Skip to main content
SpringerLink
Log in

Adaptation mechanisms of bacteria during the degradation of polychlorinated biphenyls in the presence of natural and synthetic terpenes as potential degradation inducers

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

In this study, we examined the effect of polychlorinated biphenyls (PCBs) in the presence of natural and synthetic terpenes and biphenyl on biomass production, lipid accumulation, and membrane adaptation mechanisms of two PCB-degrading bacterial strains Pseudomonas stutzeri and Burkholderia xenovorans LB400. According to the results obtained, it could be concluded that natural terpenes, mainly those contained in ivy leaves and pine needles, decreased adaptation responses induced by PCBs in these strains. The adaptation processes under investigation included growth inhibition, lipid accumulation, composition of fatty acids, cis/trans isomerization, and membrane saturation. Growth inhibition effect decreased upon addition of these natural compounds to the medium. The amount of unsaturated fatty acids that can lead to elevated membrane fluidity increased in both strains after the addition of the two natural terpene sources. The cells adaptation changes were more prominent in the presence of carvone, limonene, and biphenyl than in the presence of natural terpenes, as indicated by growth inhibition, lipid accumulation, and cis/trans isomerization. Addition of biphenyl and carvone simultaneously with PCBs increased the trans/cis ratio of fatty acids in membrane fractions probably as a result of fluidizing effects of PCBs. This stimulation is more pronounced in the presence of PCBs as a sole carbon source. This suggests that PCBs alone have a stronger effect on bacterial membrane adaptation mechanisms than when added together with biphenyl or natural or synthetic terpenes.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arensdorf JJ, Focht DD (1994) Formation of chlorocatechol meta cleavage products by a Pseudomonad during metabolism of monochlorobiphenyls. Appl Environ Microbiol 60:2884–2889

    CAS  Google Scholar 

  • Bedard DL, Unterman R, Bopp LH, Brennan MJ, Haberl ML, Johnson C (1986) Rapid assay for screening and characterizingmicroorganisms for the ability to degrade polychlorinated biphenyls. Appl Environ Microbiol 51:761–768

    CAS  Google Scholar 

  • Berg JM, Tymoczko JL, Stryer L (2006) Biochemistry, 6th edn. Freeman, New York, pp 565–600

    Google Scholar 

  • Bernal P, Segura A, Ramos JL (2007) Compensatory role of the cis–trans-isomerase and cardiolipin synthase in the membrane fluidity of Pseudomonas putida DOT-T1E. Environ Microbiol 9:1658–1664

    Article  CAS  Google Scholar 

  • Čertík M, Breierová E (2002) Adaptation responses of yeasts to environmental stress. Chem Listy 96:154–160

    Google Scholar 

  • Čertík M, Šajbidor J (1996) Variability of fatty acid composition in strains Mucor and Rhizopus and its dependence on the submersed and surface growth. Microbios 85:151–160

    Google Scholar 

  • Čertík M, Shimizu S (2000) Kinetic analysis of oil biosynthesis by arachidonic acid-producing fungus, Mortierella alpina 1S-4. Appl Microbiol Biot 54:224–230

    Article  Google Scholar 

  • Čertík M, Dercová K, Sejáková Z, Finďová M, Jakubík T (2003) Effect of polyaromatic hydrocarbons (PAHs) on the membrane lipids of bacterial cell. Biology 58:1111–1117

    Google Scholar 

  • Christopherson SW, Glass RL (1969) Preparation of milk fat methyl esters by alcoholysis in an essentially nonalcoholic solution. J Dairy Sci 52:1289–1290

    Article  CAS  Google Scholar 

  • Denich TJ, Beaudette LA, Lee H, Trevor SJT (2003) Effect of selected environmental and physicochemical factors on bacterial cytoplasmic membranes. J Microbiol Meth 52:149–182

    Article  CAS  Google Scholar 

  • Dercová K, Vrana B, Baláž Š, Šándorová A (1996) Biodegradation and evaporation of polychlorinated biphenyls (PCBs) in liquid medium. J Ind Microbiol 16:325–329

    Article  Google Scholar 

  • Dercová K, Tandlich R, Brežná B (2003) Application of terpenes as possible inducers of biodegradation of PCBs. Fresen Environ Bull 3:286–290

    Google Scholar 

  • Dercová K, Čertík M, Maľová A, Sejáková Z (2004) Effect of chlorophenols on the membrane lipids of bacterial cells. Int Biodeter Biodegr 54:251–254

    Article  Google Scholar 

  • Donnelly PK, Hedge RS, Fletcher JS (1994) Growth of PCB-degrading bacteria on compounds from photosynthetic plants. Chemosphere 28:981–988

    Article  Google Scholar 

  • Duldhardt I, Gaebel J, Chrzanowski L, Nijenhuis I, Härtig C, Schauer F, Heipieper HJ (2010) Adaptation of anaerobically grown Thauera aromatica, Geobacter sulfurreducens and Desulfococcus multivorans to organic solvents on the level of membrane fatty acid composition. Microbiol Biotech 3(2):201–209

