubility, was tested to increase diesel biodegradation along with co-inoculation with two biosurfactant-producing strains. Culture studies revealed the enhancement of diesel biodegradation by the selected consortium with the addition of SPB1 lipopeptide and in the cases of co-inoculation by biosurfactant-producing strain. In fact, an improvement of about 38.42 and 49.65 % of diesel degradation was registered in the presence of 0.1 % lipopeptide biosurfactant and when culturing B. subtilis SPB1 strain with the isolated consortium, respectively. Furthermore, the best improvement, evaluated to about 55.4 %, was recorded when using the consortium cultured with B. subtilis SPB1 and A. radioresistens RI7 strains. Gas chromatography analyses were correlated with the gravimetric evaluation of the residual hydrocarbons. Results suggested the potential applicability of the selected consortium along with the ex situ- and in situ-added biosurfactant for the effective bioremediation of diesel-contaminated water and soil.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abalos A, Vinas M, Sabate J, Manresa MA, Solanas AM (2004) Enhanced biodegradation of Casablanca crude oil by a microbial consortium in presence of a rhamnolipid produced by Pseudomonas aeruginosa AT10. Biodegradation 15:249–260

    Article  CAS  Google Scholar 

  • Abouseoud M, Yataghene A, Amrane A, Maachi R (2010) Production of a biosurfactant by Pseudomonas fluorescens—solubilizing and wetting capacity. J Hazard Mater 183:131–136

    Article  Google Scholar 

  • Adebusoye SA, Ilori MO, Amund OO, Teniola OD, Olatope SO (2007) Microbial degradation of petroleum hydrocarbons in a polluted tropical stream. World J Microbiol Biotechnol 23(8):1149–1159

    Article  CAS  Google Scholar 

  • Akpoveta VO, Osakwe S, Egharevba F, Medjor WO, Asia IO, Ize-Iyamu OK (2012) Surfactant enhanced soil washing technique and its kinetics on the remediation of crude oil contaminated soil. Pac J Sci Technol 13(1):443–456

    Google Scholar 

  • Archaya S, Gopinath LR, Sangeetha S, Bhuvaneswari R (2014) Molecular characterization of kerosene degrading bacteria isolated from kerosene polluted soil. Int J Adv Res 2(4):1117–1124

    Google Scholar 

  • Bacosa H, Suto K, Inoue C (2010) Preferential degradation of aromatic hydrocarbons in kerosene by a microbial consortium. Int Biodeter Biodegr 64:702–710

    Article  CAS  Google Scholar 

  • Bahuguna A, Lily MK, Munjal A, Singh RN, Dangwal K (2011) Desulfurization of dibenzothiophene (DBT) by a novel strain Lysinibacillus sphaericus DMT-7 isolated from diesel contaminated soil. J Environ Sci 23(6):975–982

    Article  CAS  Google Scholar 

  • Barkay T, Navon-Venezia S, Ron EZ, Rosenberg E (1999) Enhancement of solubilization and biodegradation of polyaromatic hydrocarbons by the bioemulsifier alasan. Appl Environ Microbiol 65(6):2697–2702

    CAS  Google Scholar 

  • Bautista FL, Sanz R, Molina MC, Gonzalez N, Sanchez D (2009) Effect of different non-ionic surfactants on the biodegradation of PAHs by diverse aerobic bacteria. Int Biodeter Biodegr 63:913–922

    Article  Google Scholar 

  • Ben Hamed S, Maaroufi A, Ghram A, Zouhaier BAG, Labat M (2013) Isolation of four hydrocarbon effluent-degrading Bacillaceae species and evaluation of their ability to grow under high-temperature or high-salinity conditions. Afr J Biotechnol 12(14):1636–1643

    Google Scholar 

  • Calvo C, Manzanera M, Silva-Castro GA, Uad I, González-López J (2009) Application of bioemulsifiers in soil oil bioremediation processes. Future Prosp Sci Total Environ 407:3634–3640

    Article  CAS  Google Scholar 

  • Chamkha M, Trabelsi Y, Mnif S, Sayadi S (2011) Isolation and characterization of Klebsiellaoxytoca strain degrading crude oil from a Tunisian off-shore oil field. J Basic Microbiol 51:580–589

