CoChat
Sign Up
Cited by 19Lipid Membrane Structure and BehaviorBacterial Genetics and BiotechnologyLipid metabolism and biosynthesis

The DOI matches its Crossref record.

Long-Term Adaptation of Bacillus subtilis 168 to Extreme pH Affects Chemical and Physical Properties of the Cellular Membrane

Petrackova, Denisa, Vecer, Jaroslav, Svobodova, Jaroslava, Herman, Petr·2010·Journal of Membrane Biology
DOI 10.1007/s00232-010-9226-9
Open this paper in CoChat — free account

Abstract

We characterized physical and chemical properties of cell-membrane fragments from Bacillus subtilis 168 (trpC2) grown at pH 5.0, 7.0 and 8.5. Effects of long-term bacterial adaptation reflected in growth rates and in changes of the membrane lipid composition were correlated with lipid order and dynamics using time-resolved fluorescence anisotropy of 1,6-diphenyl-1,3,5-hexatriene. We demonstrate that the pH adaptation results in a modification of a fatty acid content of cellular membranes that significantly influences both the lipid-chain order and dynamics. For cultivation at acidic conditions, the lipid order increases and membrane dynamics decreases compared to pH 7.0. This results in rigid and ordered membranes. Cultivation at pH 8.5 causes slight membrane disordering. Instant pH changes induce qualitatively similar but smaller effects. Proton flux measurements performed on intact cells adapted to both pH 5.0 and 8.5 revealed lower cell-membrane permeability compared to bacteria cultivated at pH optimum. Our results indicate that both acidic and alkalic pH stress represent a permanent challenge for B. subtilis to keep a functional membrane state. The documented adaptation-induced adjustments of membrane properties could be an important part of mechanisms maintaining an optimal intracellular pH at a wide range of extracellular proton concentrations.

Overview

Integrity signals

Registry

Crossref · 10.1007/s00232-010-9226-9

Cites

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Still being checked.

