Applied Microbiology and Biotechnology

, Volume 88, Issue 4, pp 953–963 | Cite as

Cadmium effects on transcriptional expression of rhlB/rhlC genes and congener distribution of monorhamnolipid and dirhamnolipid in Pseudomonas aeruginosa IGB83

  • Julia W. Neilson
  • Lin Zhang
  • Tracey A. Veres-Schalnat
  • Kevin B. Chandler
  • Charlotte H. Neilson
  • Jennifer D. Crispin
  • Jeanne E. Pemberton
  • Raina M. Maier
Applied Microbial and Cell Physiology

Abstract

While variable production of the biosurfactant, rhamnolipid, by Pseudomonas aeruginosa has been shown to be dependent on growth conditions, no research has evaluated potential relationships between rhamnolipid production and the presence of heavy metals. The current investigation evaluates the influence of Cd2+ on rhamnolipid synthesis. Cultures grown in the presence of 0.45 and 0.89 mM Cd2+ were monitored for rhlB/rhlC expression, rhamnolipid yield, and the ratio of monorhamnolipid (RL1) and dirhamnolipid (RL2) produced. Results show a Cd-induced enhancement of rhlB expression in mid-stationary phase (53 h). In addition, sustained production of rhamnolipid through late stationary growth phase (96 h) was observed for Cd-amended cultures, unlike Cd-free control cultures that ceased rhamnolipid production by mid-stationary growth phase. Most significant was an observed increase in the ratio of RL2 to RL1 congeners produced by cultures grown in the presence of Cd2+. Previous results have shown that the complexation constant for RL2–Cd is several orders of magnitude larger than that of RL1–Cd thus the preferential production of RL2 in the presence of Cd2+ impacts its bioavailability and toxicity both for the cell and in the surrounding environment.

Keywords

Rhamnolipid congeners Biosurfactant Cadmium rhlB expression rhlC expression Pseudomonas aeruginosa 

Notes

Acknowledgments

This research was supported by Grant CHE 071-4245 from the US National Science Foundation Collaborative Research in Chemistry program.