    Article  CAS  Google Scholar 

  • Champagne P-P, Nesheim ME, Ramsay JA (2010) Effect of a non-ionic surfactant, Merpol, on dye decolorization of reactive blue 19 by laccase. Enzymol Microb Technol 46:147–152

    Article  CAS  Google Scholar 

  • Chander CRS, Lohitnath T, Mukesh Kumar DJ, Kalaichelvan PT (2012) Production and characterization of biosurfactant from Bacillus subtilis MTCC441 and its evaluation to use as bioemulsifier for food bio-preservative. Adv Appl Sci Res 3(3):1827–1831

    Google Scholar 

  • Dayeh VR, Chow SL, Schirmer K, Bols NC (2004) Evaluating the toxicity of Triton X-100 to protozoan, fish, and mammalian cells using fluorescent dyes as indicators of cell viability. Ecotoxicol Environ Saf 57:375–382

    Article  CAS  Google Scholar 

  • Dehghani M, Taatizadeh SB, Samaei MR (2013) Biodegradation of n-Hexadecane in Acinetobacter radioresistens liquid culture. Health Scope 2(3):162–167

    Google Scholar 

  • Fracchia L, Cavallo M, Martinotti MG, Banat IM (2012) Biosurfactants and bioemulsifiers biomedical and related applications—present status and future potentials, biomedical science, engineering and technology. Prof. Dhanjoo N. Ghista (Ed.), (2012) ISBN: 978-953-307-471-9

  • Franzetti A, Caredda P, Ruggeri C, La Colla P, Tamburini E, Papacchini M, Bestetti G (2009) Potential applications of surface active compounds by Gordonia sp. strain BS29 in soil remediation technologies. Chemosphere 75(6):801–807

    Article  CAS  Google Scholar 

  • Ganesh A, Lin J (2009) Diesel degradation and biosurfactant production by gram-positive isolates. Afr J Biotechnol 8(21):5847–5854

    CAS  Google Scholar 

  • Ghribi D, Abdelkefi-Mesrati L, Mnif I, Kammoun R, Ayadi I, Saadaoui I, Maktouf S, Chaabouni-Ellouze S (2012) Investigation of antimicrobial activity and statistical optimization of Bacillus subtilis SPB1 biosurfactant production in solid-state fermentation. J Biomed Biotechnol. doi:10.1155/2012/373682

    Google Scholar 

  • Gudina EJ, Pereira JFB, Costa R, Coutinho JAP, Teixeira JA, Rodrigues LR (2013) Biosurfactant-producing and oil-degrading Bacillus subtilis strains enhance oil recovery in laboratory sand-pack columns. J Hazard Mater 261:106–113

    Article  CAS  Google Scholar 

  • Gül UD, Dönmez G (2012) Effects of dodecyl trimethyl ammonium bromide surfactant on decolorization of remazol blue by a living Aspergillus versicolor strain. J Surfactants Deterg 15:797–803

    Article  Google Scholar 

  • Hadibarata T, Tachibana S (2010) Characterization of phenanthrene degradation by strain Polyporus sp. S133. J Environ Sci 22(1):142–149

    Article  CAS  Google Scholar 

  • Hadibarata T, Adnan LA, Mohd Yusoff AR, Yuniarto A, Meor R, Ahmad Zubir MF, Khudhair AB, Teh ZC, Naser MA (2013) Microbial decolorization of an azo dye reactive black 5 using white-rot fungus Pleurotus eryngii F032. Water Air Soil Pollut 224:1595

    Article  Google Scholar 

  • Helmy Q, Kardena E, Wisjnuprapto (2009) Performance of petrofilic consortia and effect of surfactant tween 80 addition in the oil sludge removal process. J Appl Sci Environ Sanit 4(3):207–218

    Google Scholar 

  • Hu GP, Zhao Y, Song FQ, Liu B, Vasseur L, Douglas C, You MS (2014) Isolation, identification and cyfluthrin-degrading potential of a novel Lysinibacillus sphaericus strain FLQ-11-1. Res Microbiol 165(2):110–118

