Adsorption of Amino Acids and Peptides on Metal and Oxide Surfaces

Review Article pubs.acs.org/JPCB

Adsorption of Amino Acids and Peptides on Metal and Oxide Surfaces in Water Environment: A Synthetic and Prospective Review D. Costa,† L. Savio,‡ and C-M. Pradier*,§ †

Institut de Recherches de Chimie de Paris UMR 8247 ENSCP Chimie Paristech, 11 Rue P. Et M. Curie, 75005 Paris, France Istituto dei Materiali per l’Elettronica e il Magnetismo, Consiglio Nazionale delle Ricerche, U.O.S. Genova, Via Dodecaneso 33, 16146 Genova, Italy § Laboratoire de Réactivité de Surface, Sorbonne Université, UPMC Univ Paris 06, UMR CNRS 7197, 4 Place Jussieu, 75231 Paris Cedex 05, France ‡

ABSTRACT: Amino acids and peptides are often used as “model” segments of proteins for studying their behavior in various types of environments, and/or elaborating functional surfaces. Indeed, though the protein behavior is much more complex than that of their isolated segments, knowledge of the binding mode as well as of the chemical structure of peptides on metal or oxide surfaces is a significant step toward the control of materials in a biological environment. Such knowledge has considerably increased in the past few years, thanks to the combination of advanced characterization techniques and of modeling methods. Investigations of biomolecule−surface interactions in water/solvent environments are quite numerous, but only in a few cases is it possible to reach an understanding of the molecule−(water)−surface interaction with a level of detail comparable to that of the UHV studies. This contribution aims at reviewing the recent data describing the amino acid and peptide interaction with metal or oxide surfaces in the presence of water.

1. INTRODUCTION Natural, biomedical, and human environments provide multiple examples of liquid−solid interfaces where biomolecules meet solid surfaces, react, and may transform themselves or govern the reactivity/durability of materials. Let us recall the case of biocontamination of medical instruments or human implants or even biofilm growth on industrial infrastructures. The study of the interaction of surfaces with amino acids (AA), first, and with peptides, afterward, is a way to get closer to relevant biological systems. Peptides adsorb on surfaces and may form tridimensional architectures, similarly to what proteins do. Their adsorption tendency and conformation are however highly dependent on their environment. To predict the behavior at the solid−liquid interface, one should consider pH, ionic force, and, of course, peptide concentration in solution. Peptides are more and more often used for their bioactivity (increase of cell adhesion1 or damage of adhering bacteria), and this raises the issue of peptide interaction with various materials. This is the object of the present review in which, however, we will focus only on those studies fully characterizing the interaction of rather small peptides with metal and oxide surfaces in the presence of water molecules from the gas-phase or in a real aqueous environment. This is an essential clue for the understanding of the biointerfaces under realistic conditions, in biological systems, in biocatalysis, or for medical applications, to name a few examples. The description of the molecule/solvent/ surface system is, of course, complex because both solvent and reactants/modifiers interact at the solid surface in many ways. As always in the investigation of fundamental phenomena, it is therefore necessary to start from the analysis of simplified models © 2016 American Chemical Society

and move to systems with an increasing degree of complexity. For this, but also for the sake and beauty of extending the limits of basic surface science to complex systems, this review aims at presenting some recent advances in the knowledge of the interaction of the most “simple” biomolecules, amino acids and short peptides, with metal or oxide surfaces under wet conditions. Of course, to gain information at the molecular level, surface science techniques like X-ray photoelectron spectroscopy (XPS) or scanning tunneling microscopy (STM) are often complemented with other methods more appropriate in liquid or ambient environment, e.g., photon-based spectroscopies operating in ambient conditions (IR and Raman spectroscopies, sum frequency generation (SFG)) and/or electrochemical methods to perform the analysis of the biointerface in solution. Atomic information (nature of the bond with the surface) is often brought by spectroscopic studies from the solid−liquid interface, for instance in situ attenuated total reflection (ATR)-FTIR, combined with theoretical calculations. The first part of this review will deal with amino acid adsorption on metal and oxide surfaces, either in the presence of coadsorbed water or in aqueous solution. In the second part, more complex systems will be described; the behavior of dipeptides, tripeptides, and some longer peptides in water solution and interacting with metal and oxide surfaces have indeed been the subject of basic investigations. The role of water molecules on the surface chemistry, the adsorbate chemical form, and its organization on the surface will then be discussed in the light of the presented data. Received: June 13, 2016 Published: July 1, 2016 7039

DOI: 10.1021/acs.jpcb.6b05954 J. Phys. Chem. B 2016, 120, 7039−7052

Review Article

The Journal of Physical Chemistry B

2. AMINO ACIDS ON METALS While quite a lot of advances have been achieved so far in the characterization at the atomic and molecular level of the dry amino acids−metal interface,2−9 much less work has been performed on the amino acids (AA) adsorption from the liquid phase. The simplest model of the AA−surface interaction in wet conditions consists in the coadsorption of the molecular species and of water from the gas-phase under UHV conditions. The next step is the investigation of the dried biointerface after deposition from solution, to finish with the analysis of the interface immersed in solution10,11 (not discussed in the following due to length constraints). 2.1. Amino Acid and Water Coadsorption under UHV Conditions. Coadsorption of water and biomolecules at metal surfaces under UHV conditions is now feasible by exposing the surface to water vapor near the equilibrium vapor pressure (in the Torr range) at room temperature (RT). Photoemission and X-ray absorption experiments,12 now accessible at near ambient pressure, revealed that adsorption of pure water is particularly complex, due to lateral interactions and changes of the water dissociation barrier.13 Shavorskiy et al. investigated the coadsorption of water and Gly or Ala on Cu(110)14 and of water and Gly on Pt(111).15 Figure 1 reports the XPS spectra recorded in the N 1s region for the surface fully or half covered by Gly (or Ala) and allows comparison of the spectra obtained under UHV conditions with those acquired after water exposure up to near-ambient conditions. The AAs are present in different forms at the surface depending on the presence of significant H2O coadsorption. When the surface is fully covered with the amino acid, the behavior is very similar to that observed in UHV. Conversely, at low alanine coverage, coadsorption of water and alanine occurs on the Cu(110) surface, which induces the formation of a surface CN species (characterized by a shifted peak in the N 1s XP signal and sharp resonances in the N and C NEXAFS spectra) stable at room temperature and desorbing only above ∼400 K. This was interpreted by a reaction involving oxygen- and/or hydroxylinduced dehydrogenation of methyl-/ethylamine intermediates. Interestingly, the same experiments for Gly/Pt(111) lead to significantly different results. Indeed, under UHV conditions, glycine adsorbs in its neutral form up to about 0.15 ML, while additional molecules adsorb as zwitterions.16 Coadsorption with water under UHV conditions and at T < 170 K leads to surface layers strongly dependent on the adsorption sequence: When Gly is adsorbed before water, the chemical state of glycine is the same as without water. When Gly is deposited on a layer of water, it adsorbs in its zwitterionic state. 2.2. Amino Acid Deposition from Solution: The Role of Solvent and pH. It is well-established that amino acids in solution undergo an increasing degree of deprotonation when passing from low to high pH values.17,18 As a natural consequence, the AA layer created by immersion of metallic samples into such a solution will be pH dependent. For some systems, the behavior of amino acids adsorbed from solution as a function of pH was compared to results for the gas-phase deposition.17−19 Figure 2 reports polarization modulation (PM)-RAIR spectra recorded on Cys/Cu(110)17 and on a Lys-covered polycrystalline Cu surface18 after adsorption of the AA in solution at the indicated pH. In both cases we underline the reduction of the ν(CO) stretch intensity at ∼1735 cm−1 and the corresponding increase of the νsym(COO−) at ∼1407 cm−1 for increasing pH. Such a behavior is indicative of

