Skip to main content

Advertisement

SpringerLink
Log in

Effects of Rhamnolipids from Pseudomonas aeruginosa DS10-129 on Luminescent Bacteria: Toxicity and Modulation of Cadmium Bioavailability

  • Physiology and Biotechnology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

In this study, the mixture of mono- and di-rhamnolipids produced by Pseudomonas aeruginosa DS10-129 was characterized for its toxicity and modulatory effects on Cd availability to different bacteria. Gram-negative naturally bioluminescent Vibrio fischeri and recombinant bioluminescent Pseudomonas fluorescens, P. aeruginosa, Escherichia coli, and Gram-positive Bacillus subtilis were used as model organisms. Rhamnolipids reduced the bioluminescence of these bacteria in less than a second of exposure even in relatively low concentrations (30-min EC50 45–167 mg l−1). Toxicity of Cd to Gram-negative bacteria (30-min EC50 values 0.16 mg l−1 for E. coli, 0.96 mg l−1 for P. fluorescens, and 4.4 mg l−1 for V. fischeri) was remarkably (up to 10-fold) reduced in the presence of 50 mg l−1 rhamnolipids. Interestingly, the toxicity of Cd to Gram-positive B. subtilis (30-min EC50 value 0.49 mg l−1) was not affected by rhamnolipids. Rhamnolipids had an effect on desorption of Cd from soil: 40 mg l−1 rhamnolipids increased the water-extracted fraction of Cd twice compared with untreated control. However, this additionally desorbed fraction of Cd remained bound with rhamnolipids and was not available to bacteria. Hence, in carefully chosen concentrations (still effectively complexing heavy metals but not yet toxic to soil bacteria), rhamnolipids could be applied in remediation of polluted areas.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  1. Al-Tahhan R, Sandrin TR, Bodour AA, Maier RM (2000) Rhamnolipid-induced removal of lipopolysaccharide from Pseudomonas aeruginosa: effect on cell surface properties and interaction with hydrophobic substrates. Appl Environ Microbiol 66:3262–3268

    Article  CAS  PubMed  Google Scholar 

  2. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Strahl K (1987) Current protocols in molecular biology. Wiley, New York

    Google Scholar 

  3. Benincasa M, Abalos A, Oliveira I, Manresa A (2004) Chemical structure, surface properties and biological activities of the biosurfactant produced by Pseudomonas aeruginosa LBI from soap stock. Antonie Van Leeuwenhoek 1:1–8

    Article  Google Scholar 

  4. Bondarenko O, Rõlova T, Kahru A, Ivask A (2008) Bioavailability of Cd, Zn and Hg in soil to nine recombinant luminescent metal sensor bacteria. Sensors 8(11):6899–6923

    Article  CAS  Google Scholar 

  5. Bulich AA (1982) A practical and reliable method for monitoring the toxicity of aquatic samples. Process Biochem 17:45–47

    Google Scholar 

  6. Chandrasekaran EV, Bemiller JN (1980) Constituent analyses of glycosaminoglycans. Methods in carbohydrate chemistry. Academic, New York, pp 89–96

    Google Scholar 

  7. Guo YP, Hu YY, Gu RR, Lin H (2009) Characterization and micellization of rhamnolipidic fractions and crude extracts produced by Pseudomonas aeruginosa mutant MIG-N146. J Colloid Interface Sci 331(2):356–363

    Article  CAS  PubMed  Google Scholar 

  8. Haba E, Pinazo A, Jauregui O, Espuny MJ, Infante MR, Manresa A (2003) Physicochemical characterization and antimicrobial properties of rhamnolipids produced by Pseudomonas aeruginosa 47 T2 NCBIM 40044. Biotechnol Bioeng 81(3):316–22

    Article  CAS  PubMed  Google Scholar 

  9. Helander IM, Mattila-Sandholm T (2000) Fluorometric assessment of Gram-negative bacterial permeabilization. J Appl Microbiol 88:213–219

    Article  CAS  PubMed  Google Scholar 

  10. Higgins DG, Sharp PM (1988) CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73:237–244

    Article  CAS  PubMed  Google Scholar 

  11. Ivask A, Francois M, Kahru A, Dubourguier HC, Virta M, Douay F (2004) Recombinant luminescent bacterial sensors for the measurement of bioavailability of cadmium and lead in soils polluted by metal smelters. Chemosphere 22:147–156