    Article  CAS  Google Scholar 

  • Dzantor E, Woolston J, Momen B (2002) PCB dissipation and microbial community analysis in rhizosphere soil under substrate amendment conditions. Int J Phytoremediat 4:283–295

    Article  CAS  Google Scholar 

  • Furukawa K (1982) In: Chacrabarty AM (ed) Biodegradation and detoxification of environmental pollutants. CRC, Boca Raton, pp 156–178

    Google Scholar 

  • Furukawa K, Matsumura F, Tonomura K (1978) Alcaligenes and Acinetobacter strains capable of degrading polychlorinated biphenyls. Agric Biol Chem 42:543–548

    Article  CAS  Google Scholar 

  • Gilbert ES, Crowley DE (1997) Plant compounds that induce polychlorinated biphenyl biodegradation by Arthrobacter sp. Strain B1B. Appl Microbiol Biotech 63:1933–1938

    CAS  Google Scholar 

  • Grogan DW, Cronan JE (1997) Cyclopropane ring formation in membrane lipids of bacteria. Microbiol Mol Biol Rev 61:429–441

    CAS  Google Scholar 

  • Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227

    Article  CAS  Google Scholar 

  • Heipieper HJ, de Bont JAM (1994) Adaptation of Pseudomonas putida S 12 to ethanol and toluene at the level of fatty acid composition of membranes. Appl Environ Microbiol 60:4440–4444

    CAS  Google Scholar 

  • Heipieper HJ, Diefenbach R, Keweloh H (1992) Conversion of cis unsaturated fatty acids to trans, a possible mechanism for the protection of phenol-degrading Pseudomonas putida P8 from substrate toxicity. Appl Environ Microbiol 58:1847–1852

    CAS  Google Scholar 

  • Heipieper HJ, Weber FJ, Sikkema J, Keweloh H, de Bont JAM (1994) Mechanisms of resistance of whole cells to toxic organic solvents. TIBTECH 12:409–415

    Article  CAS  Google Scholar 

  • Heipieper HJ, Meinhardt F, Segura A (2003) The cis-trans isomerase of unsaturated fatty acids in Pseudomonas and Vibrio: biochemistry, molecular biology and physiological function of a unique stress adaptive mechanism. FEMS Microbiol Lett 229:1–7

    Article  CAS  Google Scholar 

  • Hernandez BS, Koh SC, Chial M, Focht DD (1997) Terpene-utilizing isolates and their relevance to enhanced biotransformation of polychlorinated biphenyls in soil. Biodegradation 8:153–158

    Article  CAS  Google Scholar 

  • Komancová M, Jurčová I, Kochánková L, Burkhard J (2003) Metabolic pathways of polychlorinated biphenyls degradation by Pseudomonas sp. 2. Chemosphere 50:537–543

    Article  Google Scholar 

  • Kumar P, Mohammadi M, Viger JF, Barriault D, Gomez-Gil L, Eltis LD, Bolin JT, Sylvestre M (2011) Structural insight into the expanded PCB-degrading abilities of a biphenyl dioxygenase obtained by directed evolution. J Mol Biol 405:531–547

    Article  CAS  Google Scholar 

  • Kwon SH, Hong MH, Choi JH, Whang KS, Lee HS, So JS, Koh SC (2009) Bioremediation of Aroclor 1242 by a consortium culture in marine sediment microcosm. Biotechnol Bioprocess Eng 13:730–737

    Article  Google Scholar 

  • Martínez P, Agulló L, Hernández M (2007) Chlorobenzoate inhibits growth and induces stress proteins in the PCB-degrading bacterium Burkholderia xenovorans LB400. Arch Microbiol 188:289–297

    Article  Google Scholar 

  • Maruna M, Šturdíková M, Liptaj T, Godány A, Múčková M, Čertík M, Prónayová N, Proksa B (2010) Isolation, structure elucidation and biological activity of angucycline antibiotics from an epiphytic yew streptomycete. J Basic Microbiol 50:1–8

    Article  Google Scholar 

  • Mrozik A, Piotrowska-Seget Z, Łabużek S (2004) Changes in whole cell-derived fatty acids induced by naphthalene in bacteria from genus Pseudomonas. Microbiol Res 159:87–95

    Article  CAS  Google Scholar 

  • Mrozik A, Łabużek S, Piotrowska-Seget Z (2005) Changes in fatty acid composition in Pseudomonas putida and Pseudomonas stutzeri during naphthalene degradation. Microbiol Res 160:149–157

    Article  CAS  Google Scholar 

  • Mrozik A, Cycoń M, Piotrowska-Seget Z (2010) Changes of FAME profiles as a marker of phenol degradation in different soils inoculated with Pseudomonas sp. CF600. Int Biodeter Biodegr 64:86–96