Figure 1. N 1s XP spectra of glycine and alanine overlayers on Cu(110) produced under different conditions: (i) Gly (full monolayer), (ii) Ala (50% of saturation coverage), and (iii) Ala (full monolayer), all deposited at 300 K in UHV; (iv) full monolayer of Gly deposited at 300 K in 0.2 Torr H2O atmosphere; (v) Ala layer (50% of saturation coverage) deposited at 266 K in 0.5 Torr H2O atmosphere; (vi) full monolayer of Ala deposited at 300 K in 0.1 Torr H2O atmosphere; (vii) Ala layer (50% of saturation coverage) deposited at 420 K in the presence of 0.5 Torr H2O pressure; (viii) full monolayer of Ala annealed to 500 K in UHV and 0.1 Torr H2O. The photon energy is 560 eV for spectra ii and v, 510 eV for all other spectra. Reprinted with permission from ref 14. Copyright 2011 American Chemical Society.

the conversion from carboxylic to carboxylate groups and confirms that the change in ionization state of the AA also affects the adsorbed species. As a general rule, adsorption keeps the chemical form of the molecules in solution. For (S)-cysteine, four different chemical forms have been identified: the zwitterionic form (predominant when the pH of the solution is close to the isoelectric point (IEP) of Cys, i.e., pH = 5.4), the cationic and the neutral ones at low pH, and the anionic form at high pH. Deprotonation of the SH group is also likely, since RAIR spectra never show any SH mode; this is a strong indication of the involvement of sulfur either in bonding with the metallic surface or in the dimerization of the cysteine molecules. A similar behavior was observed for (L)-Lys, for which dicationic, cationic, zwitterionic, and anionic forms were detected both in solution and at the wet interface with polycrystalline Cu. Varying the conditions of adsorption may influence both the orientation of the molecule on the surface and the chemical groups involved in the bonding. As an example, there is a significant conformational change of Cys depending on the preparation method: under vacuum conditions, the molecule binds to the copper surface via the sulfur atom and the two oxygens of the carboxylate group, while the ammonium group stays normal and away from the surface. Vice versa, after adsorption in solution, 7040


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Figure 2. (a) RAIR spectra of the Cu(110) surface after adsorption of (S)-cys from solutions at pH 1.0, 5.4, and 10.5. (b) PM-RAIR spectra of the Cu polycrystal surface after adsorption of L-lys at pH 1.2, 5.5, 9.5, and 12. Reprinted with permission from refs 17 and 18. Copyright 2004 and 2006, respectively, American Chemical Society.

only the sulfur atom is likely to interact directly with the surface. The intense IR mode around 1610 cm−1, corresponding to the overlapping of the contributions of the νasym(COO−) and of the δasym(NH3+), and the weak NH3+ symmetric deformation at 1500 cm−1 suggest that the two oxygens of the carboxylate group are no longer equidistant from the surface and that the orientation of the NH3+ group is not normal. The conformational change with respect to the dry conditions could be due to strong cysteine−water interactions in solution, or to the presence of Cl− (detected by XPS) on the surface, that occupies part of the surface sites. Lys, on the contrary, displays very similar RAIR spectra after deposition from solution at pH = 9.5 and after evaporation in UHV on an O-covered Cu(110) sample. A similar investigation of the influence of pH on the adsorption state of (S)-Glu on Ni(111)19 shows results consistent with those reported on Cu substrates. After adsorption in solution on Ni(111) at controlled pH and room temperature, glutamic acid adsorbs in the cationic/zwitterionic form at neutral pH, and is deprotonated at high pH. Interestingly, the next step, i.e., the investigation of the chemical activity of the (S)-Glu/Ni(111) surface toward the adsorption of methylacetoacetate, was also proved to be pH dependent. In particular, diketone formation is favored when the modifier is more protonated. E.g., for the (S)-Glu/Ni(111) surface at 300 K and pH 3.3, the diketonerelated peak in RAIR spectra is 10 times more intense than the enol-related peak. This ratio moves to 1:1 at pH 9. Ramakrishan et al.20 addressed the facet-selective binding of two peptides (Thr-Leu-Thr-Thr-Leu-Thr-Asn (T7) and Ser-Ser-Phe-Pro-Gln-Pro-Asn (S7)) at Pt(100) and Pt(111) by calculating the adsorption energy of the constituent AA toward the Pt crystalline facets in vacuum, in pure water, and in an ionic solution. The energies are higher when the AA are in water, indicating that the presence of water and ions is crucial in the AA (and peptide) adsorption process. Polar amino acids (Glu and Asn)

adsorb more strongly on both facets in vacuum, while adsorption of Phe is the strongest one in water. This discrepancy can be due to the hydrophobic side chain of Phe that induces a preferential adsorption, with water interaction being disfavored. Water preferentially binds at atop sites and parallel to the surface,21 thus forming a hydration layer which prevents direct contact between amino acids and the surface. Whatever the environment, Phe, Gln, Asn, and Pro are predicted to bind more strongly to the Pt(111) surface, while Leu and Thr prefer the Pt(100) facets. Phe, the most hydrophobic aromatic amino acid, has a very high affinity to both surfaces. The authors conclude that the facetselective adsorption of peptides cannot be solely explained by their composition; the sequence of amino acids, and the resulting peptide conformation (flexibility and mobility), must be considered, too. Finally, we mention a few studies performed on Au samples. Feyer et al. used XPS and NEXAFS to compare the adsorption of His and His-tripeptides on Au(111) and Au(110) surfaces, cleaned by sputtering and annealing cycles in UHV, and then immersed in neutral or acidic (pH 3) solution.22,23 The Au 4f core level shift indicates that chemisorption rather than physisorption occurs. In all cases, the imidazole ring is oriented, lying down parallel to the surface, and the imino nitrogen atom plays a crucial role in the interaction with gold surfaces (although only a fraction of the molecules strongly bind to the surface via the imino group). The main difference in the adsorption modes from neutral and acidic liquid phase deposition is observed for the carboxylate/carboxylic and peptidic groups. When deposited from neutral solution on Au(111), His and its peptides strongly interact with the gold surface via deprotonated carboxylate groups, and no carboxylic group is observed in absorbed molecules. The CO peptidic group is oriented roughly perpendicular to the surface.23 Vice versa, upon deposition from acidic solution, protonated and deprotonated carboxyl groups are distributed on the Au surface randomly.22 Possibly, the presence of COOH 7041