    Article  CAS  Google Scholar 

  • Hua Z, Chen Y, Du C, Chen J (2004) Effects of biosurfactants produced by Candida antarctica on the biodegradation of petroleum compounds. World J Microbiol Biotechnol 20:25–29

    Article  CAS  Google Scholar 

  • Jadhav M, Kalme S, Tamboli D, Govindwar S (2011) Rhamnolipid from Pseudomonas desmolyticum NCIM-2112 and its role in the degradation of Brown 3REL. J Basic Microbiol 51:385–396

    Article  CAS  Google Scholar 

  • Ji G, Zhang H, Huang F, Huang X (2009) Effects of nonionic surfactant Triton X-100 on the laccase-catalyzed conversion of bisphenol A. J Environ Sci 21:1486–1490

    Article  CAS  Google Scholar 

  • Joutey NT, Bahafid W, Sayel H, ElGhachtouli N (2013) Biodegradation: involved microorganisms and genetically engineered microorganisms. Chapter 11; doi: 10.5772/56194

  • Kristensen JB, Borjesson J, Bruun MH, Tjerneld F, Jørgensen H (2007) Use of surface active additives in enzymatic hydrolysis of wheat straw lignocellulose. Enzymol Microbial Technol 40:888–895

    Article  CAS  Google Scholar 

  • Kumar M, Leon V, De Sisto A, Ilzins OA (2006) Enhancemant of oil degradation by co-culture of hydrocarbon and biosurfactant producing bacteria. Polish J Microbiol 55(2):139–146

    CAS  Google Scholar 

  • Kumar M, Leon V, De Sisto AM, Ilzins OA (2007) A halotolerant and thermotolerant Bacillus sp. degrades hydrocarbons and produces tension-active emulsifying agent. World J Microbiol Biotechnol 23:211–220

    Article  CAS  Google Scholar 

  • Lai C-C, Huang Y-C, Wei Y-H, Chang J-S (2009) Biosurfactant-enhanced removal of total petroleum hydrocarbons from contaminated soil. J Hazard Mater 167(1–3):609–614

    Article  CAS  Google Scholar 

  • Lazaroaie MM (2010) Multiple responses of gram-positive and gram-negative bacteria to mixture of hydrocarbons. Braz J Microbiol 41:649–667

    CAS  Google Scholar 

  • Lily MK, Bahuguna A, Bhatt KK, Garg V, Dangwal K (2012) Strain improvement of a potent benzo-A-pyrene (BAP) degrader Bacillus subtilis BMT4I (MTCC 9447). Int J Adv Biotechnol Res 3(2):570–577

    CAS  Google Scholar 

  • Liu C-W, Liu H-S (2011) Rhodococcus erythropolis strain NTU-1 efficiently degrades and traps diesel and crude oil in batch and fed-batch bioreactors. Process Biochem 46:202–209

    Article  CAS  Google Scholar 

  • Maiti A, Das S, Bhattacharyya N (2012) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons by Bacillus thuringiensis strain NA2. J Sci 1(4):72–75

    Google Scholar 

  • Makkar RS, Rockne KJ (2003) Comparison of synthetic surfactants and biosurfactants in enhanced biodegradation of polycyclic aromatic hydrocarbons. Environ Toxicol Chem 22(10):2280–2292

    Article  CAS  Google Scholar 

  • Marquez-Rocha FJ, Hernandez-Rodriguez V, Lamela MT (2001) Biodegradation of diesel oil by a microbial consortium. Water Air Soil Pollut 128:313–320

    Article  CAS  Google Scholar 

  • Mnif S, Chamkha M, Labat M, Sayadi S (2011) Simultaneous hydrocarbon biodegradation and biosurfactant production by oilfield-selected bacteria. J Appl Microbiol 111:525–536

    Article  CAS  Google Scholar 

  • Mnif I, Ellouze-Chaabouni S, Ghribi D (2012) Response surface methodological approach to optimize the nutritional parameters for enhanced production of lipopeptide biosurfactant in submerged culture by B. subtilis SPB1. J Adv Sci Res 3(1):87–94