    Article  CAS  Google Scholar 

  • Parnell JJ, Denef VJ, Park J, Tsoi T, Tiedje JM (2010) Environmentally relevant parameters affecting PCB degradation: carbon source- and growth phase-mitigated effects of the expression of the biphenyl pathway and associated genes in Burkholderia xenovorans LB400. Biodegradation 21:147–156

    Article  CAS  Google Scholar 

  • Pepi M, Heipieper HJ, Fischer J, Ruta M, Volterrani M, Focardi SE (2008) Membrane fatty acids adaptive profile in the simultaneous presence of arsenic and toluene in Bacillus sp. ORAs2 and Pseudomonas sp. ORAs5 strains. Extremophiles 12:343–349

    Article  CAS  Google Scholar 

  • Ramos JL, Duque E, Rodriquez-Herva JJ, Godoy P, Haidour A, Reyes F, Fernandez-Barrero A (1997) Mechanisms for solvent tolerance in bacteria. J Biol Chem 272:3887–3890

    Article  CAS  Google Scholar 

  • Safe S (1978) Toxicology, structure-function relationship and human and environmental health impacts of polychlorinated biphenyls. Environ Health Persp 100:259–268

    Article  Google Scholar 

  • Šajbidor J (1997) Effect of some environmental factors on the content and composition of microbial membrane lipids. Crit Rev Biotechnol 17(2):87–103

    Article  Google Scholar 

  • Segura A, Duque E, Msqueda G, Ramos JL, Junker F (1999) Multiple responses of Gram-negative bacteria to organic solvents. Environ Microbiol 1:191–198

    Article  CAS  Google Scholar 

  • Shabala L, Ross T (2008) Cyclopropane fatty acids improve Escherichia coli survival in acidified minimal media by reducing membrane permeability to H+ and enhanced ability to extrude H+. Res Microbiol 159:458–461

    Article  CAS  Google Scholar 

  • Sikkema J, de Bont JAM, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222

    CAS  Google Scholar 

  • Sylvestre M (1995) Biphenyl/Chlorobiphenyls catabolic pathway of Comamonas testosterone B-356: Prospect for use in bioremediation. Int Biodeter Biodegr 53:189–211

    Article  Google Scholar 

  • Tandlich R, Brežná B, Dercová K (2001) The effect of terpenes on the biodegradation of polychlorinated biphenyls by Pseudomonas stutzeri. Chemosphere 44:1547–1555

    Article  CAS  Google Scholar 

  • Tandlich R, Vrana B, Payne S, Dercová K, Balaz S (2011) Biodegradation mechanism of biphenyl by a strain of Pseudomonas stutzeri. J Environ Sci Health A 46(4):1–8

    Article  Google Scholar 

  • Tříska J, Kuncová G, Macková M, Nováková H, Paasivirta J, Lahtiperä M, Vrchotová N (2004) Isolation and identification of intermediates from biodegradation of low chlorinated biphenyls (DELOR-103). Chemosphere 54:725–733

    Article  Google Scholar 

  • Weber FJ, de Bont JAM (1996) Adaptation mechanisms of microorganisms to the toxic effects of organic solvents on membranes. Biochem Biophys Acta 1286:225–245

    CAS  Google Scholar 

  • Zorádová S, Dudášová H, Lukáčová L, Dercová K, Čertík M (2011) The effect of polychlorinated biphenyls (PCBs) on the membrane lipids of Pseudomonas stutzeri. Int Biodeter Biodegr 65:1019–1023

    Article  Google Scholar 

Download references

Acknowledgment

The financial support from Slovak Grant Agency (grant No 1/0399/10) and (grant No 1/0734/12) are gratefully acknowledged.

Author information

Authors and Affiliations

  1. Institute of Biotechnology and Food Science, Department of Biochemical Technology, Slovak University of Technology, Faculty of Chemical and Food Technology, Radlinského 9, 812 37, Bratislava, Slovakia

    Slavomíra Zorádová-Murínová, Hana Dudášová, Lucia Lukáčová, Milan Čertík & Katarína Dercová

  2. Water Research Institute, Nábrežie arm. gen. L. Svobodu 5, 812 49, Bratislava, Slovakia

    Katarína Šilharová & Branislav Vrana

Authors
  1. Slavomíra Zorádová-Murínová
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hana Dudášová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lucia Lukáčová
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Milan Čertík
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Katarína Šilharová
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Branislav Vrana
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Katarína Dercová
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Slavomíra Zorádová-Murínová.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zorádová-Murínová, S., Dudášová, H., Lukáčová, L. et al. Adaptation mechanisms of bacteria during the degradation of polychlorinated biphenyls in the presence of natural and synthetic terpenes as potential degradation inducers. Appl Microbiol Biotechnol 94, 1375–1385 (2012). https://doi.org/10.1007/s00253-011-3763-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-011-3763-8

Keywords

Search

Navigation