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surface bear negative charges. According to ref 30, aspartic acid adsorbs on titanium oxide via ligand exchange with a hydroxyl group at the surface Ti atom. At low surface coverage, aspartate may bind through both carboxylate groups as suggested by XPS measurements, i.e., “lying down” on the rutile surface. At high coverage, the reaction stoichiometry for aspartate likely involves an “outer-sphere or hydrogen-bonded aspartate surface species”.29 Adsorption of AAs (methionine, alanine, cysteine) on TiO2 surfaces was studied by XPS, and the role of pH was investigated.31 The AAs are not very tightly bound to the surface. Methionine, alanine, and β-alanine desorbed after rinsing. Homocysteine chemisorbed at a slightly acidic pH. The results confirmed the ligand exchange model of hydroxyl replacement. Ab initio works including the explicit solvent are scarce, due to the high computational cost. Langel et al.32 studied methionine, serine, and cysteine on rutile (100) and (110) surfaces at different OH coverage, with Car−Parrinello molecular dynamics (CPMD). In the chosen model, all the bridging O atoms of TiO2 were protonated, but no monodentate (i.e., terminal) OH groups were present. Neglecting the monodentate groups, hydroxylation in water corresponds to an acidic environment where only the bridging atoms are protonated and the basic hydroxyl groups are dissolved. The simulations showed that “the oxygens of the carboxyl group form bonds with surface titanium atoms of the dehydroxylated surfaces.”32 Ti−OH or Ti−SH bond formation in the case of serine or cysteine molecules, respectively, was also considered. It was found that “binding of the carboxyl groups to the surface through hydrogen bonds and Ti−O interaction is weak in all cases”.32 3.4. Amino Acid Adsorption on Other Oxides. Glycine adsorption on boehmite (γ-AlO(OH))33 and Al2O334 was studied by ATR-FTIR. It was concluded that glycine adsorbs in an outer sphere mode on the boehmite surface through NH2− OH hydrogen bonds and electrostatic interactions. This system has been recently studied by ab initio molecular dynamics35,25 which confirmed the formation of an Al−O−C−O bond, already predicted by DFT calculations without solvent. Inner sphere adsorption is favored over outer sphere adsorption.36 Glycine adsorbs on maghemite (γ-Fe2O3)37 up to a surface coverage of 4.5 molecules/nm2 (or 1.36 ML) in a bridging bidentate conformation, while alanine adsorbs on α- and γ-Al2O3 in an outer sphere mode, through electrostatic interactions, as revealed by diffuse reflectance infrared Fourier transform spectroscopy (DRIFTS).38 Adsorption of glutamic acid and aspartic acid on γ-Al2O3 was studied by in situ ATR-FTIR.39 Tetradentate tetranuclear and bidentate binuclear species were predominant with both carboxylate groups interacting with “either four or two Al surface atoms (covalent bonds or H-bonds)”.39 Sverjenski et al.40 studied glutamate adsorption on ferrihydrite Fe10O14(OH)2. The deprotonated divalent anion at pH 3−5 adsorbs “...in the form of chelating-monodentate or bridgingbidentate species attached to the surface through three or four of the carboxylate oxygens, respectively. The amine group may interact weakly with the surface. At similar pH and higher surface coverage, glutamate adsorbs mainly as a monovalent or divalent anion chelated to the surface by the γ-carboxylate group. In this configuration, the α-carboxylate and amine groups might be free to interact above the surface with the free ends of additional glutamates, suggesting a possible mechanism for chiral selforganization and peptide bond formation.”40

groups in molecules adsorbed from acidic solution causes a difference in hydrogen bond network formation, thus favoring the formation of a disordered phase. Interestingly, the process of protonation−deprotonation of the amino and carboxyl groups is fully reversible and depends not only on the pH of the AA solution (as in the previously discussed examples) but also on the pH of the rinsing solution. The last rinsing literally washes away any information from previous treatments.

3. ADSORPTION OF AMINO ACIDS ON OXIDE SURFACES FROM THE LIQUID PHASE 3.1. Oxide Surfaces in Liquid: A Short Introduction. In the presence of liquid water, oxides are hydroxylated/hydrated and bear charges; on the other hand, amino acids are solvated and charged, and water acts as a screen with respect to the surface. In addition, water has a local role in coadsorbing with the biomolecule in a cooperative/competitive scheme, and also impacting the electrostatic work during adsorption.24 This shows the complexity of such systems! We review experimental and theoretical works describing AA adsorption on oxide surfaces at the oxide−liquid interface at the molecular level. Theoretical studies dealing with the solid−liquid interface have been developing for some years. In particular, molecular dynamics calculations based on density functional theory (DFT-MD) now allow description of both the oxide surface and the liquid phase with the same level of theory, i.e., including bond breaking and making.25 Amino acid adsorption on TiO2 is presented first, followed by some examples of AA adsorption on other oxides. Adsorption on silica26 was treated recently and is thus not considered. 3.2. Glycine on TiO2. TiO2 has an overall pKa of 6.5. To our knowledge, only one experimental study of adsorption of glycine on rutile TiO2 nanoparticles in aqueous medium at pH 9 was performed.27 No Gly adsorption was evidenced. This experimental result contrasts with calculations of glycine interaction with rutile from water solution, which predict glycine adsorption.28 As evident from Figure 3, the monodentate conformation, with

Figure 3. Minimum free energy configurations and relative energies of glycine on rutile TiO2(110) in the presence of water, obtained with ReaxFF. Glycine adsorbed: (a) in a bridging bidentate mode and (b) in monodentate mode. Reprinted with permission from ref 28. Copyright 2012 American Chemical Society.

one carboxyl oxygen bound to a Ti atom (Figure 3b), is more stable than the bridging one (Figure 3a), which is favored in UHV conditions. 3.3. Larger Amino Acids Adsorbed on TiO2 from the Liquid Phase. Earlier experimental adsorption isotherms report adsorption of lysine and glutamic acid on spherical particles of amorphous TiO2.29 Adsorption is pH dependent and occurs at pH > 8, in which condition both the amino acids and the 7042


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The Journal of Physical Chemistry B Molecular dynamics study of adsorption of AA at low coverage on several ZnO surfaces was also performed.41 The authors conclude that the layered character of water near the surface affects the adsorption of AAs. Indeed AA adsorption is 45 times weaker in the presence of water than in vacuum. The largest binding energy is found for tyrosine (7 kJ mol−1). However, no clear trend is found in the ranking of adsorption of AAs.

