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Applied Microbiology and Biotechnology

, Volume 89, Issue 5, pp 1573–1581 | Cite as

Long-term influence of the presence of a non-aqueous phase on the cell surface hydrophobicity of Pseudomonas in two-phase partitioning bioreactors

  • María Hernández
  • Raúl Muñoz TorreEmail author
Applied Microbial and Cell Physiology

Abstract

The long-term influence of silicone oil 200 cSt (SO200) and 2, 2, 4, 4, 6, 8, 8-heptamethylnonane (HMN) on the cell surface hydrophobicity (CSH) of a hexane-degrading Pseudomonas aeruginosa strain and a toluene-degrading Pseudomonas putida strain was assessed in two-phase partitioning bioreactors under batch and continuous operation. CSH was evaluated using a modified BATH method based on optical density (CSHOD) and colony-forming unit (CSHCFU) measurements. In the presence of HMN, P. aeruginosa turned hydrophobic over the time course as shown by the gradual increase in CSHOD (61 ± 1%) and CSHCFU (53 ± 3%) under batch degradation and in CSHOD (49 ± 0%) under continuous operation. However, P. putida turned hydrophobic only under continuous operation (\( {\hbox{CS}}{{\hbox{H}}_{\rm{OD}}} = 28 \pm 2\% \)). On the other hand, no significant CSH enhancement was observed in both Pseudomonas strains in the presence of SO200. These results suggested that CSH is species, non-aqueous phase, and cultivation mode dependant, and an inducible property of bacteria. Maximum hexane elimination capacities increased by 2 and 3 in the presence of SO200 and HMN, respectively. Based on the absence of CSH in P. aeruginosa in the presence of SO200, the higher elimination capacities recorded were likely due to an improved hexane mass transfer (physical effect). However, in the presence of HMN, a direct hexane uptake from the non-aqueous phase (biological effect) might have also contributed to this enhancement.

Keywords

Cell surface hydrophobicity 2, 2, 4, 4, 6, 8, 8-heptamethylnonane Pseudomonas Silicone oil Two-phase partitioning bioreactors 

Notes

Acknowledgments

This research was supported by the Spanish Ministry of Education and Science (RYC-2007-01667 and BES-2007-15840 contracts, and projects CTQ2009-07601 and CONSOLIDER-CSD 2007-00055). Dr. Marcia Morales and Dr. Ana Segura are also gratefully acknowledged for kindly supplying the bacterial strains used in this investigation.

