Skip to main content

Advertisement

Log in

Biosynthesis of ω-alicyclic fatty acids induced by cyclic precursors and change of membrane fluidity in thermophilic bacteria Geobacillus stearothermophilus and Meiothermus ruber

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

Two thermophilic strains belonging to Geobacillus stearothermophilus and Meiothermus ruber, which naturally do not synthesize ω-alicyclic fatty acids (ω-FAs) were cultivated with cyclopropyl, cyclobutyl, cyclopentyl and cyclohexyl carboxylic acids. Gas chromatography–mass spectrometry analysis of fatty acid methyl and picolinyl esters showed that both strains are able to synthesize ω-FAs when cultivated with the appropriate precursor. The incorporation of cyclic acids influenced the whole FA composition as well as membrane fluidity. Membrane fluidity of intact cells was studied by measuring the fluorescence polarisation of the probe l,6-diphenyl-1,3,5-hexatriene incorporated into membrane lipid bilayers. Cytoplasmic membrane became more fluid with increasing content of ω-FAs. This is caused by considerable changes in lipid packing within the membrane induced by the presence of ω-FAs not found in the natural environment of Geobacillus and Meiothermus strains.

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

Similar content being viewed by others

References

  • Albers SV, Driessen AJM (2008) Membranes and transport proteins of thermophilic microorganisms. In: Robb FT (ed) Thermophiles. CRC Press LLC, Boca Raton, USA, pp 39–54

  • Bligh ED, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Biophysiol 37:911–917

    Article  CAS  Google Scholar 

  • Blume A, Greher R, Poralla K (1978) The influence of branched-chain and ω-alicyclic fatty acids on the transition temperature of Bacillus subtilis lipids. BBA Biomembr 512:489–494

    Article  CAS  Google Scholar 

  • Catalog of Cultures (1999) Bacteria, Fungi, 6th edn. Czech Collection of Microorganisms, Masaryk University Brno, Faculty of Science

  • Chang S-S, Kang D-H (2004) Alicyclobacillus spp. in the fruit juice industry: history, characteristics, and current isolation/detection procedures. Crit Rev Microbiol 30:55–74

    Article  PubMed  Google Scholar 

  • Chu-Ky S, Tourdot-Marechal R, Marechal PA, Guzzo J (2005) Combined, cold, acid, ethanol shocks in Oenococcus oeni: effects on membrane fluidity and cell viability. BBA Biomembr 1717:118–124

    Article  CAS  Google Scholar 

  • Chung AP, Rainey F, Nobre MF, Burghardt J, da Costa MS (1997) Meiothermus cerbereus sp. nov., a new slightly thermophilic species with high levels of 3-hydroxy fatty acids. Int J Syst Bact 47:1225–1230

    Article  CAS  Google Scholar 

  • De Rosa M, Gambacorta A (1975) Identification of natural and semisynthetic ω-cycloalkyl fatty acids. Phytochemistry 14:209–210

    Article  Google Scholar 

  • De Rosa M, Gambacorta A, Bu’Lock JD (1974) Specificity effects in the biosynthesis of fatty acids in Bacillus acidocaldarius. Phytochemistry 13:905–910

    Article  Google Scholar 

  • Denich TJ, Beaudette LA, Lee H, Trevors JT (2003) Effect of selected environmental and physico-chemical factors on bacterial cytoplasmic membranes. J Microbiol Methods 52:149–182

    Article  PubMed  CAS  Google Scholar 

  • Dobson G (1998) Cyclic fatty acids: qualitative and quantitative analysis. In: Hamilton RJ (ed) Lipid analysis in oils and fats. Blackie, London, pp 136–180

    Google Scholar 

  • Dreher R, Poralla K, Konig WA (1976) Synthesis of ω-alicyclic fatty acids from cyclic precursors in Bacillus subtilis. J Bacteriol 127:1136–1140

    PubMed  CAS  Google Scholar 

  • Ferreira AM, Wait R, Nobre MF, da Costa MS (1999) Characterization of glycolipids from Meiotherrnus spp. Microbiology 145:1191–1199

    Article  PubMed  CAS  Google Scholar 

  • Goto K, Tanaka T, Yakamoto R, Suzuki T, Tokuda H (2007) Characteristics of Alicyclobacillus. In: Yokota A, Fujii T, Goto K (eds) Alicyclobacillus: thermophilic acidophilic bacilli. Springer, Japan, pp 9–48

    Google Scholar 

  • Hamilton JTG, Christie WW (2000) Mechanisms for ion formation during the electron impact-mass spectrometry of picolinyl ester and 4,4-dimethyloxazoline derivatives of fatty acids. Chem Phys Lipids 105:93–104