4. PEPTIDES AT METAL AND OXIDE SURFACES 4.1. Adsorption of Short Peptides on Metal/Oxide Surfaces in Aqueous Solution. 4.1.1. Short Peptides on Noble Metals. Adsorption of glutathione (GSH, i.e., Gly-CysGlu tripeptide) on Au(111) has been widely described after adsorption from aqueous solutions, revealing that, conversely to the case of amino acids (see section 2.2)42 after soft rinsing in pure water, the peptides retain the ionic form they have in solution. Upon harsh rinsing and/or long flowing, the chemical state of the adsorbed peptide may change and convert to that expected from the pH of the rinsing solution. Bieri and Bürgi were precursors when they described the interaction of L-glutathione with Au thin films. They determined the adsorption kinetics of this tripeptide on gold surfaces in ethanol by using ATR-IR and quartz crystal microbalance (QCM), and they evidenced reversible changes in the peptide conformation when passing from acidic to basic solvents.43 In addition, two regimes appear, ascribed to different rates of deprotonation of the two carboxylic groups of the molecule (see Figure 4). They also showed that, if deprotonated, GSH binds to

Figure 5. Schematic representation of the protonation/deprotonation process of GSH on gold. The evolution of the IR signals suggests that the deprotonation of the carboxylic groups is accompanied by their binding to the gold surface in addition to the Au−S interaction. Reprinted with permission from ref 43. Copyright 2005 American Chemical Society.

for a molecule containing a thiol termination, with an additional link of the NH2 group. Increasing the potential causes the Au−NH2 bond to be released and favors the formation of a disulfide bridge bound to Au atoms. The same tendency was observed with cysteine, which forms dimers at high potential. In comparison with the adsorption of cysteine on the same surface, the authors interpreted the observed spectral changes as a progressive reduction of the Au−S bond and a lowering of the charge transfer toward the charged Au(110) surface. Thomas et al.45 characterized the binding mode of anserine (a dipeptide of the β-alanine and amino acid derivative methyl histidine) on silver nanoparticles by Raman spectroscopy. In contrast to IR spectroscopy, enhanced Raman enables detection of low frequency vibrations between the metal and atoms of the molecule. In the present case, a Ag−O vibration appears, with a maximum intensity for a complete monolayer; the interaction of anserine proceeds via the carboxylate groups, with the imidazole ring being in a tilted or quasi upright position with respect to the surface; other spectral changes were observed in the amide region, which support a reorientation of the whole molecule in the submonolayer range as schematized in Figure 6.

Figure 4. From ref 43: “Absorbance of signals at 1650 (upper curve) and 1725 cm−1 (lower curve) as a function of time for a modulation experiment. GSH was adsorbed on a gold-coated Ge crystal, in zwitterionic form from ethanol solution. An alternate flow of ethanol, followed by a flow of ethanol + HCl of equal time was admitted to the GSH sample during a modulation experiment. The time dependence of the two signals reveals two regimes with different deprotonation kinetics.” Reprinted with permission from ref 43. Copyright 2005 American Chemical Society. Figure 6. Scheme of adsorbed β anserine on Ag: (a) submonolayer regime and (b) monolayer coverage. Reprinted with permission from ref 45. Copyright 2013 Elsevier.

gold via the carboxylate group of the Glu fragment in addition to the interaction via the S atom (Figure 5). Investigating the interaction of peptides with metal surfaces in liquid phase also raises the question of self-assembly and orientation. To illustrate this matter, the cysteine-tryptophan dipeptide was adsorbed on Au(110) and monitored by reflectance anisotropic spectroscopy (RAS).44 Binding mode, orientation, and ordering of the dipeptide depend on the applied potential. At −0.6 eV the dipeptide binds to gold via its S atom, as expected

4.1.2. Short Peptides on Oxides. The glutathione disulfide (GSSG) adsorption/desorption behavior was investigated on α-Al2O3 nanoparticles experimentally and theoretically with classical molecular dynamics.46 Adsorption occurs via interaction of the carboxylate groups. In continuation with GSH, glutathion disulfide adsorption was investigated on colloidal alumina particles 7043


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The Journal of Physical Chemistry B modified by amino (NH2), carboxylate (COOH), phosphate (PO3H2), or sulfonate (SO3H) groups.47 GSSG easily adsorbs “...on native, NH2-functionalized, and SO3H-functionalized alumina but not on COOH- and PO3H2-functionalized particles. GSSG is likely to bind via the carboxylate groups of one of its two glutathionyl (GS) moieties onto native and NH2-modified alumina, whereas it binds to SO3H-modified alumina via the primary amino groups of the two GS moieties. Thus, GSSG adsorption and orientation can be tailored by varying the molecular composition of the particle surface.”47 Adsorption of the dipeptides H-Ala-Glu-NH2 and H-AlaLys-NH2 has been investigated on the TiO2(110) surface in the presence of water.48,49 Both experimental and theoretical findings agree that peptide carbonyl oxygens and nitrogens are likely to be the coordination atoms, and “...self-interaction effects may induce molecular reorientations and less strongly adsorbed species.”50 Diglycine adsorption on a hydroxylated (110) rutile surface was simulated under vacuum conditions and for a bridging bidentate configuration. As a second step, liquid water was introduced into the system, and MD simulations (ReaxFF) were run for 60 ps.28 It was found that “...the adsorbates were only slightly biased by water interactions during the trajectory covered in the simulation time. The direct coordination of their carboxyl groups with the surface Ti atoms was preserved.”28 The same team studied adsorption of KEK aggregated peptides (clusters of two tripeptides) on a negatively charged TiO2(110) surface with noncomplete OH coverage.50 The number of terminal hydroxyls “...corresponds to a pH value of about 7 and their location to minimal Coulombic repulsion. The net negative structural charge was balanced with positively Ca2+ counterions.”50 Both peptides are stabilized on TiO2 through the side-chain groups of both Lys and Glu. Interestingly, “...the carboxyl oxygen is coordinated to a titanium site at the beginning of the simulation, but also located in close proximity to a Ca2+ ion (adsorbed between two terminal oxygens). This oxygen detaches from its original binding site and moved toward the Ca2+ ion during the last 4 ns of the simulation. This behaviour, visible in Figure 7, suggests that the adsorption of COO− groups can occur via Ca2+ ions acting as a bridge between the peptide and the surface.”50 Classical MD simulations were employed to investigate the adsorption behavior of the arginine-glycine-aspartate (RGD) tripeptide onto the fully hydroxylated51,52 and the nonhydroxylated53 rutile (110) surfaces, in the presence of Na+ or Ca2+. An RGD sequence approached the negatively charged hydroxylated rutile (110) surface. It is concluded that “the competition between the positively charged Arg side chain and the negatively charged Asp side chains may drive the more weakly attached group away from the surface.”53 In a subsequent work,52 the same MD method allowed researchers to study the binding of the negatively charged residue (Asp) of RGD onto a negatively charged hydroxylated rutile (110) surface in aqueous solution, containing divalent (Mg2+, Ca2+, or Sr2+) or monovalent (Na+, K+, or Rb+) cations. The results indicate that “...ionic radii and charges significantly affect the hydration, adsorption geometry and distance of cations from the rutile surface, thereby regulating the Asp/rutile binding mode. The Asp side chain in NaCl, KCl, and RbCl solutions remains H-bonded to the surface hydroxyls and the monovalent cations act as a bridge between the COO− group and the rutile. In contrast, the divalent cations actively participate in linking the

Figure 7. From ref 50: “Four frames extracted from the MD simulation of the adsorption of KEK on TiO2. One of the Glu side chains (COO group) detaches from the titanium atom of the surface and binds directly to a Ca2+ ion (orange atom). Peptide atoms are shown in stick mode (hydrogen, white; nitrogen, blue; oxygen, red, carbon gray), whereas surface atoms (titanium brown, oxygen red) and calcium ions (orange) are displayed as balls. Water is omitted for clarity. Reprinted with permission from ref 50. Copyright 2009 American Chemical Society.