References

  1. Allison DG, Brown MRW, Evans DE, Gilbert P (1990) Surface hydrophobicity and dispersal of Pseudomonas aeruginosa from biofilms. FEMS Microbiol Lett 71:101–104. doi: 10.1016/0378-1097(90)90039-S CrossRefGoogle Scholar
  2. Ascon Cabrera MA, Lebeault JM (1995) Cell hydrophobicity influencing the activity/stability of xenobiotic-degrading microorganisms in a continuous biphasic aqueous–organic system. J Ferment Bioeng 80:270–275. doi: 10.1016/0922-338X(95)90828-N CrossRefGoogle Scholar
  3. Baoyu G, Xiaobiao Z, Chunhua X, Qinyan Y, Weiwei L, Jincheng W (2008) Influence of extracellular polymeric substances on microbial activity and cell hydrophobicity in biofilms. J Chem Technol Biotechnol 83:227–232. doi: 10.1002/jctb.1792 CrossRefGoogle Scholar
  4. Bordel S, Muñoz R, Díaz LF, Villaverde S (2007) New insights on toluene biodegradation by Pseudomonas putida F1: influence of pollutant concentration and excreted metabolites. Appl Microbiol Biotechnol 74:857–866. doi: 10.1007/s00253-006-0724-8 CrossRefGoogle Scholar
  5. Boudreau NG, Daugulis AJ (2006) Transient performance of two-phase partitioning bioreactors treating a toluene contaminated gas stream. Biotechnol Bioeng 94:448–457. doi: 10.1002/bit.20876 CrossRefGoogle Scholar
  6. Bunt CR, Jones DS, Tucker IG (1995) The effects of pH, ionic strength and polyvalent ions on the cell surface hydrophobicity of Escherichia coli evaluated by the BATH and HIC methods. Int J Pharm 113:257–261. doi: 10.1016/0378-5173(94)00205-J CrossRefGoogle Scholar
  7. Cesário MT, Beverloo WA, Tramper J, Befftink HH (1997) Enhancement of gas–liquid mass transfer rate of apolar pollutants in the biological waste gas treatment by a dispersed organic solvent. Enzyme Microb Technol 21:578–588. doi: 10.1016/S0141-0229(97)00069-0 CrossRefGoogle Scholar
  8. Chrzanowski L, Kaczorec E, Olszanowski A (2005) Relation between Candida maltosa hydrophobicity and hydrocarbon biodegradation. World J Microbiol Biotechnol 21:1273–1277. doi: 10.1007/s11274-005-2107-1 CrossRefGoogle Scholar
  9. Chrzanowski L, Bielicka-Daszkiewicz K, Owsianiak M, Aurich A, Kaczorek E, Olszanowski A (2008) Phenol and n-alkanes (C12 and C16) utilization: influence on yeast cell surface hydrophobicity. World J Microbiol Biotechnol 24:1943–1949. doi: 10.1007/s11274-008-9704-8 CrossRefGoogle Scholar
  10. Déziel E, Comeau Y, Villemur (1999) Two-liquid-phase bioreactors for enhanced degradation of hydrophobic/toxic compounds. Biodegradation 10:219–233. doi: 10.1023/A:1008311430525 CrossRefGoogle Scholar
  11. Gaur R, Khare SK (2009) Cellular response mechanisms in Pseudomonas aeruginosa PseA during growth in organic solvents. Lett Appl Microbiol 49:372–377. doi: 10.1111/j.1472-765X.2009.02671.x CrossRefGoogle Scholar
  12. Hancock IC (1991) Microbial cell surface architecture. In: Mozes N (ed) Microbial cell surface analysis, 1st edn. Wiley-VCH, New YorkGoogle Scholar
  13. Hernández M, Quijano G, Thalasso F, Daugulis AJ, Villaverde S, Muñoz R (2010) A comparative study of solid and liquid non-aqueous phases for the biodegradation of hexane in two-phase partitioning bioreactors. Biotechnol Bioeng 106:731–740. doi: 10.1002/bit.22748 CrossRefGoogle Scholar
  14. Jimenez IY, Bartha R (1996) Solvent augmented mineralization of pyrene by Micobacterium sp. Appl Environ Microbiol 62:2311–2316Google Scholar
  15. Lacal J (2008) Caracterización bioquímica y molecular del sistema de dos componentes TODS/TODT de Pseudomonas putida DOT-T1E. Dissertation, Consejo Superior de Investigaciones científicas (Estación experimental del Zaidín) and University of GranadaGoogle Scholar
  16. MacLeod CT, Daugulis AJ (2005) Interfacial effects in a two-phase partitioning bioreactor: degradation of polycyclic aromatic hydrocarbons (PAHs) by hydrophobic mycobacterium. Process Biochem 40:1799–1805. doi: 10.1016/j.procbio.2004.06.042 CrossRefGoogle Scholar
  17. Muñoz R, Arriaga S, Hernandez S, Guieysse B, Revah S (2006) Enhanced hexane biodegradation in a two phase partitioning bioreactor: overcoming pollutant transport limitations. Process Biochem 41:1614–1619. doi: 10.1016/j.procbio.2006.03.007 CrossRefGoogle Scholar
