Skip to main content
Log in

Synergistic Effect of Rhamnolipids and Inoculation on the Bioremediation of Petroleum-Contaminated Soils by Bacterial Consortia

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Crude oil is a serious soil pollutant, requiring large-scale remediation efforts. Bacterial consortia in combination with rhamnolipids can be an effective bioremediation method. However, the underlying mechanisms and associated changes in soil bacterial composition remain uncharacterized. Therefore, this study sought to evaluate the effectiveness of rhamnolipids in petroleum hydrocarbon removal, and the associated bacterial community dynamics during bioremediation of petroleum-contaminated soils. Contaminated soils were subjected to natural attenuation, bioremediation with rhamnolipids, bioremediation with bacterial consortia, or bioremediation with bacterial consortia supplemented with rhamnolipids (BMR). High-throughput sequencing of bacterial sample partial 16S rRNA sequences was performed. Additionally, the n-alkanes and aromatic fractions were analyzed by gas chromatography-mass spectroscopy. The results showed that rhamnolipid supplementation increased the rate and extent of total petroleum hydrocarbon biodegradation to a maximum of 81% within 35 days. Further, phylogenetic analysis revealed that the bacterial community was composed of 14 phylotypes (similarity level = 97%). Actinobacteria and Proteobacteria were the two core phyla in all samples, accounting for 63–89%, but Proteobacteria was the most dominant phylum in the BMR sample (~ 53%). Among the top 20 genera, Pseudomonas, Pseudoxanthomonas, Cavicella, Mycobacterium, Rhizobium, and Acinetobacter were more abundant in BMR samples compared to other samples. Predicted functional profiles revealed that rhamnolipid addition also induced changes in gene abundance related to hydrocarbon metabolic pathways. This study provided comprehensive insights into the synergistic effect of rhamnolipids and bacterial consortia for altering bacterial populations and specific functional traits, which may serve to improve bacteria-mediated petroleum hydrocarbon biodegradation in contaminated soils.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Hu G, Li J, Zeng G (2013) Recent development in the treatment of oily sludge from petroleum industry: a review. J Hazard Mater 261:470–490

    Article  CAS  PubMed  Google Scholar 

  2. Widdel F, Rabus R (2001) Anaerobic biodegradation of saturated and aromatic HCs. Curr Opin Biotechnol 12:259–276. https://doi.org/10.1016/S0958-1669(00)00209-3

    Article  PubMed  CAS  Google Scholar 

  3. Costa SG, Nitschke M, Lepine F (2010) Structure, properties and applications of rhamnolipids produced by Pseudomonas aeruginosa L2–1 from cassava wastewater. Process Biochem 45:1511–1516

    Article  CAS  Google Scholar 

  4. Brzeszcz J, Kaszycki P (2018) Aerobic bacteria degrading both n-alkanes and aromatic hydrocarbons: an undervalued strategy for metabolic diversity and flexibility. Biodegradation 29:359–407

    Article  PubMed  Google Scholar 

  5. Charles H, Stanley DR, Jeffrey WS, Daniel E, James LB, Brenda EB, David BI (2013) Long-term ecosystem response to the Exxon Valdez oil spill. Science 302:2082–2086

    Google Scholar 

  6. Megharaj M, Ramakrishnan B, Venkateswarlu K, Sethunathan N, Naidu R (2011) Bioremediation approaches for organic pollutants: a critical perspective. Environ Int 37:1362–1375

    Article  CAS  PubMed  Google Scholar 

  7. Jasmine J, Mukherji S (2015) Characterization of oily sludge from a refinery and biodegradability assessment using various hydrocarbon degrading strains and reconstituted consortia. J Environ Manage 149:118–125

    Article  CAS  PubMed  Google Scholar 

  8. Smith E, Thavamani P, Ramadass K, Naidu R, Srivastava P, Megharaj M (2015) Remediation trials for hydrocarbon-contaminated soils in arid environments: evaluation of bioslurry and biopiling techniques. Int Biodeterior Biodegrad 101:56–65

    Article  CAS  Google Scholar 

  9. Zhao Z, Ammaiyappan S, Jonathan W (2011) Effects of rhamnolipids on cell surface hydrophobicity of PAH degrading bacteria and the biodegradation of phenanthrene. Bioresource Technol 102:3999–4007