COO− group to the rutile surface”,52 even in the absence of any hydrogen bonds with the surface hydroxyls. In the following we will see a confirmation of the “glue” role of cations in the adsorption of long polypetides on alumina, either in pure water or in buffer (see section 4.2.2). Already in 1999, Roddick-Lanzilotta investigated the adsorption of lysine-derivated peptides (from dilysine to pentalysine) on titanium and chromium oxide surfaces from aqueous solutions, using in situ infrared spectroscopy.54 Changes in the IR spectra of the peptides, when passing from the solution to the adsorbed phase (see Figure 8), demonstrate the involvement of the carboxylate groups in the binding to the TiO2 surface. All lysine peptides do adsorb on TiO2 at pH 7.4, as expected from the negative and positive charges of TiO2 and peptides, respectively.55,56 By looking carefully at the IR spectra, the increase of the wavenumber splitting of the antisymmetric and symmetric COO− stretches (Δν), at ∼1400 and 1550 cm−1, respectively, compared to the peptide in solution, suggests a direct interaction of COO− groups with the Ti4+ cations. Moreover, the binding constant increases with the size of the lysine peptide, indicating that the longer the peptide, the higher the number of carboxylate groups interacting with the surface. Adsorption of the same peptides was then investigated on a chromium oxide film, but no adsorption has ever been observed. This may be related to the positive charge of this oxide, which hinders electrostatic interactions, the exactly opposite situation to that observed on TiO2. This stresses the importance of the surface charge at physiological pH! To finish with short peptide adsorption, MD simulations were performed to investigate the adsorption mode of the KEK peptide which has “...only hydrophilic amino acids with alternating negative and positive charges on titanium dioxide, 7044


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Interestingly, the authors tentatively attributed this shape-control ability of specific peptide sequences to the position of amino acids in the sequence; as examples, the aromatic group at the end of the S7 sequence may preferentially bind to the (111) facets thanks to the good match with their hexagonal atomic surface arrangement, while the hydroxyl-rich peptide sequence is likely to favor platinum− oxygen bonds with adjacent platinum atoms of the (100) facets. The interaction of peptides with metal nanoparticles was also described in another work where the Cys-Leu-Pro-Phe-Phe-Asp (CLPFFD) peptide, conjugated to a gold nanoparticle, is used to specifically recognize β-amyloid protein for a therapeutic goal. The question to be addressed is the integrity of the peptide once attached to the gold nanoparticle and how it is interacting. The authors deduced from in situ surface-enhanced Raman spectroscopy (SERS) that the peptide interacts with gold with its phenylalanine ring, which is close to the surface and almost parallel to it (Figure 10). This result was supported by molecular mechanics and extended Hückel theory calculations.58

Figure 8. IR spectra of trilysine (a) adsorbed on a TiO2 film and (b) in solution. Reprinted with permission from ref 54. Copyright 1999 Elsevier.

muscovite mica, and graphite surfaces. In agreement with experimental data, the peptide and its aggregates weakly adsorb on graphite, and strongly adsorb on both titanium dioxide and muscovite, involving direct and indirect interactions (mediated by calcium and potassium ions) with the surface atoms through the amino acid side chains”50. 4.2. Adsorption of Longer Peptides. 4.2.1. Adsorption of Longer Peptides on Metal Surfaces. Studies of peptide−metal interfaces in aqueous environment are scarce. The two main works, which we are going to present, demonstrate the interest of understanding and controlling these complex interfaces at the molecular scale. First, though not being strictly an in situ characterization of peptide−metal interactions, the work by Chiu et al. reports that peptides present during the synthesis of Pt nanoparticles can specifically bind to certain facets and induce particular shapes of the obtained single crystals. Two peptides, Thr-Leu-Thr-ThrLeu-Thr-Asn (T7) and Ser-Ser-Phe-Pro-Gln-Pro-Asn (S7), were selected after a phage-display process, for their preferential affinity to (100) or (111) facets, respectively (Figure 9); then,

Figure 10. Schematic representation of the CLPFFD peptide adsorbed on gold. Reprinted with permission from ref 58. Copyright 2015 Elsevier.

4.2.2. Adsorption of Longer Peptides on TiO2 and Other Oxides. Sano and Shiba identified a hexapeptide motif, Arg-LysLeu-Pro-Asp-Ala (RKLPDA), as playing a role in phage adsorption on TiO2. Then, in order to identify the group (or groups) involved in the interaction with the surface, they synthesized a series of peptides only differing by substituting alanine to one of the amino acid fragments. As a result, they propose a model where the terminal arginine NH2 groups interact with Ti−O− (Lewis base site), and the COO− of aspartic acid interacts with Ti−OH2+ (Lewis acid site) (see Figure 11). They also showed that increasing the surface OH concentration favors peptide binding.1 Langel et al. studied dodecapeptide adsorption on perfect and rough TiO2 surfaces.59 The surface roughness has a determinant effect on the adsorption mode of the peptide (as illustrated in Figure 12). It was found that multipoint anchoring induced higher adsorption energies, and that rigid secondary structures prevent amino acids from reaching the surfaces. Moreover, water near the oxide surface loses mobility as compared to bulk water. The main effect of surface charge is not attraction of oppositely charged molecular groups, but reduction of water mobility. In addition, peptide or protein adsorption proceeds faster on mobile than on rigidly bonded water. On rough surfaces, water in

Figure 9. Illustration of a peptide-directed synthesis of nanocrystals, and corresponding TEM images, by stabilizing (100) or (111) facets, given peptides favor the formation of cubes or tetrahedrons, respectively. Reprinted by permission from Macmillan Publishers Ltd.: Nature Chemistry (ref 57). Copyright 2011.

platinum nanocrystals were synthesized, from chloroplatinic salts and with addition of either peptide, leading to remarkable preferential formation of Pt cubes or Pt tetrahedrons, and so forth, and the process in solution could be reversed.57 7045


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simulations were also performed to elucidate the secondary structure differences. The important and original conclusion is that the inclusion of a linker containing four proline residues, by favoring a helical secondary structure at the base of the peptide, reduces the mobility of the chains and allows them to pack tighter, increasing the packing density; such a rigid and dense surface is also the one which had the best antifouling properties. This original work demonstrates the importance of selecting an appropriate peptide linker that allows a well-defined secondary structure to be formed and leads to a closely packed, uniform monolayer.62 At this point, one must recall the precursor work by Boulmedais et al.,63 who characterized the secondary structure of peptide layers by building multilayered poly(L-glutamic acid)/ poly(L-lysine) films taking advantage of intermolecular electrostatic and hydrogen bonds. It is interesting that on a surface, like in solution, polypeptide complexes adopt a stable secondary structure such as α-helices and β-sheets. In a rather similar way, thin films of poly-L-lysine (PL) and poly-L-glutamic acid (PG) were adsorbed on planar and powder surfaces of aluminum oxide. Polarization modulation-reflection absorption infrared spectroscopy (PM-RAIRS), operating in a cell especially built to probe the solid surface in contact with the liquid, made clear a strong influence of pH and salts upon polypeptide adsorption.64 At pH values higher than 5, the presence of CaCl2 in solution induces a net increase of PG adsorption, whereas no influence of the pH was observed for PL. Specific interactions between the peptide COO-groups and the surface, or intermolecular interactions, were thought to explain these differences (see Figure 13). Ca2+ cations do have a promoting effect upon adsorption when the polymer bears carboxylate groups in its side chains. As an illustration, adsorption of PG is maximal at pH above the COOH pKa value. The synergetic role of Ca2+ and COO− groups is confirmed by experiments performed at low pH on PG, or on PL, which shows no enhancement of the adsorption in the presence of salts (see Figure 14).64 Spectroscopic investigation of the structure of two RGDlinked peptides, EAK 16-RGD and RGD-scrambled EAK, on Au and TiO265 confirmed the extreme sensitivity of the organization of adsorbed peptides to the amino acid sequence. Let us take the example of H-RGDAEAEAKAKAKAEAEAKAK-NH2 (Pept A) and H-RGD-AAKAEAEAAEKAKAEK-NH2 (Pept B). Both peptides were immobilized on TiO2 by incubation in aqueous solution.

