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Cytoplasmic membrane fluidity and fatty acid composition of Acidithiobacillus ferrooxidans in response to pH stress

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Abstract

Strain variation in the acidophile Acidithiobacillus ferrooxidans was examined as a product of membrane adaptation in response to pH stress. We tested the effects of sub and supra-optimal pH in two type strains and four strains isolated from acid mine drainage water around Sudbury, Ontario, Canada. Growth rate, membrane fluidity and phase, determined from the fluorescence polarization of 1,6-diphenyl-1,3,5-hexatriene, and fatty acid profiles were compared. The effect of pH 1.5 was the most pronounced compared to the other pH values of 1.8, 3.1, and 3.5. Three different types of response to lower pH were observed, the first of which appeared to maintain cellular homeostasis more effectively. This adaptive mode included a decrease in membrane fluidity and concomitant depression of the phase transition in two distinct membrane lipid components. This was explained through the increase in saturated fatty acids (predominantly 16:0 and cyclopropane 19:0 w8c) with a concomitant decrease in 18:1 w7c fatty acid. The other strains also showed common adaptive mechanisms of specific fatty acid remodeling increasing the abundance of short-chain fatty acids. However, we suspect membrane permeability was compromised due to potential phase separation, which may interfere with energy transduction and viability at pH 1.5. We demonstrate that membrane physiology permits differentiating pH tolerance in strains of this extreme acidophile.

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References

  • Amaro AM, Chamorro D, Seeger M, Arredondo R, Peirano I, Jerez CA (1991) Effect of external pH perturbations on in vivo protein synthesis by the acidophilic bacterium Thiobacillus ferrooxidans. J Bacteriol 173(2):910–915

    CAS  PubMed  Google Scholar 

  • Baker-Austin C, Dopson M (2007) Life in acid: pH homeostasis in acidophiles. Trends Microbiol 15(4):165–171

    Article  CAS  PubMed  Google Scholar 

  • Beney L, Gervais P (2001) Influence of the fluidity of the membrane on the response of microorganisms to environmental stress. Appl Microbiol Biotechnol 57:34–42

    Article  CAS  PubMed  Google Scholar 

  • Booth IR (1985) Regulation of cytoplasmic pH in bacteria. Microbiol Rev 49(4):359–378

    CAS  PubMed  Google Scholar 

  • Borenstain V, Barenholz Y (1993) Characterization of liposomes and other lipid assemblies by multiprobe fluorescence polarization. Chem Phys Lipids 64:117–127

    Article  CAS  PubMed  Google Scholar 

  • Brown JL, Ross T, McMeekin TA, Nichols PD (1997) Acid habituation of Escherichia coli and the potential role of cyclopropane fatty acids in low pH tolerance. Int J Food Microbiol 37:163–173

    Article  CAS  PubMed  Google Scholar 

  • Chao J, Wang W, Xiao S, Liu X (2008) Response of Acidithiobacillus ferrooxidans ATCC 23270 gene expression to acid stress. World J Microbiol Biotechnol 24:2103–2109

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cobley JG, Cox JC (1983) Energy conservation in acidophilic bacteria. Microbiol Rev 4(4):579–595

    Google Scholar 

  • Cox JC, Nicholls DG, Ingledew WJ (1979) Transmembrane electrical potential and transmembrane pH gradient in the acidophile Thiobacillus ferrooxidans. Biochem J 178:195–200

    CAS  PubMed  Google Scholar 

  • Cronan JE (2003) Bacterial membrane lipids: where do we stand? Annu Rev Microbiol 57:203–224

    Article  CAS  PubMed  Google Scholar 

  • Driessen AJM, van de Vossenburg JLCM, Konings WN (1996) Membrane composition and ion-permeability in extremophiles. FEMS Microbiol Rev 18:139–148

    Article  CAS  Google Scholar 

  • Ferguson SJ, Ingledew WJ (2008) Energetic problems faced by micro-organisms growing or surviving on parsimonious energy sources and at acidic pH: I. Acidithiobacillus ferrooxidans as a paradigm. Biochim Biophys Acta 1777(12):1471–1479

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Ingledew WJ (1982) Thiobacillus ferrooxidans: the bioenergetics of an acidophilic chemolithotroph. Biochim Biophys Acta 683:89–117

    CAS  PubMed  Google Scholar 

  • Jerez CA, Chamorro D, Peirano I, Toledo H, Arredondo R (1988) Studies of the stress response in chemolithotrophic acidophilic bacteria. Biochem Int 17(6):989–999