References

  1. Al-Tahhan RA, Sandrin TR, Bodour AA, Maier RM (2000) Rhamnolipid-induced removal of lipopolysaccaride from Pseudomonas aeruginosa: effect on cell surface properties and interaction with hydrophobic substrates. Appl Environ Microbiol 66:3262–3268CrossRefGoogle Scholar
  2. Asci Y, Nurbas M, Acikel YS (2008) A comparative study for the sorption of Cd (II) by soils with different clay contents and mineralogy and the recovery of Cd (II) using rhamnolipid biosurfactant. J Hazard Mater 154:663–673CrossRefGoogle Scholar
  3. Bodour AA, Miller-Maier RM (1998) Application of a modified drop-collapse technique for surfactant quantitation and screening of biosurfactant-producing microorganisms. J Microbiol Meth 32:273–280CrossRefGoogle Scholar
  4. Bodour AA, Drees KP, Maier RM (2003) Distribution of biosurfactant-producing bacteria in undisturbed and contaminated arid southwestern soils. Appl Environ Microbiol 69:3280–3287CrossRefGoogle Scholar
  5. Boyer M, Wisneiwski-Dyé F (2009) Cell-cell signaling in bacteria: not simply a matter of quorum. FEMS Microbiol Ecol 70:1–19CrossRefGoogle Scholar
  6. Caiazza NC, Shanks RMQ, O’Toole GA (2005) Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacterial 187:7351–7361CrossRefGoogle Scholar
  7. Davey ME, Caiazza NC, O’Toole GA (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185:1027–1036CrossRefGoogle Scholar
  8. Déziel E, Lépine F, Milot S, Villemur R (2003) rhlA is required for the production of a novel biosurfactant swarming motility in Pseudomonas aeruginosa: 3-(-3-hydroxyalkanoyloxy)alkanoic acids (HAAs), the precursors of rhamnolipids. Microbiol 149:2005–2013CrossRefGoogle Scholar
  9. Drees KP (2004) Quantitative analysis of soil microbial diversity in the hyperarid Atacama Desert, Chile. Dissertation, University of Arizona, pp. 52–85Google Scholar
  10. Duan K, Surette M (2007) Environmental regulation of Pseudomonas aeruginosa PA01 Las and Rhl quorum-sensing systems. J Bacteriol 189:4827–4836CrossRefGoogle Scholar
  11. Green SK, Schroth MN, Cho JJ, Kominos SD, Vitanza-Jack VB (1974) Agricultural plants and soils as a reservoir for Pseudomonas aeruginosa. Appl Microbiol 28:987–991Google Scholar
  12. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, Kumar N, Schembri MA, Song Z, Kristoffersen P, Manefield M, Costerton JW, Molin S, Eberl L, Steinberg P, Kjelleberg S, Høiby N, Givskov M (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803–3815CrossRefGoogle Scholar
  13. Heurlier K, Williams F, Heeb S, Dormond C, Pessi G, Singer D, Cámara M, Williams P, Haas E (2004) Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J Bacteriol 186:2936–2945CrossRefGoogle Scholar
  14. Heyd M, Kohnert A, Tan T-H, Nusser M, Kirschhöfer F, Brenner-Weis G, Franzreb M, Berensmeier S (2008) Development and trends of biosurfactant analysis and purification using rhamnolipid as an example. Anal Bioanal Chem 391:1579–1590CrossRefGoogle Scholar
  15. Hoffman DR, Okon JL, Sandring TR (2005) Medium composition affects the degree and pattern of cadmium inhibition of naphthalene biodegradation. Chemosphere 59:919–927CrossRefGoogle Scholar
  16. Huggett J, Dheda K, Bustin S, Zumla A (2005) Real-time RT-PCR normalization; strategies and considerations. Genes Immun 6:279–284CrossRefGoogle Scholar
  17. Juhas M, Eberl L, Tümmler B (2005) Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ Microbiol 7:459–471CrossRefGoogle Scholar
  18. Kassab DM, Roane TM (2006) Differential responses of a mine tailings Pseudomonas isolate to cadmium and lead exposures. Biodegradation 17:379–387CrossRefGoogle Scholar
  19. Kownatzki R, Tummler B, Doring G (1987) Rhamnolipid of Pseudomonas aeruginosa in sputum of cystic fibrosis patients. Lancet 1:1026–1027CrossRefGoogle Scholar
  20. Lebrón-Paler A (2008) Solution and Interfacial Characterization of Rhamnolipid Biosurfactant from Pseudomonas aeruginosa ATCC 9027. Dissertation, University of ArizonaGoogle Scholar
  21. Lebrón-Paler A, Pemberton JE, Becker BA, Otto WH, Larive CK, Maier RM (2006) Determination of the acid dissociation constant of the biosurfactant monorhamnolipid in aqueous solution by potentiomentric and spectroscopic methods. Anal Chem 78:7649–7658CrossRefGoogle Scholar
  22. Leedjärv A, Ivask A, Virta M (2008) Interplay of different transporters in the mediation of divalent heavy metal resistance in Pseudomonas putida KT2440. J Bacteriol 190:2680–2689CrossRefGoogle Scholar
  23. Leza A, Palmeros B, Garcia JO, Galindo E, Soberón-Chávez G (1996) Xanthomonas campestris as a host for the production of recombinant Pseudomonas aeruginosa lipase. J Indust Microbiol 16:22–28CrossRefGoogle Scholar
  24. Lewinson O, Lee AT, Rees DC (2009) A P-type ATPase importer that discriminates between essential and toxic transition metals. Proc Natl Acad Sci USA 12:4677–4682CrossRefGoogle Scholar
  25. Maier RM, Soberón-Chávez G (2000) Pseudomonas aeruginosa rhamnolipids: biosynthesis and potential applications. Appl Microbiol Biotechnol 54:625–633CrossRefGoogle Scholar