Figure 11. Model of the RKLPDA peptide interaction with a titanium oxide surface. Reprinted with permission from ref 1. Copyright 2003 American Chemical Society.

the grooves also has little mobility, and peptide adsorption preferably occurs on top of the grooves rather than inside.59 This is an interesting example of the competition between the biomolecule and water in the adsorption. In a similar approach, interaction of cyclic and linear peptides was tested on two metal oxide surfaces, TiO2 and SiO2,60,61 leading to conclude that the electrostatic interactions are essential and sufficient to bind positively charged residues (K or R) to a negatively charged TiO2 surface. Moreover, though the linear peptide displays exactly the same behavior on both oxide surfaces, the cyclic peptide has a weaker binding affinity. The structural flexibility of a linear peptide permits a wide range of conformations and an optimization of its interactions. Once adsorbed, and precisely due their flexibility, peptides may organize on the surface and form dense, packed, layers. Let us take the example of two peptides containing the low fouling segment EKEKEKE, made of four negative glutamic acid residues (E) and three positive lysine residues (K). When aiming at elaborating a fouling-resistant surface, the challenge is to bind these peptidic fragments by combining them with a linker, expected to favor the formation of a densely packed layer. To do so, either a cysteine or a longer hydrophobic segment made of four proline and a terminal cysteine was simply added to the sequence; then, the nonfouling sequences EKEKEKE-PPPPCand EKEKEKE-C were attached to a gold surface, and the impacts of the length and of the nature of the linker to form a well-packed, antifouling peptide, SAM were investigated by combining circular dichroism (CD) and ATR-FTIR in solution. Molecular dynamics

Figure 12. Surface adsorption of the peptides. Two surface models are shown, flat (left) and rough (right). Atoms are colored as titanium (purple), oxygen (red), nitrogen (dark blue), carbon (cyan), and hydrogen (white). Reprinted with permission from ref 59. Copyright 2013 Elsevier. 7046


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Despite the presence of identical chemical groups in both peptides, reflectance IR spectra display better defined absorption bands, thus revealing a more ordered structure for Pept A than for Pept B. Moreover, NEXAFS measurements at the C and N K-edges, performed at normal and grazing incidence (see Figure 15), revealed that, on both Au or TiO2 substrates,

Figure 13. Schematic representation of the formation of Ca2+ bridges between two carboxylate groups of the PG chains. Another possibility would be that a coordinative bond, associating water molecules, ensures the binding to the surface or in between chains. Reprinted with permission from ref 64. Copyright 2007 American Chemical Society.

Figure 15. C and N K-edge spectra of the Au and TiO2 surfaces after deposition of Pept A and Pept B, recorded at grazing and normal incidences. One sees no influence of the incidence angle on the NEXAFS spectra of Pept B, whereas signals at grazing incidence are enhanced for Pept A. Reprinted with permission from ref 65. Copyright 2007 Elsevier.

Pept A forms an ordered assembly with the main chain axis almost normal to the surface, whereas Pept B shows no preferential orientation (see Figure 15). This important result suggests that the organization of a peptide layer on a surface is governed by intermolecular interactions rather than by the nature of the substrate. Adsorption of Trp Ala6-NH2, Trp Ser6-NH2, Trp Lys6-NH2, Trp His6-NH2, and Trp Asp6-NH2 was tested on copper, cobalt, titanium, and some other metal oxide nanoparticles; the tryptophan end fragment was a trick to evaluate the strength of adsorption by monitoring the level of fluorescence quenching when adding nanoparticles in the peptide solution.66 While, with all peptides, fluorescence quenching was observed when adding CuO nanoparticles, only His and Asp peptides seemed to adsorb on Co3O4 nanoparticles. Hexahistidine is by far the most strongly binding peptide likely due to the tendency of nitrogen in the imidazole ring to form coordinative bonds with transition metals; note also that the observed binding constants, higher on copper than on cobalt oxide, are in agreement with the affinity of proteins with Cu2+ and Co2+ metal centers.67 The binding of Trp Ala6-NH2, easily explainable a priori by electrostatic interactions between negatively charged alanine and the positively charged surface, is rather also due to the formation of coordinative bonds between carboxylate groups and metal

Figure 14. In situ PM-IRRAS spectra of an aluminum surface in a D2O solution of polyglutamic acid. The pH was adjusted before contacting with the surface; CaCl2 salts were added during the adsorption. Reprinted with permission from ref 64. Copyright 2007 American Chemical Society. 7047


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Figure 16. SFG spectra of the peptide/silica (left), and peptide/polystyrene (right) interfaces in buffer at various ionic strengths. On silica, only ice-like water modes were observed. On polystyrene, CH modes of the peptide and water structures can be seen. Reprinted with permission from ref 71. Copyright 2007 American Chemical Society.

(lysine = K) residues.70 These two peptides do adsorb on both polystyrene and silica surfaces, in a higher amount for the longer one. Moreover, no preferential orientation was observed on silica, but on polystyrene, the observation of νCH SFG signals suggests an alignment of the nonpolar side chain of the peptides as if the orientation of the adsorbate was driven by hydrophobic interactions with the surface. In a further study, the same authors made clear the influence of the ionic strength of the solvent upon peptide assembly on the same hydrophilic or hydrophobic surfaces.71 Again, SFG brought very innovative data in an investigation of a 14-amino acid leucine-lysine peptide on hydrophobic polystyrene and hydrophilic silica.72 On silica, no CH modes were observed, suggesting no alignment of the peptide chains (Figure 16, left panel); the peptide likely maintains its helical structure. On polystyrene, the orientation and intensity of the CH modes do not depend on the ionic strength, which suggests that the adsorption of the amphiphilic peptide on a hydrophobic surface is related to the rearrangement of the interfacial water molecules; peptide adsorption induces alignment of its CH2 chains and ordering of interfacial water molecules at low ionic strength (see Figure 16, right panel), likely originating from the presence of the charged lysine residues.

centers; this was deduced from a comparison with MgO nanoparticles on which no adsorption of Trp Ala6-NH2 was detected. The study of the interaction of several tetradecapeptides with Ag colloidal surface using SERS is very original.68 Peptides bind to silver mainly via their Trp and Met residues. Substitutions in the peptide chain were also shown to induce changes in the whole peptide orientation on the surface.