    Article  CAS  Google Scholar 

  12. Ivask A, Rõlova T, Kahru A (2009) A suite of recombinant luminescent bacterial strains for the quantification of bioavailable heavy metals and toxicity testing. BMC Biotech 9:41. doi:10.1186/1472-6710-9-41

    Article  CAS  Google Scholar 

  13. Ivask A, Virta M, Kahru A (2002) Construction and use of specific luminescent recombinant bacterial sensors for the assessment of bioavailable fraction of cadmium, zinc, mercury and chromium in the soil. Soil Biol Biochem 34(10):1439–1447

    Article  CAS  Google Scholar 

  14. Juwarkar A, Anupa N, Dubey KV, Singh SK, Sukumar D (2007) Biosurfactant technology for remediation of cadmium and lead contaminated soils. Chemosphere 68(10):1996–2002

    Article  CAS  PubMed  Google Scholar 

  15. Kahru A (1993) In vitro toxicity testing using marine luminescent bacteria Photobacterium phosphoreum: the Biotox™ test. ATLA 21(2):210–215

    Google Scholar 

  16. Kahru A, Ivask A, Kasemets K, Põllumaa L, Kurvet I, François M, Dubourguier HC (2005) Biotests and biosensors in ecotoxicological risk assessment of field soils polluted with zinc, lead and cadmium. Environ Toxicol Chem 24(11):2973–2982

    Article  CAS  PubMed  Google Scholar 

  17. Kim IS, Park JS, Kim KW (2001) Enhanced biodegradation of polycyclic aromatic hydrocarbons using nonionic surfactants in soil slurry. Appl Geochem 16:1419–1428

    Article  CAS  Google Scholar 

  18. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  19. Leedjärv A, Ivask A, Virta M, Kahru A (2006) Analysis of bioavailable phenols from natural samples by recombinant luminescent bacterial sensors. Chemosphere 64:1910–1919

    Article  PubMed  CAS  Google Scholar 

  20. Maslin PM, Maier RM (2000) Rhamnolipid enhanced mineralization of phenanthrene in organic metal co-contaminated soils. Bioremed J 4:295–308

    Article  CAS  Google Scholar 

  21. Matsufuji M, Nakata K, Yoshimoto A (1997) High production of rhamnolipids by Pseudomonas aeruginosa growing on ethanol. Biotechnol Lett 19:1213–1215

    Article  CAS  Google Scholar 

  22. Meighen EA (1991) Molecular biology of bacterial bioluminescence. Microbiol Rev 55:123–142

    CAS  PubMed  Google Scholar 

  23. Mortimer M, Kasemets K, Heinlaan M, Kurvet I, Kahru A (2008) High throughput kinetic Vibrio fischeri bioluminescence inhibition assay for study of toxic effects of nanoparticles. Toxicol Vitro 22(5):1412–1417

    Article  CAS  Google Scholar 

  24. Mulligan CN, Yong RN, Gibbs BF (2001) Heavy metal removal from sediments by biosurfactants. J Hazard Mater 85:111–125

    Article  CAS  PubMed  Google Scholar 

  25. Nitschke M, Costa SGVAO (2007) Biosurfactants in food industry. Trends Food Sci Technol 18(5):252–259

    Article  CAS  Google Scholar 

  26. Ochoa-Loza FJ, Artiola JF, Maier RM (2001) Stability constants for the complexation of various metals with a rhamnolipid biosurfactant. J Environ Qual 30(2):479–485

    Article  CAS  PubMed  Google Scholar 

  27. Pornsunthorntawee O, Wongpanit P, Chavadej S, Abe M, Rujiravanit R (2008) Structural and physicochemical characterization of crude biosurfactant produced by Pseudomonas aeruginosa SP4 isolated from petroleum-contaminated soil. Bioresour Technol 99:1589–1595

    Article  CAS  PubMed  Google Scholar 

  28. Rahman KSM, Rahman TJ, Lakshmanaperumalsamy P, Marchant R, Banat IM (2002) Emulsification potential of bacterial isolates with a range of hydrocarbon substrates. Acta Biotechnol 23:335–345

    Article  Google Scholar 

  29. Rahman KSM, Rahman TJ, McClean S, Marchant R, Banat IM (2002) Rhamnolipid biosurfactants production by strains of Pseudomonas aeruginosa using low cost raw materials. Biotechnol Prog 18:1277–1281