    CAS  Google Scholar 

  • Mnif I, Sahnoun R, Ellouze-Chaabouni S, Ghribi D (2013a) Evaluation of B. subtilis SPB1 biosurfactants’ potency for diesel-contaminated soil washing: optimization of oil desorption using Taguchi design. Environ Sci Pollut Res. doi:10.1007/s11356-013-1894-4

    Google Scholar 

  • Mnif I, Ellouze-Chaabouni S, Ghribi D (2013b) Economic production of Bacillus subtilis SPB1 biosurfactant using local agro-industrial wastes and its application in enhancing solubility of diesel. J Chem Technol Biotechnol 88:779–787

    Article  CAS  Google Scholar 

  • Mnif I, Ellouze-Chaabouni S, Ayedi Y, Ghribi D (2014) Treatment of diesel- and kerosene-contaminated water by B. subtilis SPB1 biosurfactant-producing strain. Water Environ Res 86(8):707–716

    Article  CAS  Google Scholar 

  • Moran AC, Olivera N, Commendatore M, Esteves JL, Siñeriz F (2000) Enhancement of hydrocarbon waste biodegradation by addition of a biosurfactant from Bacillus subtilis O9. Biodegradation 11:65–71

    Article  CAS  Google Scholar 

  • Mukred AM, Hamid AA, Hamzah A, Yusoff WM (2008) Development of three bacteria consortium for the bioremediation of crude petroleum-oil in contaminated water. Online J Biol Sci 8(4):73–79

    Article  Google Scholar 

  • Noordman WH, Wahter JH, De Boer GJ, Janssen DB (2002) The enhancement by surfactants of hexadecane degradation by Pseudomonas aeruginosa varies with substrate availability. J Biotechnol 94:195–212

    Article  CAS  Google Scholar 

  • Owsianiak M, Chrzanowski L, Szulc A, Staniewski J, Olszanowski A, Olejnik-Schmidt AK, Heipieper HJ (2009) Biodegradation of diesel/biodiesel blends by a consortium of hydrocarbon degraders: effect of the type of blend and the addition of biosurfactants. Bioresour Technol 100:1497–1500

    Article  CAS  Google Scholar 

  • Pacwa-Plociniczak M, Plaza GA, Piotrowska-Seget Z, Cameotra SS (2011) Environmental applications of biosurfactants: recent advances. Int J Mol Sci 12:633–654

    Article  CAS  Google Scholar 

  • Pavlic Z, Cifrek ZV, Puntaric D (2005) Toxicity of surfactants to green microalgae Pseudokirchneriella subcapitata and Scenedesmus subspicatus and to marine diatoms Phaeodactylum tricornutum and Skeletonema costatum. Chemosphere 61:1061–1068

    Article  CAS  Google Scholar 

  • Reddy MS, Naresh B, Leela T, Prashanthi M, Madhusudhan NC, Dhanasri G, Devi P (2010) Biodegradation of phenanthrene with biosurfactant production by a new strain of Brevibacillus sp. Bioresour Technol 101:7980–7983

    Article  CAS  Google Scholar 

  • Saeki H, Sasaki M, Komatsu K, Miura A, Matsuda H (2009) Oil spill remediation by using the remediation agent JE1058BS that contains a biosurfactant produced by Gordonia sp. strain JE-1058. Bioresour Technol 100:572–577

    Article  CAS  Google Scholar 

  • Santos BF, Ponezi AN, Filetia AMF (2014) Strategy of using waste for biosurfactant production through fermentation by Bacillus subtilis. Chem Eng Trans 37:727–732

    Google Scholar 

  • Sathishkumar M, Binupriya AR, Baik S-H, Yun S-E (2008) Biodegradation of crude oil by individual bacterial strains and a mixed bacterial consortium isolated from hydrocarbon contaminated areas. Clean 36(1):92–96

    CAS  Google Scholar 

  • Shoeb E, Akhlaq F, Badar U, Akhter J, Imtiaz S (2013) Classification and industrial applications of biosurfactants. Part-I: Nat Appl Sci 4(3):242–252

    Google Scholar 

  • Swe MM, Yu LE, Hung K-C, Chen B-H (2006) Solubilization of selected polycyclic aromatic compounds by nonionic surfactants. J Surfactants Deterg 9(3):237–244