5. SOME HINTS INTO MORE COMPLEX SYSTEMS AND BIOLOGICAL APPLICATIONS Some recent papers report a strategy to investigate the interaction of peptides with hydrophilic or hydrophobic surfaces, which consists of grafting organic molecules with specific properties on solid surfaces. Though slightly beyond the scope of this report, we give some of these results which provide valuable insights into the mechanism of peptide adsorption and assembly on a surface. Let us take the example of the B18 peptide (18 amino acids, namely LGLLL-RHLRHHSNLLANI), very much studied because it plays a crucial role in membrane binding and also because its conformation is very sensitive to its environment. For the investigation of the effect of surface chemistry, some silicon wafers were prepared in a mixture of H2O, H2O2, and NH4OH, to obtain hydroxylated surfaces; some others were modified with polyelectrolyte multilayers [(poly-allylamine hydrochloride) (PAH)/poly(styrenesulfonate)], or with n-octadecyl-trichlorosilane (OTS) leading to surfaces that are negatively/positively charged, or strongly hydrophobic, respectively.69 Very different behaviors of the B18 peptide were observed, in solution at pH 7, on these surfaces leading to the following conclusions: (i) On a hydrophilic surface, peptide adsorption is governed by electrostatic interactions, and B18 only adsorbs on negatively charged films, with slow kinetics and forming aggregates. (ii) On a hydrophobic surface, B18 peptide adsorbs rapidly and forms a rather homogeneous film. The high affinity of the B18 peptide to hydrophobic surfaces has been attributed to the presence of leucine residues on the peptide backbone. This is an important consideration for understanding the mechanism of fusion of the lipid vesicle induced by the model amyloid B18 (LGLLLRHLRHHSNLLANI) peptide. Adsorption of amphiphilic peptides was evaluated in the liquid phase on polystyrene and silica surfaces by combining SFG and QCM measurements. Let us take the cases of LK7 (Ac-LKKLLKL-NH2) and LK14 (Ac-LKKLLKLLKKLLKL-NH2), containing hydrophobic (leucine = L) and positively charged

6. SUMMARY AND OUTLOOK This review, though far from presenting an exhaustive list of studies addressing systems which mimic “in situ” biointerfaces, shows examples of significant results in the field. It makes a point on the present knowledge and contributes to the understanding of some complex and strategic systems constituted by biomolecules interacting with metal or oxide surfaces, a major issue in nanobiotechnology. Progress in the development of surface analysis techniques, and most of the time their combination with theoretical tools, has permitted characterization of complex systems at a quasi molecular level. Besides that, and probably due to the broad field of applications in biorelated technology, there is a huge increase of studies aiming at understanding and controlling the interaction of amino acids, peptides, and, of course, proteins with solid surfaces, under nonmodel conditions. This review is limited to “simple” or, more exactly, small biomolecules in the presence of water. Several examples show that amino acid adsorption is significantly modified in the presence of water for at least two reasons: (i) Water modifies intermolecular interactions, and sometimes 7048


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experimental surface science approach and (ii) addressing real systems, by simplifying them reasonably (e.g., studying adsorption of one single bacteria to mimic a biofilm, or investigating the growth of a cell on a model surface, etc.), taking advantage of and applying the data on model systems. This is nothing less than bridging the gap between model and real biological interfaces. Perhaps the next step in that direction will be the use of in situ (in liquid) characterization techniques, with an atomic scale resolution, together with ab initio dynamics or accurate force fields methods. Once again, though peptides cannot pretend being a model for proteins, great progress would be to determine adequate sequences of amino acids which accomplish properties of proteins. Here comes the issue of peptide secondary structures, inevitably linked to long peptides, and their selfassembly, which thus also need to be characterized. Tuning the amino acid sequence of peptides may, one day, enable researchers to direct their secondary structure and thus to design 2D/3D hybrid nanostructures, another broad field to explore. One may then dream of having rather complex biomolecules on material surfaces, and tuning their binding mode, their structure, and their chemical state to attain a desired functionality (biocompatibility, molecular recognition, chirality, biofilm resistance, just as examples), simply by changing some parameters like solvent, pH, ionic strength, or temperature.

the chemical form and thus the protonation of some binding points of the molecule. (ii) Water induces oxidation/ hydroxylation of most metals (except Au), thus modifying their reactivity. Adsorption from aqueous solution changes the ionic form of the peptide drastically with respect to the one obtained upon deposition in UHV. The possibility to control the charge of the adsorbed amino acid/peptide by adsorbing it from solutions at selected pH values is important. In addition, linked to point ii, while site adsorption is almost certainly responsible for amino acid adsorption on nonhydroxylated oxides from the gas-phase, in the case of adsorption from aqueous solutions a nonspecific mechanism may also be considered, namely, electrostatic adsorption of a charged molecule on a charged surface. Theoretical studies now take into account small biomolecules and explicit solvent surface charges (and thus pH conditions), surface roughness, and ions when studying adsorption of amino acids or peptides. In particular, it has been well-established that the intricate solvent−surface interaction strongly influences the geometry and energy of adsorption of molecules. On one hand, ab initio molecular dynamics is feasible for longer time scales, remaining however in the range of the tens of picoseconds. These calculations are important because they provide a precise description of the organization of the solvent and of the surface groups. In particular, the agreement between pKa calculations of surface OH groups and experimental data demonstrates that the models are robust for the description of reactivity. Note that only theory allows description of the interaction with the solvent at the atomistic scale. In addition, calculations provide accurate results on small chemical functions and biomolecule adsorption, with no secondary and tertiary structures and thus no major entropy contribution in the free energy. Finally, they represent benchmarks for lighter methods. On the other hand, classical force fields are more and more accurate, and the description of the metal or oxide/water interface is approaching realistic conditions. The description of the full free energy landscape remains challenging, especially the entropic aspects of the biomolecule conformations (coil versus organized structures), but indubitably more and more indications are, and will be, brought by theory. At the present time, the driving chemical factors, including solution pH, structure of the surfaces, and electrostatic arguments, are viewed in a rather “bulk-like” and “static” way: the real pH at the metal (or metal oxide)−solution interface is not considered; the structure of water at the interfaces or the role of the charge dynamic is generally not taken into account; the charge image term is generally neglected; and few papers take the ionic force in the due account. We notice the exception of E. Vogler, who developed a general approach for predicting adsorption of proteins by considering that “protein molecules partition from solution into a threedimensional (3D) interphase separating bulk solution from the physical-adsorbent surface”,73 thus considering water displacement explicitly. Other approaches address water mobility for lipids layers,74,75 or surface curvature and hydrophilicity,76 with Monte Carlo and force fields simulations, in the free energies calculations. Note that a comprehensive review of the use of force fields for modeling protein adsorption was done by Robert Latour.77 An important lesson is that the combination of experiments and theory is mandatory for a full understanding of such complex multipartner and multiparameter systems. Two prospective routes are emerging: (i) unravelling a more and more complex system by such a combined theory plus

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Phone: +33 683 594 762. Notes