Research works printed but not linked: 47

  1. Amler E, Jasinska R, Drahota Z, Zborowski J (1990) Membrane lateral pressure as a modulator of glycerol-3-phosphate dehydrogenase activity. FEBS Lett 271:165–168 · DOI
  2. Beechem JM, Ameloot M, Brand L (1985) Global and target analysis of complex decay phenomena. Anal Instrument 14:379–402 · DOI
  3. Bisschop A, Konings WN (1976) Reconstitution of reduced nicotinamide adenine dinucleotide oxidase activity with menadione in membrane vesicles from the menaquinone-deficient Bacillus subtilis aro D. Relation between electron transfer and active transport. Eur J Biochem 67:357–365 · DOI
  4. 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. Biochim Biophys Acta 1717:118–124 · DOI
  5. Clejan S, Krulwich TA, Mondrus KR, Seto-Young D (1986) Membrane lipid composition of obligately and facultatively alkalophilic strains of Bacillus spp. J Bacteriol 168:334–340 · DOI
  6. Cross AJ, Fleming GR (1984) Analysis of time-resolved fluorescence anisotropy decays. Biophys J 46:45–56 · DOI
  7. 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 · DOI
  8. Dupree JL, Pomicter AD (2009) Myelin, DIGs, and membrane rafts in the central nervous system. Prostaglandins Other Lipid Mediat. doi: 10.1016/j.prostaglandins.2009.04.005 · DOI
  9. Fozo EM, Quivey RG Jr (2004) Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl Environ Microbiol 70:929–936 · DOI
  10. Fozo EM, Kajfasz JK, Quivey RG Jr (2004) Low pH-induced membrane fatty acid alterations in oral bacteria. FEMS Microbiol Lett 238:291–295 · DOI
  11. Fulford AJ, Peel WE (1980) Lateral pressures in biomembranes estimated from the dynamics of fluorescent probes. Biochim Biophys Acta 598:237–246 · DOI
  12. Fullekrug J, Simons K (2004) Lipid rafts and apical membrane traffic. Ann N Y Acad Sci 1014:164–169 · DOI
  13. Glass RL (1971) Alcoholysis, saponification and the preparation of fatty acid methyl esters. Lipids 6:919–926 · DOI
  14. Goni FM, Alonso A, Bagatolli LA, Brown RE, Marsh D, Prieto M, Thewalt JL (2008) Phase diagrams of lipid mixtures relevant to the study of membrane rafts. Biochim Biophys Acta 1781:665–684 · DOI
  15. Gurr M, Harwood JL, Frayn KN (2002) Lipid biochemistry: an introduction. Wiley-Blackwell, New York · DOI
  16. Hazel JR (1995) Thermal adaptation in biological membranes—is homeoviscous adaptation the explanation. Annu Rev Physiol 57:19–42 · DOI
  17. Herman P, Konopasek I, Plasek J, Svobodova J (1994) Time-resolved polarized fluorescence studies of the temperature adaptation in Bacillus subtilis using DPH and TMA-DPH fluorescent probes. Biochim Biophys Acta 1190:1–8 · DOI
  18. Herman P, Konopasek I, Vecer J, Svobodova J (1998) Time-resolved fluorescence and thermal adaptation of Bacillus subtilis: the role of membrane proteins. In: Slavik J (ed) Fluorescence microscopy and fluorescent probes. Springer, New York, pp 25–29
  19. Jahnig F (1979) Structural order of lipids and proteins in membranes: evaluation of fluorescence anisotropy data. Proc Natl Acad Sci USA 76:6361–6365 · DOI
  20. Jordan KN, Oxford L, O’Byrne CP (1999) Survival of low-pH stress by Escherichia coli O157:H7: correlation between alterations in the cell envelope and increased acid tolerance. Appl Environ Microbiol 65:3048–3055 · DOI
  21. Kaneda T (1977) Fatty acids of the genus Bacillus: an example of branched-chain preference. Bacteriol Rev 41:391–418 · DOI
  22. Kaneda T (1991) Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol Rev 55:288–302 · DOI
  23. Kinosita KJ, Kawato S, Ikegami A (1977) A theory of fluorescence polarization decay in membranes. Biophys J 20:289–305 · DOI
  24. Knutson JR, Beechem JM, Brand L (1983) Simultaneous analysis of multiple fluorescence decay curves—a global approach. Chem Phys Lett 102:501–507 · DOI
  25. Lakowicz JR (1999) Principles of fluorescence spectroscopy, 2nd edn. Kluwer Academic/Plenum, New York · DOI
  26. Lipari G, Szabo A (1980) Effect of librational motion on fluorescence depolarization and nuclear magnetic-resonance relaxation in macromolecules and membranes. Biophys J 30:489–506 · DOI
  27. Mansilla MC, Cybulski LE, Albanesi D, de Mendoza D (2004) Control of membrane lipid fluidity by molecular thermosensors. J Bacteriol 186:6681–6688 · DOI
  28. McElhaney RN, Souza KA (1976) Relationship between environmental-temperature, cell-growth and fluidity and physical state of membrane lipids in Bacillus stearothermophilus. Biochim Biophys Acta 443:348–359 · DOI
  29. Mykytczuk NC, 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 · DOI
  30. Owicki JC, Springgate MW, McConnell HM (1978) Theoretical study of protein–lipid interactions in bilayer membranes. Proc Natl Acad Sci USA 75:1616–1619 · DOI
  31. Poolman B, Blount P, Folgering JH, Friesen RH, Moe PC, van der Heide T (2002) How do membrane proteins sense water stress? Mol Microbiol 44:889–902 · DOI
  32. Poolman B, Spitzer JJ, Wood JM (2004) Bacterial osmosensing: roles of membrane structure and electrostatics in lipid–protein and protein–protein interactions. Biochim Biophys Acta 1666:88–104 · DOI
  33. Radin NS (1981) Extraction of tissue lipids with a solvent of low toxicity. Methods Enzymol 72:5–7 · DOI
  34. Shinitzky M, Barenholz Y (1978) Fluidity parameters of lipid regions determined by fluorescence polarization. Biochim Biophys Acta 515:367–394 · DOI
  35. Suutari M, Laakso S (1992) Unsaturated and branched chain-fatty acids in temperature adaptation of Bacillus subtilis and Bacillus megaterium. Biochim Biophys Acta 1126:119–124 · DOI
  36. Svobodova J, Julak J, Pilar J, Svoboda P (1988) Membrane fluidity in Bacillus subtilis. Validity of homeoviscous adaptation. Folia Microbiol (Praha) 33:170–177 · DOI
  37. Tao T (1969) Time-dependent fluorescence depolarization and brownian rotational diffusion coefficients of macromolecules. Biopolymers 8:609–632 · DOI
  38. Trevors JT (2003) Fluorescent probes for bacterial cytoplasmic membrane research. J Biochem Biophys Methods 57:87–103 · DOI
  39. van de Vossenberg JLCM, Driessen AJM, da Costa MS, Konings WN (1999a) Homeostasis of the membrane proton permeability in Bacillus subtilis grown at different temperatures. Biochim Biophys Acta Biomembr 1419:97–104 · DOI
  40. van de Vossenberg JLCM, Driessen AJM, Grant WD, Konings WN (1999b) Lipid membranes from halophilic and alkali-halophilic Archaea have a low H+ and Na+ permeability at high salt concentration. Extremophiles 3:253–257 · DOI
  41. van der Meer W, Pottel H, Herreman W, Ameloot M, Hendrickx H, Schroder H (1984) Effect of orientational order on the decay of the fluorescence anisotropy in membrane suspensions. A new approximate solution of the rotational diffusion equation. Biophys J 46:515–523 · DOI
  42. van Schaik W, Gahan CG, Hill C (1999) Acid-adapted Listeria monocytogenes displays enhanced tolerance against the lantibiotics nisin and lacticin 3147. J Food Prot 62:536–539 · DOI
  43. Wan FY, Wang YN, Zhang GJ (2002) Influence of the physical states of membrane surface area and center area on lysosomal proton permeability. Arch Biochem Biophys 404:285–292 · DOI
  44. Yuk HG, Marshall DL (2004) Adaptation of Escherichia coli O157:H7 to pH alters membrane lipid composition, verotoxin secretion, and resistance to simulated gastric fluid acid. Appl Environ Microbiol 70:3500–3505 · DOI
  45. Yuk HG, Marshall DL (2005) Influence of acetic, citric, and lactic acids on Escherichia coli O157:H7 membrane lipid composition, Verotoxin secretion, and acid resistance in simulated gastric fluid. J Food Protect 68:673–679 · DOI
  46. Zannoni C (1981) A theory of fluorescence depolarization in membranes. Mol Physics 42:1303–1320 · DOI
  47. Zhang GJ, Liu HW, Yang L, Zhong YG, Zheng YZ (2000) Influence of membrane physical state on the lysosomal proton permeability. J Membr Biol 175:53–62 · DOI