  18. Muñoz R, Villaverde S, Guieysse B, Revah S (2007) Two partitioning bioreactors for treatment of volatile organic compounds. Biotechnol Adv 25:410–422. doi: 10.1016/j.biotechadv.2007.03.005 CrossRefGoogle Scholar
  19. Muñoz R, Chambaud M, Bordel S, Villaverde S (2008) A systematic selection of the non-aqueous phase in a bacterial two liquid phase bioreactor treating α-pinene. Appl Microbiol Biotechnol 79:33–41. doi: 10.1007/s00253-008-1400-y CrossRefGoogle Scholar
  20. Neumann G, Cornelissen S, Breukelen FV, Hunger S, Lippold H, Loffhagen N, Wick LY, Heipieper HJ (2006) Energetics and surface properties of Pseudomonas putida DOT-T1E in a two-phase fermentation system with 1-decanol as second phase. Appl Environ Microbiol 71:6606–6612. doi: 10.1128/AEM.71.11.6606-6612.2005 CrossRefGoogle Scholar
  21. Nielsen DR, Daugulis AJ, McLellan PJ (2007) Dynamic simulation of benzene vapour treatment by a two-phase partitioning bioscrubber. Part II: model calibration, validation, and predictions. Biochem Eng J 36:250–261. doi: 10.1016/j.bej.2007.02.027 CrossRefGoogle Scholar
  22. Obuekwe CO, Al-Jadi ZK, Al-Saleh ES (2008) Comparative hydrocarbon utilization by hydrophobic and hydrophilic variants of Pseudomonas aeruginosa. J Appl Microbiol 105:1876–1887. doi: 10.1111/j.1365-2672.2008.03887.x CrossRefGoogle Scholar
  23. Obuekwe CO, Al-Jadi ZK, Al-Saleh ES (2009) Hydrocarbon degradation in relation to cell-surface hydrophobicity among bacterial hydrocarbon degraders from petroleum-contaminated Kuwait desert environment. Int Biodeterior Biodegrad 63:273–279. doi: 10.1016/j.ibiod.2008.10.004 CrossRefGoogle Scholar
  24. Owsianiak M, Szule A, Chrzanowski L, Cyplik P, Bogacki M, Olejnik-Schmidt AK, Heipieper HJ (2009) Biodegradation and surfactant-mediated biodegradation of diesel fuel by 218 microbial consortia are not correlates to cell surface hydrophobicity. Appl Microbiol Biotechnol 84:545–553. doi: 10.1007/s00253-009-2040-6 CrossRefGoogle Scholar
  25. Parker ND, Munn CB (1984) Increased cell surface hydrophobicity associated with possession of an additional surface protein by Aeromonas salmonicida. FEMS Microbiol Lett 21:233–237CrossRefGoogle Scholar
  26. Pijanowska A, Kaczorek E, Chrzanowski Ł, Olszanowski A (2007) Cell hydrophobicity of Pseudomonas spp. and Bacillus spp. bacteria and hydrocarbon biodegradation in the presence of Quillaya saponin. World J Microbiol Biotechnol 23:677–682. doi: 10.1007/s11274-006-9282-6 CrossRefGoogle Scholar
  27. Quijano G, Revah S, Gutiérrez-Rojas M, Flores-Cotera LB, Thalasso F (2009) Oxygen transfer in three-phase airlift and stirred tank reactors using silicone oil as transfer vector. Process Biochem 44:619–624. doi: 10.1016/j.procbio.2009.01.015 CrossRefGoogle Scholar
  28. Rocha-Ríos J, Bordel S, Hernández S, Revah S (2009) Methane degradation in two phase partition bioreactors. Chem Eng J 152:289–292. doi: 10.1016/j.cej.2009.04.028 CrossRefGoogle Scholar
  29. Rosenberg M, Gutnick D, Rosenberg E (1980) Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 9:29–33CrossRefGoogle Scholar
  30. Van Loosdrecht MCM, Lyklema J, Norde W, Schraa G, Zehnder AJ (1987) The role of bacterial cell wall hydrophobiictu in adhesion. Appl Environ Microbiol 53:1893–1897Google Scholar
  31. Yeom SH, Daugulis AJ, Nielsen DR (2010) A strategic approach for the design and operation of two-phase partitioning bioscrubbers for the treatment of volatile organic compounds. Biotechnol Prog. doi: 10.1002/btpr.481 Google Scholar
  32. Yu-Ying L (2010) The influences of Tween60 and rhamnolipid on the bioremediation of n-hexadecane. 4th International Conference on Bioinformatics and Biomedical Engineering. ISSN 21517615Google Scholar
  33. 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
  34. Zikmanis P, Shakirova L, Auzina L, Andersone (2007) Hydrophobicity of bacteria Zymomonas mobilis under varied environmental conditions. Process Biochem 42:745–750. doi: 10.1016/j.procbio.2007.01.002 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Department of Chemical Engineering and Environmental TechnologyValladolid UniversityValladolidSpain

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