    Article  PubMed  CAS  Google Scholar 

  • Handa S, Floss HG (1997) Biosynthesis of ω-cyclohexyl fatty acids in Alicyclobacillus acidocaldarius: the stereochemistry of the initial 1,4-conjugate elimination. Chem Commun 153–154

  • Harvey DJ (1984) Picolinyl derivatives for the characterization of cyclopropane fatty acids by mass spectrometry. Biomed Environ Mass Spectrom 11:187–192

    Article  CAS  Google Scholar 

  • Hu YD, Floss HG (2006) Starter unit specificity of the asukamycin “upper” chain polyketide synthase and the branched-chain fatty acid synthase of Streptomyces nodosus subsp. asukaensis. Heterocycles 69:133–149

    Article  CAS  Google Scholar 

  • Kaneda T (1977) Gas chromatographic retention characteristics of ω-alicyclic fatty acids. J Chromatogr 136:323–327

    Article  CAS  Google Scholar 

  • Kaneda T (1991) Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol Rev 55:288–302

    PubMed  CAS  Google Scholar 

  • Kannenberg E, Blume A, Poralla K (1984) Properties of ω-cyclohexane fatty acids in membranes. FEBS 172:331–334

    Article  CAS  Google Scholar 

  • Laroche C, Beney L, Marechal PA, Gervais P (2001) The effect of osmotic pressure on the membrane fluidity of Saccharomyces cerevisiae at different physiological temperatures. Appl Microbiol Biotechnol 56:249–254

    Article  PubMed  CAS  Google Scholar 

  • Moore BS, Poralla K, Floss HG (1993) Biosynthesis of the cyclohexanecarboxylic acid starter unit of ω-cyclohexyl fatty acids in Alicyclobacillus acidocaldarius. J Am Chem Soc 115:5267–5274

    Article  CAS  Google Scholar 

  • Nordström KM, Laakso SV (1992) Effect of growth temperature on fatty acid composition of ten Thermus strains. Appl Environ Microb 58:1656–1660

    Google Scholar 

  • Oshima M, Ariga T (1975) ω-Cyclohexyl fatty acids in acidophilic thermophilic bacteria: studies on their presence, structure, and biosynthesis using precursors labeled with stable isotopes and radioisotopes. J Biol Chem 250:6963–6968

    PubMed  CAS  Google Scholar 

  • Ray PH, White DC, Brock TD (1971) Effect of temperature on the fatty acid composition of Thermus aquaticus. J Bacteriol 106:25–30

    PubMed  CAS  Google Scholar 

  • Reizer J, Grossowicz N, Barenholz Y (1985) The effect of growth temperature on the thermotropic behavior of the membranes of a thermophilic Bacillus: composition–structure–function relationships. BBA-Biomembranes 815:268–280

    Article  PubMed  CAS  Google Scholar 

  • Rezanka T (1990) Identification of very long polyenoic acids as picolinyl esters by Ag+ ion-exchange high-performance liquid-chromatography, reversed-phase high-performance liquid-chromatography and gas-chromatography mass-spectrometry. J Chromatogr 513:344–348

    Article  CAS  Google Scholar 

  • Schogt JCM, Begemann PH (1965) Isolation of 11-cyclohexylundecanoic acid from butter. J Lip Res 6:466–470

    CAS  Google Scholar 

  • Shinitzky M (1984) Membrane fluidity and cellular functions. In: Shinitzky M (ed) Physiology of membrane fluidity. CRC Press, Boca Raton, pp 1–52

    Google Scholar 

  • Siristova L, Melzoch K, Rezanka T (2009) Fatty acids, unusual glycophospholipids and DNA analyses of thermophilic bacteria isolated from hot springs. Extremophiles 13:101–109

    Article  PubMed  CAS  Google Scholar 

  • Suutari M, Laakso S (1994) Microbial fatty acids and thermal adaptation. Crit Rev Microbiol 20:285–328

    Article  PubMed  CAS  Google Scholar 

  • Tymczyszyn EE, Gomez-Zavaglia A, Disalvo EA (2005) Influence of the growth at high osmolality on the lipid composition, water permeability and osmotic response of Lactobacillus bulgaricus. Arch Biochem Biophys 443:66–73

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The research was supported by GACR P503/10/P182 and by Institutional Research Concept AV 0Z 502 0910.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lucie Siristova.

Additional information

Communicated by T. Matsunaga.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 184 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Siristova, L., Luhovy, R., Sigler, K. et al. Biosynthesis of ω-alicyclic fatty acids induced by cyclic precursors and change of membrane fluidity in thermophilic bacteria Geobacillus stearothermophilus and Meiothermus ruber . Extremophiles 15, 423–429 (2011). https://doi.org/10.1007/s00792-011-0373-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-011-0373-4

Keywords

Navigation