    Article  CAS  Google Scholar 

  • Thamer M, Al-Kubaisi AR, Zahraw Z, Abdullah HA, Hindy I, Abd Khadium A (2013) Biodegradation of Kirkuk light crude oil by Bacillus thuringiensis. North Iraq Nat Sci 5(7):865–873

    CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–468

    Article  CAS  Google Scholar 

  • Toren A, Navon-Venezia S, Ron EZ, Rosenberg E (2001) Emulsifying activity of purified alasan proteins from Acinetobacter radioresistens. Appl Environ Microbiol 67:1102–1106

    Article  CAS  Google Scholar 

  • Urum K, Grigson S, Pekdemir T, McMenamy S (2006) A comparison of the efficiency of different surfactants for removal of crude oil from contaminated soils. Chemosphere 62:1403–1410

    Article  CAS  Google Scholar 

  • Van Hamme JD, Ward OP (2001) Physical and metabolic interactions of Pseudomonas sp. Strain JA5-B45 and Rhodococcus sp. Strain F9-D79 during growth on crude oil and effect of a chemical surfactant on them. Appl Environ Microbiol 67:4874–4879

    Article  Google Scholar 

  • Whang L-M, Liu P-WG, Ma C-C, Cheng S-S (2008) Application of biosurfactants, rhamnolipid, and surfactin, for enhanced biodegradation of diesel-contaminated water and soil. J Hazard Mater 151:155–163

    Article  CAS  Google Scholar 

  • Wijanarko A, Yuliani H, Hermansyah H, Sahlan M (2012) Isolation and properties characterization of biosurfactant synthesized by pyrene degrading Bacillus subtilis C19. J Chem Eng 6:889–896

    CAS  Google Scholar 

  • Wong JWC, Fang M, Zhao Z, Xing B (2004) Effect of surfactants on solubilization and degradation of phenanthrene under thermophilic conditions. J Environ Qual 33:2015–2025

    Article  CAS  Google Scholar 

  • Yakimov MM, Denaro R, Genovese M, Cappello S, D’Auria G, Chernikova TN, Timmis KN, Golyshi PN (2005) Natural microbial diversity in superficial sediments of Milazzo Harbor (Sicily) and community successions during microcosm enrichment with various hydrocarbons. Environ Microbiol 7:1426–1441

    Article  CAS  Google Scholar 

  • Yengejeh JR, Sekhavatjou MS, Maktabi P, Arbab Soleimani N, Khadivi S, Pourjafarian V (2014) The biodegradation of crude oil by Bacillus subtilis isolated from contaminated soil in hot weather areas. Int J Environ Res 8(2):509–514

    Google Scholar 

  • Yuliani H, Sahlan M, Hermansyah H, Wijanarko A (2012) Selection and identification of polyaromatic hydrocarbon degrading bacteria. World Appl Sci J 20(8):1133–1138

    CAS  Google Scholar 

  • Zhang Y, Zeng Z, Zeng G, Liud X, Liu Z, Chen M, Liu L, Lie J, Xie G (2012) Effect of Triton X-100 on the removal of aqueous phenol by laccase analyzed with a combined approach of experiments and molecular docking. Colloids Surf B 97:7–12

    Article  CAS  Google Scholar 

  • Zhou MF, Yuan XZ, Zhong H, Liu ZF, Li H, Jiang LL, Zeng GM (2011) Effect of biosurfactants on laccase production and phenol biodegradation in solid-state fermentation. Appl Biochem Biotechnol 164:103–114

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work has been supported by grants from “Tunisian Ministry of Higher Education, Scientific Research and Technology.”

Ethical statement

The experimental protocols were conducted in accordance with the Guide for the Care and Use of Laboratory Animals issued by the University of Sfax, Tunisia, and approved by the Tunisia Committee of Animal Ethics.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Inès Mnif.

Additional information

Responsible editor: Robert Duran

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mnif, I., Mnif, S., Sahnoun, R. et al. Biodegradation of diesel oil by a novel microbial consortium: comparison between co-inoculation with biosurfactant-producing strain and exogenously added biosurfactants. Environ Sci Pollut Res 22, 14852–14861 (2015). https://doi.org/10.1007/s11356-015-4488-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-4488-5

Keywords

Navigation