    Article  CAS  PubMed  Google Scholar 

  30. Ramos JL, Duque E, Gallegos MT, Godoy P, Ramos-Gonzalez MI, Rojas A, Teran W, Segura A (2002) Mechanisms of solvent tolerance in Gram-negative bacteria. Annu Rev Microbiol 56:743–768

    Article  CAS  PubMed  Google Scholar 

  31. Rodrigues L, Banat IM, Teixeira J, Oliveira R (2006) Biosurfactants: potential applications in medicine. J Antimicrob Chemother 57:609–618

    Article  CAS  PubMed  Google Scholar 

  32. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  33. Sandrin TR, Chech AM, Maier RM (2000) A rhamnolipid biosurfactant reduces cadmium toxicity during naphthalene biodegradation. Appl Environ Microbiol 66:4585–4588

    Article  CAS  PubMed  Google Scholar 

  34. Shin KH, Ahn Y, Kim KW (2005) Toxic effect of biosurfactant addition on the biodegradation of phenanthrene. Environ Toxicol Chem 24(11):2768–2774

    Article  CAS  PubMed  Google Scholar 

  35. Stacey SP, McLaughlin MJ, Cakmak I, Hettiarachchi GM, Scheckel KG, Karkkainen M (2008) Root uptake of lipophilic zinc–rhamnolipid complexes. J Agric Food Chem 56(6):2112–2117

    Article  CAS  PubMed  Google Scholar 

  36. Villaescusa I, Martinez M, Pilar M, Murat JC, Hostan C (1996) Toxicity of cadmium species in luminescent bacteria. Fresenius J Anal Chem 354:566–570

    CAS  Google Scholar 

  37. Wang X, Gong L, Liang S, Xiurong Han X, Zhu C, Li Y (2005) Algicidal activity of rhamnolipid biosurfactants produced by Pseudomonas aeruginosa. Harmful Algae 4:433–443

    Article  CAS  Google Scholar 

  38. Zhang Y, Miller RM (1992) Enhanced octadecane dispersion and biodegradation by a Pseudomonas rhamnolipid surfactant (biosurfactant). Appl Environ Microbiol 58(10):3276–3282

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Estonian Ministry of Science and Education (targeted funding project SF0690063s08), Maj and Tor Nessling Foundation (grant no 2008416), Estonian Science Foundation (grant no 6974), and European Social Fund. We thank Prof. Henri-Charles Dubourguier for fruitful discussions, Thomas Leydier for help in chemical analysis of the samples, Sirje Vija for her advice in thin-layer chromatography, and Martin Romantshuk for P. fluorescens OS8 strain. PKSM Rahman thanks the Teesside University-sponsored Research and Enterprise Development Fund and Higher Education Innovation Fund (HEIF) for their support towards the completion of this project and the Bioscience for Business-Knowledge Transfer Network (BfB-KTN) for the award of “From Renewable Platform Chemicals to Value Added Products” (FROPTOP) fund to explore the biocatalytic study of biosurfactant production from renewable resources.

Author information

Authors and Affiliations

  1. Laboratory of Molecular Genetics, National Institute of Chemical Physics and Biophysics, Tallinn, Estonia

    Olesja Bondarenko, Anne Kahru & Angela Ivask

  2. Chemical and Bioprocess Engineering Group, School of Science and Technology, Teesside University, Middlesbrough, UK

    Pattanathu K. S. M. Rahman

  3. Institute of Human Genetics, Newcastle University, Newcastle upon Tyne, UK

    Thahira J. Rahman

  4. Akadeemia tee 23, 12618, Tallinn, Estonia

    Angela Ivask

Authors
  1. Olesja Bondarenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pattanathu K. S. M. Rahman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thahira J. Rahman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anne Kahru
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Angela Ivask
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Angela Ivask.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bondarenko, O., Rahman, P.K.S.M., Rahman, T.J. et al. Effects of Rhamnolipids from Pseudomonas aeruginosa DS10-129 on Luminescent Bacteria: Toxicity and Modulation of Cadmium Bioavailability. Microb Ecol 59, 588–600 (2010). https://doi.org/10.1007/s00248-009-9626-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-009-9626-5

Keywords

Search

Navigation