Controlled ionic condensation at the surface of a native extremophilemembrane

Abstract

entor nz gonter D F nd o¤ %t hovskyD uF nd y nD tF pF @PHIHA 9gontrolled ioni ondens tion t the surf e of n tive extremophile mem r neF9D x nos leFD P F ppF PPPEPPWF Further information on publisher's website:httpXGGdxFdoiForgGIHFIHQWGfWx HHPRVu Publisher's copyright statement:Additional information: Use policyThe full-text may be used and/or reproduced, and given to third parties in any format or medium, without prior permission or charge, for personal research or study, educational, or not-for-pro t purposes provided that:• a full bibliographic reference is made to the original source • a link is made to the metadata record in DRO • the full-text is not changed in any way The full-text must not be sold in any format or medium without the formal permission of the copyright holders.Please consult the full DRO policy for further details. At the nanoscale level biological membranes present a complex interface with the solvent. The functional dynamics and relative flexibility of membrane components together with the presence of specific ionic effects can combine to create exciting new phenomena that challenge traditional 10 theories such as the Derjaguin, Landau, Verwey and Overbeek (DLVO) theory or models interpreting the role of ions in terms of their ability to structure water (structure making/breaking).Here we investigate ionic effects at the surface of a highly charged extremophile membrane composed of a proton pump (bacteriorhodopsin) and archaeal lipids naturally assembled into a 2D crystal. Using amplitude-modulation atomic force microscopy (AM-AFM) in solution, we obtained 15 sub-molecular resolution images of ion-induced surface restructuring of the membrane. We demonstrate the presence of a stiff cationic layer condensed at its extracellular surface. This layer cannot be explained by traditional continuum theories. Dynamic force spectroscopy experiments suggest that it is produced by electrostatic correlation mediated by a Manning-type condensation of ions. In contrast, the cytoplasmic surface is dominated by short range repulsive hydration forces. 20These findings are relevant to archaeal bioenergetics and halophilic adaptation. Importantly, they present experimental evidence of a natural system that locally controls its interactions with the surrounding medium and challenges our current understanding of biological interfaces.

Water-induced correlation between single ions imaged at the solid–liquid interface

“…Biological interfaces are however more complex, due to their strong and local dependence on the surrounding pH, and the conformational flexibility of the molecules. Correlated ionic networks are however likely to play key roles in charge transfer 12,38 and membrane shaping 58 , and both experiments and simulations are already underway to examine these possibilities.…”

“…The latter is chemically different than mica and, although only weakly charged, provides an appropriate hydration landscape that allows for the formation of ionic structures stable enough to be observed by AFM. The generality of the effect suggests that it could play an important role in wide range of systems, for example, in controlling and enhancing charge transport at interfaces 12,38 , in influencing crystal growth 17 or the stability of colloidal solutions and emulsions 18 . In addition, this effect could also be exploited in the design and self-assembly of nanomaterials 39 and used to template nanostructures 16 .…”

“…This assumption becomes problematic at the nanoscale where most solids exhibit some structure with localized charges and a welldefined hydration landscape that can determine the position and organization of single ions at the interface. Such a complexity is key to many processes such as the folding and function of biomolecules 11 , the accumulation and transfer of charges at the surface of extremophiles 12,13 or at the electrodes of solar cells 14 , electro-friction 15 , the nucleation of nanoparticles on surfaces 16 , or the preferential adsorption of a particular type of ion onto minerals 17 . Even at the macroscopic level, intense research is currently dedicated to the synthesis of colloid particles exhibiting non-homogeneous charge distributions at their surface for better controlling the stability or ordering of colloidal solutions 18 .…”

Sub-nanometer Resolution Imaging with Amplitude-modulation Atomic Force Microscopy in Liquid

“…In FM-AFM 28,41,56 , it is the oscillation frequency of the cantilever/tip that is kept constant while the tip scans the sample. Both techniques provide comparable topographic resolution in liquid 36,57 . Quantification of the tip-sample interaction tends to be more straightforward and accurate in FM-AFM, but AM-AFM is easier to implement, more robust, and allows working with softer cantilevers, something useful for studying easily deformable or delicate samples.…”

“…Over the last decade, the field of dynamic AFM in liquid has seen important developments, from the advent of video-rate AFM [21][22][23] , to multifrequency measurements 24,25 and sub-nanometer imaging of hydration structures at interfaces [26][27][28][29][30][31] . AFM operation while immersed in liquid is now routinely used in biology and biophysics [32][33][34][35][36] , polymer research 37 , electrochemistry [38][39][40] and solid-liquid interfaces characterisation [41][42][43][44] . The presence of liquid around the vibrating cantilever considerably alters its dynamics 45 as well as the interaction between the tip and the sample 29,42 .…”