  26. Maslin P, Maier RM (2000) Rhamnolipid-enhanced mineralization of phenanthrene in organic-metal co-contaminated soils. Bioremediation J 4:295–308CrossRefGoogle Scholar
  27. Medina G, Juárez K, Díaz R, Soberón-Chávez G (2003) Transcriptional regulation of Pseudomonas aeruginosa rhlR, encoding a quorum-sensing regulatory protein. Microbiol 149:3073–3081CrossRefGoogle Scholar
  28. Miller RM (1995) Biosurfactant-facilitated remediation of metal-contaminated soils. Environ Health Perspect 103:59–61SCrossRefGoogle Scholar
  29. Mulligan CN, Wang SL (2006) Remediation of a heavy metal-contaminated soil by rhamnolipid foam. Eng Geol 85:75–81CrossRefGoogle Scholar
  30. Nordgård O, Kvaløy JT, Farmen RK, Heikkilä R (2006) Error propagation in relative real-time reverse transcription polymerase chain reaction quantification models: the balance between accuracy and precision. Anal Biochem 356:182–193CrossRefGoogle Scholar
  31. Neilson JW, Artiola JF, Maier RM (2003) Characterization of lead removal from contaminated soils by nontoxic soil-washing agents. J Environ Qual 32:899–908CrossRefGoogle Scholar
  32. Ochoa-Loza FJ, Artiola JF, Maier RM (2001) Stability constants for the complexation of various metals with a rhamnolipid biosurfactant. J Environ Qual 30:479–485CrossRefGoogle Scholar
  33. Ochsner UA, Fiechter A, Reiser J (1994) Isolation, characterization, and expression in Escherichia coli of the Pseudomonas aeruginosa rhlAB genes encoding a rhamnosyltransferase involved in rhamnolipid biosurfactant synthesis. J Biol Chem 269:19787–19795Google Scholar
  34. Pamp SJ, Tolker-Nielsen T (2007) Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa. J Bacteriol 189:2531–2539CrossRefGoogle Scholar
  35. Pellet S, Bigley DV, Grimes DJ (1983) Distribution of Pseudomonas aeruginosa in a riverine ecosystem. Appl Environ Microbiol 45:328–332Google Scholar
  36. Perron K, Caille O, Rossier C, Van Delden C, Dumas J, Köhler T (2004) CzcR-CzcS, a two-component system involved in heavy metal and carbapenem resistance in Pseudomonas aeruginosa. J Biol Chem 279:8761–8768CrossRefGoogle Scholar
  37. Pfaffl MW (2001) A new mathematical model for relative quantification on real-time RT-PCR. Nucleic Acids Res 29:e45CrossRefGoogle Scholar
  38. Rahim R, Achsner UA, Olvera C, Graninger M, Messner P, Lam JS, Soberón-Chávez G (2001) Cloning and functional characterization of the Pseudomonas aeruginosa rhlC gene that encodes rhamnosyltransferase 2, an enzyme responsible for di-rhamnolipid biosynthesis. Mol Microbiol 40:708–718CrossRefGoogle Scholar
  39. Raja CE, Sasikumar S, Selvam GS (2008) adaptive and cross resistance to cadmium (II) and zinc (II) by Pseudomonas aeruginosa BC15. Biologia 4:461–465CrossRefGoogle Scholar
  40. Sandrin TR, Chech AM, Maier RM (2000) a rhamnolipid biosurfactant reduces cadmium toxicity during naphthalene biodegradation. Appl Environ Microbiol 66:4585–4588CrossRefGoogle Scholar
  41. Savli H, Karadenizli A, Kolayli F, Gundes S, Ozbek U, Vahaboglu H (2003) Expression stability of six housekeeping genes: a proposal for resistance gene quantification studies of Pseudomonas aeruginosa by real-time quantitative RT-PCR. J Med Microbiol 52:403–408CrossRefGoogle Scholar
  42. Schuster M, Greenberg EP (2006) A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296:73–81CrossRefGoogle Scholar
  43. Schuster M, Lostroh CP, Ogi T, Greenberg EP (2003) Identification, timing and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185:2066–2079CrossRefGoogle Scholar
  44. Soberón-Chávez G, Lépine F, Déziel E (2005) Production of rhamnolipids by Pseudomonas aeruginosa. Appl Microbiol Biotechnol 68:718–725CrossRefGoogle Scholar
  45. Wagner VE, Bushnell D, Passador L, Brooks AI, Iglewski BH (2003) Microarray analysis of Pseudomonas aeruginosa quorum sensing regulons: effects of growth phase and environment. J Bacteriol 185:2080–2095CrossRefGoogle Scholar
  46. Zhang Y, Miller RM (1994) Effect of a Pseudomonas rhamnolipid biosurfactant on cell hydrophobicity and biodegradation of octadecane. Appl Environ Microbiol 60:2101–2106Google Scholar
  47. Zhu K, Rock CO (2008) RhlA converts β-hydroxyacyl-acyl carrier protein intermediates in fatty acid synthesis to the β-hydroxydecanoyl-β-hydroxydecanoate component of rhamnolipids in Pseudomonas aeruginosa. J Bacteriol 190:3147–3154CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Julia W. Neilson
    • 1
  • Lin Zhang
    • 1
  • Tracey A. Veres-Schalnat
    • 2
  • Kevin B. Chandler
    • 1
  • Charlotte H. Neilson
    • 1
  • Jennifer D. Crispin
    • 1
  • Jeanne E. Pemberton
    • 2
  • Raina M. Maier
    • 1
  1. 1.Department of Soil, Water, and Environmental ScienceUniversity of ArizonaTucsonUSA
  2. 2.Department of Chemistry and BiochemistryUniversity of Arizona,1306 E. University BoulevardTucsonUSA

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