Cited by

Sorted by citations

See all 19

Metadata

Authors
Petrackova, D., Vecer, J., Svobodova, J., & Herman, P.
Venue
Journal of Membrane Biology
Publisher
Springer Science and Business Media LLC
Published
2010-02
Volume
233
Issue
1-3
Pages
73-83
ISSN
  • 0022-2631 (ISSN-L)
  • 1432-1424
DOI
10.1007/s00232-010-9226-9
OpenAlex
W1968051911
Cited by
19
References
0
Citations by year
2026: 1 · 2025: 2 · 2024: 1 · 2021: 1 · 2020: 1 · 2018: 3 · 2017: 1 · 2016: 1 · 2015: 2 · 2014: 2 · 2013: 1 · 2012: 1
FWCI
0.49
Type
journal article
Language
en
Open access
closed
Licence
www.springer.com/tdm (tdm)
Locations
  • The Journal of Membrane Biology (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
Keywords
Bacillus subtilis 168, pH adaptation, bacterial membranes, membrane lipid composition, fatty acid content, lipid chain order, membrane dynamics, membrane permeability, proton flux, intracellular pH homeostasis
MeSH terms
Bacillus subtilis, Cell Membrane, Diphenylhexatriene, Fluorescence Polarization, Hydrogen-Ion Concentration

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Long-Term Adaptation of Bacillus subtilis 168 to Extreme pH Affects Chemical and Physical Properties of the Cellular Membrane. https://app.cochat.ai/papers/10.1007/s00232-010-9226-9
The paper
Petrackova, D., Vecer, J., Svobodova, J., & Herman, P. (2010). Long-Term Adaptation of Bacillus subtilis 168 to Extreme pH Affects Chemical and Physical Properties of the Cellular Membrane. Journal of Membrane Biology. https://doi.org/10.1007/s00232-010-9226-9