    Article  CAS  Google Scholar 

  10. Trellu CG, Oleksandra PS (2016) Combination of anodic oxidation and biological treatment for the removal of phenanthrene and Tween 80 from soil washing solution. Chem Eng J 306:588–596

    Article  CAS  Google Scholar 

  11. Zhang H, Tang J, Wang L, Liu J, Gurav RG, Sun K (2016) A novel bioremediation strategy for petroleum hydrocarbon pollutants using salt tolerant Corynebacterium variabile HRJ4 and biochar. J Environ Sci 47:7–13

    Article  CAS  Google Scholar 

  12. Cheng M, Zeng G, Huang D, Yang C, Lai C, Zhang C, Liu Y (2017) Advantages and challenges of Tween 80 surfactant-enhanced technologies for the remediation of soils contaminated with hydrophobic organic compounds. Chem Eng J 314:98–113

    Article  CAS  Google Scholar 

  13. Zhong H, Liu G, Jiang Y, Yang J, Liu Y, Yang X, Liu Z, Zeng G (2017) Transport of bacteria in porous media and its enhancement by surfactants for bioaugmentation: a review. Biotechnol Adv 35:490–504

    Article  CAS  PubMed  Google Scholar 

  14. Wang X, Sun L, Wang H, Wu H, Chen S, Zheng X (2017) Surfactant-enhanced bioremediation of DDTs and PAHs in contaminated farmland soil. Environ Technol 39:1–21. https://doi.org/10.1080/09593330.2017.1337235

    Article  CAS  Google Scholar 

  15. Zeng ZT, Liu Y, Zhong H, Xiao R, Zeng GM, Liu ZF, Cheng M, Lai C, Zhang C, Liu GS, Qin L (2018) Mechanisms for rhamnolipids-mediated biodegradation of hydrophobic organic compounds. Sci Total Environ 634:1–11. https://doi.org/10.1016/j.scitotenv.2018.03.349

    Article  PubMed  CAS  Google Scholar 

  16. Lu C, Hong Y, Liu J, Gao YZ, Ma Z, Yang B, Ling WT, Waigi MG (2019) A PAH-degrading bacterial community enriched with contaminated agricultural soil and its utility for microbial bioremediation. Environ Pollut 251:773–782

    Article  CAS  PubMed  Google Scholar 

  17. Chakraborty J, Das S (2016) Molecular perspectives and recent advances in microbial remediation of persistent organic pollutant. Environ Sci Pollut Res 23(17):16883–16903

    Article  CAS  Google Scholar 

  18. Ma K, Sun M, Dong W, He C, Chen F, Ma Y (2016) Effects of nutrition optimization strategy on rhamnolipid production in a Pseudomonas aeruginosa strain DN1 for bioremediation of crude oil. Biocatal Agric Biotechnol 6:144–151. https://doi.org/10.1016/j.bcab.2016.03.008

    Article  Google Scholar 

  19. Zhu S, Liang S, You X (2013) Effect of rhamnolipid biosurfactant on solubilization and biodegradation of polycyclic aromatic hydrocarbons, [C]// third international conference on intelligent system design and engineering applications. IEEE. https://doi.org/10.1109/SDEA.2012.156

    Article  Google Scholar 

  20. Congiu E, Parsons J, Ortega CJ (2015) Dual partitioning and attachment effects of rhamnolipid on pyrene biodegradation under bioavailability restrictions. Environ Pollut 205:378–384

    Article  CAS  PubMed  Google Scholar 

  21. Liu Y, Zeng GM, Zhong H, Wang ZQ, Liu ZF, Cheng M, Liu GS, Yang X, Liu SH (2017) Effect of rhamnolipid solubilization on hexadecane bioavailability: enhancement or reduction? J Hazard Mater 322 (part B): 394–401.

