Temperature-dependent phase transitions in zeptoliter volumes of a complex biological membrane

Phase transitions in purple membrane have been a topic of debate for the past two decades. In this work we present studies of a reversible transition of purple membrane in the 50-60 °C range in zeptoliter volumes under different heating regimes (global heating and local heating). The temperature of the reversible phase transition is 52 ± 5 °C for both local and global heating, supporting the hypothesis that this transition is mainly due to a structural rearrangement of bR molecules and trimers. To achieve high resolution measurements of temperature-dependent phase transitions, a new scanning probe microscopy-based method was developed. We believe that our new technique can be extended to other biological systems and can contribute to the understanding of inhomogeneous phase transitions in complex systems.

[1]  Anthony Watts,et al.  Differential stiffness and lipid mobility in the leaflets of purple membranes. , 2006, Biophysical journal.

[2]  H. Luecke,et al.  X-ray crystallographic analysis of lipid-protein interactions in the bacteriorhodopsin purple membrane. , 2003, Annual review of biophysics and biomolecular structure.

[3]  Ryan J. Kershner,et al.  Placement and orientation of individual DNA shapes on lithographically patterned surfaces. , 2009, Nature nanotechnology.

[4]  Stephen Jesse,et al.  Morphology Mapping of Phase-Separated Polymer Films Using Nanothermal Analysis , 2010 .

[5]  Eric Lesniewska,et al.  Surface Topography of Membrane Domains , 2022 .

[6]  S. Kalinin,et al.  Dual-frequency resonance-tracking atomic force microscopy , 2007 .

[7]  T. L. Wright,et al.  Electrical, Thermal, and Mechanical Characterization of Silicon Microcantilever Heaters , 2006, Journal of Microelectromechanical Systems.

[8]  C. le Grimellec,et al.  Temperature‐dependent localization of GPI‐anchored intestinal alkaline phosphatase in model rafts , 2007, Journal of molecular recognition : JMR.

[9]  R. Brasseur,et al.  The SIV tilted peptide induces cylindrical reverse micelles in supported lipid bilayers. , 2006, Biochemistry.

[10]  V. Lattanzio,et al.  Lipid-protein stoichiometries in a crystalline biological membrane: NMR quantitative analysis of the lipid extract of the purple membrane. , 2002, Journal of lipid research.

[11]  J. Killian,et al.  Domain formation in phosphatidylcholine bilayers containing transmembrane peptides: specific effects of flanking residues. , 2002, Biochemistry.

[12]  J. Killian,et al.  Visualization of highly ordered striated domains induced by transmembrane peptides in supported phosphatidylcholine bilayers. , 2000, Biochemistry.

[13]  E. Finot,et al.  Investigation of temperature-induced phase transitions in DOPC and DPPC phospholipid bilayers using temperature-controlled scanning force microscopy. , 2004, Biophysical journal.

[14]  Watt W. Webb,et al.  Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension , 2003, Nature.

[15]  Stephen Jesse,et al.  Resonance enhancement in piezoresponse force microscopy: Mapping electromechanical activity, contact stiffness, and Q factor , 2006 .

[16]  W. King,et al.  Measuring material softening with nanoscale spatial resolution using heated silicon probes. , 2007, The Review of scientific instruments.

[17]  Stephen Jesse,et al.  Local thermomechanical characterization of phase transitions using band excitation atomic force acoustic microscopy with heated probe , 2008 .

[18]  G. Sprott,et al.  Salt Tolerance of Archaeal Extremely Halophilic Lipid Membranes* , 2006, Journal of Biological Chemistry.

[19]  Hao Yan,et al.  Controlled delivery of DNA origami on patterned surfaces. , 2009, Small.

[20]  Thermal transitions in the purple membrane from Halobacterium halobium , 1993, FEBS letters.

[21]  J. Lanyi,et al.  Bacteriorhodopsin as a model for proton pumps , 1995, Nature.

[22]  A. Jin,et al.  Lipid membrane phase behaviour elucidated in real time by controlled environment atomic force microscopy. , 2002, Journal of electron microscopy.

[23]  E. Winfree,et al.  Toward reliable algorithmic self-assembly of DNA tiles: a fixed-width cellular automaton pattern. , 2008, Nano letters.

[24]  Fausto Sanz,et al.  Effect of temperature on the nanomechanics of lipid bilayers studied by force spectroscopy. , 2005, Biophysical journal.

[25]  Gerald H. Pollack,et al.  Phase Transitions in Cell Biology , 2008 .

[26]  Fausto Sanz,et al.  Nanomechanics of lipid bilayers by force spectroscopy with AFM: a perspective. , 2010, Biochimica et biophysica acta.

[27]  A. Muga,et al.  A pathway for the thermal destabilization of bacteriorhodopsin , 1995, FEBS letters.

[28]  C. le Grimellec,et al.  Coexistence of a two-states organization for a cell-penetrating peptide in lipid bilayer. , 2005, Biophysical journal.

[29]  Sergei V. Kalinin,et al.  Local bias-induced phase transitions , 2008 .

[30]  R. Henderson.  The purple membrane from Halobacterium halobium. , 1977, Annual review of biophysics and bioengineering.

[31]  J. Cladera,et al.  The role of retinal in the thermal stability of the purple membrane. , 1992, European journal of biochemistry.

[32]  J. Sturtevant,et al.  Phase transitions of the purple membranes of Halobacterium halobium. , 1978, Biochemistry.

[33]  Richard G. W. Anderson,et al.  Lipid rafts: at a crossroad between cell biology and physics , 2007, Nature Cell Biology.

[34]  M. Salmeron,et al.  Wetting and capillary phenomena of water on mica , 1998 .

[35]  D. Oesterhelt,et al.  Rhodopsin-like protein from the purple membrane of Halobacterium halobium. , 1971, Nature: New biology.

[36]  R. Korenstein,et al.  Energetics and chronology of phototransients in the light response of the purple membrane of Halobacterium halobium. , 1976, Biochimica et biophysica acta.

[37]  Liangfang Zhang,et al.  Nanoparticle-induced surface reconstruction of phospholipid membranes , 2008, Proceedings of the National Academy of Sciences.

[38]  Yves F Dufrêne,et al.  Nanoscale analysis of supported lipid bilayers using atomic force microscopy. , 2010, Biochimica et biophysica acta.

[39]  Kai Simons,et al.  Lipid Rafts As a Membrane-Organizing Principle , 2010, Science.

[40]  Jie Chao,et al.  Dynamic Patterning Programmed by DNA Tiles Captured on a DNA Origami Substrate , 2009, Nature nanotechnology.

[41]  Hao Yan,et al.  Scaffolded DNA origami of a DNA tetrahedron molecular container. , 2009, Nano letters.