The authors declare no competing financial interest. Biographies

Dominique Costa is Research Director at CNRS, France. She received her Ph.D. in Material Science in 1989, began at CNRS in 1990, and first specialized in UHV surface analysis techniques (XPS) for corrosion protection of metals and alloys. Then she switched to studying ab initio calculations applied to heterogeneous catalysis, at Laboratory of Surface Reactivity, Paris VI, and was invited one year by the French Institute of Oil. Since then, she has been studying the hard/soft matter interactions ab initio, e.g., biomolecules and organic molecules on surfaces, for applications in corrosion protection, at the Physico Chemistry of Surfaces department at the Institute of Research in Chemistry in Paris, ENSCP ChimieParistech. 7049


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(4) Forster, M.; Dyer, M. S.; Persson, M.; Raval, R. Probing Conformers and Adsorption Footprints at the Single-Molecule Level in a Highly Organized Amino Acid Assembly of (S)-Proline on Cu(110). J. Am. Chem. Soc. 2009, 131 (29), 10173−10181. (5) Humblot, V.; Tielens, F.; Luque, N. B.; Hampartsoumian, H.; Methivier, C.; Pradier, C.-M. Characterization of Two-Dimensional Chiral Self-Assemblies L- and D-Methionine on Au(111). Langmuir 2014, 30 (1), 203−212. (6) Kuhnle, A.; Linderoth, T. R.; Hammer, B.; Besenbacher, F. Chiral Recognition in Dimerization of Adsorbed Cysteine Observed by Scanning Tunnelling Microscopy. Nature 2002, 415 (6874), 891−893. (7) Kuhnle, A.; Linderoth, T. R.; Schunack, M.; Besenbacher, F. LCysteine Adsorption Structures on Au(111) Investigated by Scanning Tunneling Microscopy Under Ultrahigh Vacuum Conditions. Langmuir 2006, 22 (5), 2156−2160. (8) Jones, T. E.; Baddeley, C. J.; Gerbi, A.; Savio, L.; Rocca, M.; Vattuone, L. Molecular Ordering and Adsorbate Induced Faceting in the Ag{110}-(S)-Glutamic Acid System. Langmuir 2005, 21 (21), 9468− 9475. (9) Costa, D.; Pradier, C.-M.; Tielens, F.; Savio, L. Adsorption and SelfAssembly of Bio-Organic Molecules at Model Surfaces: A Route Towards Increased Complexity. Surf. Sci. Rep. 2015, 70 (4), 449−553. (10) Huerta, F.; Morallon, E.; Vazquez, J. L.; Aldaz, A. Electrochemical behaviour of amino acids on Pt(hkl). A voltammetric and in situ FTIR study Part IV. Serine and alanine on Pt(100) and Pt(110). J. Electroanal. Chem. 1999, 475 (1), 38−45. (11) Sandoval, A. P.; Orts, J. M.; Rodes, A.; Feliu, J. M. A Comparative Study of the Adsorption and Oxidation of L-Alanine and L-Serine on Au(100), Au(111) and Gold Thin Film Electrodes in Acid Media. Electrochim. Acta 2013, 89, 72−83. (12) Salmeron, M.; Schlogl, R. Ambient Pressure Photoelectron Spectroscopy: A New Tool for Surface Science and Nanotechnology. Surf. Sci. Rep. 2008, 63 (4), 169−199. (13) Andersson, K.; Ketteler, G.; Bluhm, H.; Yamamoto, S.; Ogasawara, H.; Pettersson, L. G. M.; Salmeron, M.; Nilsson, A. Autocatalytic Water Dissociation on Cu(110) at Near Ambient Conditions. J. Am. Chem. Soc. 2008, 130 (9), 2793−2797. (14) Shavorskiy, A.; Aksoy, F.; Grass, M. E.; Liu, Z.; Bluhm, H.; Held, G. A Step toward the Wet Surface Chemistry of Glycine and Alanine on Cu{110}: Destabilization and Decomposition in the Presence of NearAmbient Water Vapor. J. Am. Chem. Soc. 2011, 133 (17), 6659−6667. (15) Shavorskiy, A.; Eralp, T.; Schulte, K.; Bluhm, H.; Held, G. Surface Chemistry of Glycine on Pt{111} in Different Aqueous Environments. Surf. Sci. 2013, 607, 10−19. (16) Lofgren, P.; Krozer, A.; Lausmaa, J.; Kasemo, B. Glycine on Pt(111): A TDS and XPS Study. Surf. Sci. 1997, 370 (2−3), 277−292. (17) Marti, E. M.; Methivier, C.; Pradier, C. M. (S)-Cysteine Chemisorption on Cu(110), from the Gas or Liquid Phase: An FTRAIRS and XPS Study. Langmuir 2004, 20 (23), 10223−10230. (18) Humblot, V.; Methivier, C.; Pradier, C. M. Adsorption of L-Lysine on Cu(110): A RAIRS Study from UHV to the Liquid Phase. Langmuir 2006, 22 (7), 3089−3096. (19) Jones, T. E.; Rekatas, A. E.; Baddeley, C. J. Influence of Modification pH and Temperature on the Interaction of Methylacetoacetate with (S)-Glutamic Acid-Modified Ni{111}. J. Phys. Chem. C 2007, 111 (14), 5500−5505. (20) Ramakrishnan, S. K.; Martin, M.; Cloitre, T.; Firlej, L.; Cuisinier, F. J. G.; Gergely, C. Insights on the Facet Specific Adsorption of Amino Acids and Peptides toward Platinum. J. Chem. Inf. Model. 2013, 53 (12), 3273−3279. (21) Michaelides, A.; Ranea, V. A.; de Andres, P. L.; King, D. A. General Model for Water Monomer Adsorption on Close-Packed Transition and Noble Metal Surfaces. Phys. Rev. Lett. 2003, 90 (21), 216102. (22) Feyer, V.; Plekan, O.; Ptasinska, S.; Iakhnenko, M.; Tsud, N.; Prince, K. C. Adsorption of Histidine and a Histidine Tripeptide on Au(111) and Au(110) from Acidic Solution. J. Phys. Chem. C 2012, 116 (43), 22960−22966.

Letizia Savio is a researcher at the Istituto dei Materiali per l’Elettronica ed il Magnetismo of CNR, Italy. She received her Ph.D. in Physics at the Università degli Studi di Genova in 2002, discussing a thesis on the role of low coordination sites for the adsorption of simple molecules at Ag surfaces. Later she was a postdoctoral researcher at at the Freie University in Berlin and then at the Università degli Studi di Genova, until she began at CNR in 2008. At present, her research interests are centered on the investigation of molecule−surface interactions at the nanoscopic level by spectroscopic (HREELS and XPS) and microscopic (STM) means. In particular, she has focused her attention on the study of the hybrid organic−inorganic interface and on self-assembly phenomena at metal surfaces and 2D layers.

Claire-Marie Pradier is Research Director at CNRS, France. She received her Ph.D. in Material Science in 1984, and worked for more than 20 years on the adsorption and reactivity of small molecules on model metal surfaces using surface analysis techniques in UHV conditions. She extended her fields of research to the adsorption and self-assembly of amino acids and peptides with applications to the elaboration of biosensors as well as to antiadhesive surfaces, more generally for the understanding and control of the reactivity of metallic surfaces in a biological environment. She is now working at the Labortaoire de Réactivité de Surface, a mixed unit of CNRS and Université Pierre et Marie Curie (Paris VI).

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Adsorption of Amino Acids and Peptides on Metal and Oxide Surfaces

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