    Article  CAS  PubMed  Google Scholar 

  22. Singh P, Jain R, Srivastava N, Borthakur A, Pal DB, Singh R (2017) Current and emerging trends in bioremediation of petrochemical waste: a review. Crit Rev Environ Sci Technol 47(3):155–201

    Article  Google Scholar 

  23. Zhong H, Liu Y, Liu Z, Jiang Y, Fei T, Zeng G, Yuan X (2014) Degradation of pseudo-solubilized and mass hexadecane by a Pseudomonas aeruginosa with treatment of rhamnolipid biosurfactant. Int Biodeterior Biodegrad 94:152–159

    Article  CAS  Google Scholar 

  24. Li J, Xue S, He C, Qi H, Chen F, Ma Y (2018) Effect of exogenous inoculants on enhancing oil recovery and indigenous bacterial community dynamics in long-term field pilot of low permeability reservoir. World J Microb Biotechnol 34:53

    Article  CAS  Google Scholar 

  25. He CQ, Dong W, Li J, Li YP, Huang C, Ma YL (2017) Characterization of rhamnolipid biosurfactants produced by recombinant Pseudomonas aeruginosa strain DAB with removal of crude oil. Biotechnol Lett 39(9):1381–1388. https://doi.org/10.1007/s10529-017-2370-x

    Article  PubMed  CAS  Google Scholar 

  26. Huang C, Li Y, Tian Y, Hao Z, Ma Y (2018) Enhanced rhamnolipid production of Pseudomonas aeruginosa DN1 by metabolic engineering under diverse nutritional factors. J Pet Environ Biotechnol 9:384. https://doi.org/10.4172/2157-7463.1000384

    Article  Google Scholar 

  27. Leys N, Bastiaens L, Verstraete W, Springael D (2005) Influence of the carbon/nitrogen /phosphorus ratio on polycyclic aromatic hydrocarbon degradation by Mycobacterium and Sphingomonas in soil. Appl Microbiol Biotechnol 66:726–736. https://doi.org/10.1007/s00253-004-1766-4

    Article  PubMed  CAS  Google Scholar 

  28. Huesemann MH (1995) Predictive model for estimating the extent of petroleum hydrocarbon biodegradation in contaminated soils. Environ Sci Technol 29:7–18

    Article  CAS  PubMed  Google Scholar 

  29. Wu M, Li W, Dick WA, Ye X, Chen K, Kost D, Chen L (2017) Bioremediation of hydrocarbon degradation in a petroleum-contaminated soil and microbial population and activity determination. Chemosphere 169:124–130

    Article  CAS  PubMed  Google Scholar 

  30. Caporaso JG, Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996

    Article  CAS  PubMed  Google Scholar 

  32. Edgar RC, Haas B, Clemente JC, Quince C, Knight R (2011) UCHIIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60

    PubMed  PubMed Central  Google Scholar 

  34. AßHauer KP, Bernd W, Rolf D, Peter M (2015) Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 31:2882–2884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Wang S, Xiang W, Chao Z, Li F, Guo G (2016) Bioremediation of oil sludge contaminated soil by landfarming with added cotton stalks. Int Biodeterior Biodegrad 106:150–156

    Article  CAS  Google Scholar 

  36. Liu G, Zhong H, Jiang Y, Brusseau ML, Huang J, Shi L (2017) Effect of low-concentration rhamnolipid biosurfactant on Pseudomonas aeruginosa transport in natural porous media. Water Resour Res 53:361–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Chebbi A, Hentati D, Zaghden H, Baccar N, Rezgui F, Chalbi M, Sayadi S, Chamkha M (2017) Polycyclic aromatic hydrocarbon degradation and biosurfactant production by a newly isolated Pseudomonas sp. strain from used motor oil-contaminated soil. Int Biodeterior Biodegrad 122:128–140

    Article  CAS  Google Scholar 

  38. Hitoshi I, Hosokawa R, Morikawa M, Okuyama H (2008) A turbine oil-degrading bacterial consortium soils of oil fields and its characteristics. Int Biodeterior Biodegrad 61:223–232

    Article  CAS  Google Scholar 

  39. Olajuyigbe FM, Ehiosun KI (2016) Assessment of crude oil degradation efficiency of newly isolated actinobacteria reveals untapped bioremediation potentials. Bioremediat J 20:133–143

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. 31000069), and the Key Project on Social Development of Science and Technology in Shaanxi Province (Grant No. 2017ZDXM-SF-102).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yan-ling Ma.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Additional information

Publisher's Note

Springer Nature 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

Xue, Sw., Huang, C., Tian, Yx. et al. Synergistic Effect of Rhamnolipids and Inoculation on the Bioremediation of Petroleum-Contaminated Soils by Bacterial Consortia. Curr Microbiol 77, 997–1005 (2020). https://doi.org/10.1007/s00284-020-01899-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-020-01899-3

Navigation