    CAS  Google Scholar 

  • Kar NS, Dasgupta AK (1996) The possible role of surface charge in membrane organization in an acidophile. Indian J Biochem Biophys 33(5):398–402

    CAS  PubMed  Google Scholar 

  • Kar NS, Datta TK, Dasgupta AK (1996) Inter-conversion of chemiosmotic parameters and its inhibition in Acidithiobacillus ferrooxidans. Curr Sci 71(12):996–1001

    CAS  Google Scholar 

  • Karamanev DG, Nikolov LN, Mamtarkova V (2002) Rapid and simultaneous quantitative determination of ferric and ferrous ions in drainage waters and similar solutions. Miner Eng 15:341–346

    Article  CAS  Google Scholar 

  • Kim IS, Beaudette LA, Cassidy MB, Lee H, Trevors JT (2002) Alterations in fatty acid composition and fluidity of cell membranes affect the accumulation of PCB congener 2,2′,5,5′-tetrachlorphenyl by Ralstonia eutropha H850. J Chem Tech Biotechnol 77:793–799

    Article  CAS  Google Scholar 

  • Kondrat’eva TF, Karavaiko GI (1997) Genomic variability in Thiobacillus ferrooxidans and its role in biohydrometallurgical processes. Microbiology 66(6):612–620

    Google Scholar 

  • Konings WN, Albers S-V, Koning S, Driessen JM (2002) The cell membrane plays a crucial role in the survival of bacteria and archaea in extreme environments. Antoine van Leeuwenhoek 81:61–72

    Article  CAS  Google Scholar 

  • Leduc LG, Ferroni GD (1994) The chemolithotrophic bacterium Thiobacillus ferrooxidans. FEMS Microbiol Rev 14:103–120

    Article  CAS  Google Scholar 

  • Leduc LG, Trevors JT, Ferroni GD (1993) Thermal characterization of different isolates of Thiobacillus ferrooxidans. FEMS Microbiol Lett 108:189–194

    Article  CAS  Google Scholar 

  • Lee AG (2005) How lipids and proteins interact in a membrane: a molecular approach. Mol BioSyst 1(3):203–212

    Article  CAS  PubMed  Google Scholar 

  • Matin A (1990) Bioenergetics parameters and transport in obligate acidophiles. Biochim Biophys Acta 1018:267–270

    Article  CAS  Google Scholar 

  • McElhaney RN (1974) The effect of alterations in the physical state of the membrane lipids on the ability of Acholeplasma laidlawii B to grow at various temperatures. J Mol Biol 84:145–157

    Article  CAS  PubMed  Google Scholar 

  • Meruane G, Vargas T (2003) Bacterial oxidation of ferrous iron by Acidithiobacillus ferrooxidans in the pH range 2.5–7.0. Hydrometallurgy 71:149–158

    Article  CAS  Google Scholar 

  • Morein S, Anderson A-S, Rilfors L, Lindblom G (1996) Wild-type Escherichia coli cells regulate the membrane lipid composition in a “Window” between gel and non-lamellar structures. J Biol Chem 271(12):6801–6809

    Article  CAS  PubMed  Google Scholar 

  • Mykytczuk NCS, Trevors JT, Leduc LG, Ferroni GD (2007) Fluorescence polarization in studies of bacterial cytoplasmic membrane fluidity under environmental stress. Prog Biophys Mol Biol 95:60–82

    Article  CAS  PubMed  Google Scholar 

  • Mykytczuk NCS, Trevors JT, Ferroni GD, Leduc LG (2010a) Cytoplasmic membrane response to copper and nickel in Acidithiobacillus ferrooxidans. Microbiol Res (in press)

  • Mykytczuk NCS, Trevors JT, Twine SM, Ferroni GD, Leduc LG (2010b) Membrane fluidity and fatty acid comparisons in psychrotrophic and mesophilic strains of Acidithiobacillus ferrooxidans under cold growth temperatures. Arch Microbiol (accepted)

  • Rawlings DE (2002) Heavy metal mining using microbes. Annu Rev Microbiol 56:65–91

    Article  CAS  PubMed  Google Scholar 

  • Russell NJ, Evans RI, ter Steeg PF, Hellemons J, Verheul A, Abee T (1995) Membranes as a target for stress adaptation. Int J Food Microbiol 28(2):255–261

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Shinitzky M, Barenholz Y (1978) Fluidity parameters determined by fluorescence polarization. Biochim Biophys Acta 515:367–394

    CAS  PubMed  Google Scholar 

  • Souzu H (1986) Fluorescence polarization studies of Escherichia coli membrane stability and its relation to the resistance of the cell to freeze thawing: II. Stabilization of the membranes by polyamines. Biochim Biophys Acta 861:361–367

    Article  CAS  PubMed  Google Scholar 

  • Streit F, Delettre J, Corrieu G, Beal C (2008) Acid adaptation of Lactobacillus delbrueckii subsp. bulgaricus induces physiological responses at membrane and cytosolic levels that improves cryotolerance. J Appl Microbiol 105:1071–1080

    Article  CAS  PubMed  Google Scholar 

  • Sugio T, Iwahori K, Takai M, Takeuchi F, Kamimura K (2003) Molecular diversity of cytochrome oxidase among Acidithiobacillus ferrooxidans strains resistant to molybdenum, mercury, sulfite and 2,4-dinitrophenol. Hydrometallurgy 71:159–164

    Article  CAS  Google Scholar 

  • Suzuki I, Lee D, Mackay B, Hrahuc L, Key Oh J (1999) Effect of various ions, pH, and osmotic pressure on oxidation of elemental sulphur by Thiobacillus ferrooxidans. Appl Environ Microbiol 65(11):5163–5168

    CAS  PubMed  Google Scholar 

  • Trevors JT (2003) Fluorescent probes for bacterial cytoplasmic membrane research. J Biochem Biophys Meth 57:87–103

    Article  CAS  PubMed  Google Scholar 

  • Tuovinen OH, Kelly DP (1973) Studies on the growth of Thiobacillus ferrooxidans I. Use of membrane filters and ferrous iron agar to determine viable numbers, and comparison with 14+CO2-fixation and iron oxidation as measures of growth. Arch Microbiol 88:285–298

    CAS  Google Scholar 

  • Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428(6978):37–43

    Article  CAS  PubMed  Google Scholar 

  • Valdés J, Pedroso I, Quatrini R, Dodson RJ, Tettelin H, Blake II R, Eisen JA, Holmes DS (2008) Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genomics 9(597). http://www.biomedcentral.com/1471-2164/9/597

  • van de Vossenberg JLCM, Driessen AJM, Sillig W, Konings WN (1998) Bioenergetics and cytoplasmic membrane stability of the extremely acidophilic, thermophilic archaeon Pichrophilus oshimae. Extremophiles 2:67–74

    Article  PubMed  Google Scholar 

  • van de Vossenberg JLCM, Driessen AJM, Konings WN (2000) Adaptations of the cell membrane for life in extreme environments. In: Storey KB, Storey JM (eds) Cell and molecular responses to stress. Elsevier Science Ltd., Amsterdam, pp 71–88

    Google Scholar 

  • Vincent M, England LS, Trevors JT (2004) Cytoplasmic membrane polarization in Gram-positive and Gram-negative bacteria grown in the absence and presence of tetracycline. Biochim Biophys 1672:131–134

    CAS  Google Scholar 

  • Zychlinsky E, Matin A (1983) Cytoplasmic pH homeostasis in an acidophilic bacterium, Thiobacillus acidophilus. J Bacteriol 156(3):1352–1355

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank the Natural Sciences and Engineering Research Council of Canada (NSERC) for supporting this research through a Discovery grant held by JTT, a Discovery grant held by LGL and GDF, as well as a Canadian Graduate Scholarship awarded to NCSM.

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Authors and Affiliations

  1. Department of Biology, Laurentian University, Sudbury, ON, P3E 2C6, Canada

    N. C. S. Mykytczuk & L. G. Leduc

  2. School of Environmental Sciences, University of Guelph, Guelph, ON, N1G 2W1, Canada

    J. T. Trevors

  3. Division of Medical Sciences, Northern Ontario School of Medicine, Laurentian Campus, Sudbury, ON, P3E 2C6, Canada

    G. D. Ferroni

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  1. N. C. S. Mykytczuk
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  2. J. T. Trevors
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  3. G. D. Ferroni
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  4. L. G. Leduc
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Correspondence to N. C. S. Mykytczuk.

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Communicated by A. Driessen.

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Mykytczuk, N.C.S., Trevors, J.T., Ferroni, G.D. et al. Cytoplasmic membrane fluidity and fatty acid composition of Acidithiobacillus ferrooxidans in response to pH stress. Extremophiles 14, 427–441 (2010). https://doi.org/10.1007/s00792-010-0319-2

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  • DOI: https://doi.org/10.1007/s00792-010-0319-2

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