Adsorption Behavior and Mechanism of SCA-1 on a Calcite Surface: A

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Adsorption Behavior and Mechanism of SCA-1 on Calcite Surface: A Molecular Dynamics Study Zhengyang Xue, Qiying Shen, Lijun Liang, Jia-Wei Shen, and Qi Wang Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.7b01217 • Publication Date (Web): 30 Jun 2017 Downloaded from http://pubs.acs.org on July 5, 2017

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Adsorption Behavior and Mechanism of SCA-1 on Calcite Surface: A Molecular Dynamics Study Zhengyang Xue1, Qiying Shen2, Lijun Liang3, Jia-Wei Shen2,*, Qi Wang1,* 1

Department of Chemistry, Zhejiang University, Hangzhou 310027, People’s

Republic of China 2

School of Medicine, Hangzhou Normal University, Hangzhou 310016, People’s

Republic of China 3

College of Life Information Science and Instrument Engineering, Hangzhou Dianzi

University, Hangzhou, People's Republic of China ABSTRACT: The crystallization mechanism for natural mineral especially the role of biological molecules in biomineralization is still under debate. Protein adsorption on material surfaces plays a key role in biomineralization. In this paper, molecular dynamics (MD) simulations were performed to systematically investigate the adsorption behavior of struthio camelus eggshell protein struthiocalcin-1 (SCA-1) on calcite (104) surface with several different starting orientations in an explicit water environment. For each binding configuration, detailed adsorption behaviors and mechanism were presented with the analysis of interaction energy, binding residues, hydrogen-bond and structures (such as DSSP, dipole moment and electrostatic potential calculation etc.). The results indicate that the positively charged and polar residues are the dominant residues for protein adsorption on calcite (104) surface, and the strong electrostatic interaction drives the binding of model protein to the surface. The hydrogen bond bridge was found to play an important role in surface interaction 1

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as well. These results also demonstrate that SCA-1 is relatively rigid in spite of strong adsorption with few structural changes in α-helix and β-sheet content. The results of orientation

calculation

suggest

that

the

dipole

moment

of

the

protein tends to remain parallel to calcite in most stable cases, which was confirmed by electrostatic potential isosurfaces analysis. 1. INTRODUCTION Biomineralization is the process by which living organisms produce minerals. Many biological materials such as eggshells, teeth, or nacre exhibit remarkably high strength and toughness in spite of being formed from relatively weak constituents.1 For instance, the inorganic component of eggshell is calcium carbonate, which is hard but brittle, and the remaining components are organic, mainly proteins. Eggshell overcomes the apparent disadvantages of its constituents by combining the strengths of CaCO3 with elasticity of organic matrix to become stiff and tough. It is little surprise that the outstanding mechanical performance is mostly attributed to their unique and complex hierarchical structures at different length scales.2-4 The hierarchical structures are formed under precise control by biomolecules. It is now well recognized that several C-type lectin-like proteins are crucial to the avian eggshell formation.5 This group of protein is thought to have a well-preserved structure with a calcium binding region.2 Among these C-type lectin-like proteins, ovocleidin-17, which received much attention, has been identified as the major protein of calcified Gallus gallus eggshell.6 Some studies revealed that

2


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struthiocalcin-1 (SCA-1) plays an important role in inducing calcium carbonate precipitation and facilitating the formation of a stable form of calcite in struthio camelus eggshell.7,8 The comparative study of SCA-1 and OC-17 confirm about 40% similarity between the sequences of OC-17 and SCA-1. But the locations of some key residues may be different, suggesting that the proteins could perform different functions.9 These studies also observed that the electrostatic potential on two protein surfaces are dissimilar, with OC-17 dominated by a basic patch and SCA-1 dominated by an acidic patch.8,9 Progress in crystallization experiments has improved our understanding of the role of SCA-1 in biomineralization. Marín-García et al.10 have reported the effect of protein SCA-1 on the crystal growth behavior of calcium carbonate (calcite) by dynamic light scattering experiments, and showed that SCA-1 led to considerable changes in the crystal habit and the nucleation process of calcium carbonate. In their work, the electrochemical methods were also employed to investigate the interaction between proteins and the calcite, emphasizing that chemical recognition of SCA-1 toward carbonate ions is more than that toward calcium ions. Sánchez-Puig et al.11 have studied the influence of protein SCA-1 involved in the in vivo biomineralization of calcium carbonate. SCA-1 completely inhibited the formation of biomorphs resulting only in worm-like aggregates due to its chemical interaction with carbonate anions by a chelating mechanism. How proteins interact with inorganic surface is a crucial issue underlying the hierarchical structure of mineralized tissue.12 In particular, the knowledge of the 3


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structural and dynamic basis at the molecular level for this complex physical and chemical issue is fundamental to understand the mechanisms for eggshell’s biomineralization. Molecular dynamics (MD) simulations is an effective tool to provide useful information and approaches for theoretically investigating the binding processes at the interface as well as the adsorption behavior of proteins.13-17 Local features including secondary structural changes, characteristics of the different amino acid side groups, hydrogen bonds etc. can be explained by MD simulations. Yang et al.18 have studied the interaction between peptides and a calcite surface in water and found that these peptides generally have strong interactions with the calcite surface and the peptides changed their configuration to maximize this interfacial interaction. Adsorption behavior of OC-17 on a calcite (104) surface has already been studied by MD simulations,19 and the results demonstrated that the arginine residues are the most important binding sites to carbonate anion. This result was in a good agreement with the works of Reyes-Grajeda et al.6 and Lakshminarayanan et al.20 They also found that OC-17 protein is relatively rigid, without structural changes on contact with the calcite surface. The most stable polymorph of calcium carbonate is calcite. Calcite compose of 95% percent (by weight) of birds eggshell that provides the basis for protection.21 Moreover, calcite possesses high affinity to the proteins, thus calcite is considered as an ideal model to investigate the growth mechanisms of biomineralization and eggshell formation.22,23 The (104) surface of calcite is overall nonpolar and thermodynamically the most stable surface in water solution because of closely 4


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packed, alternatively arranged of the oppositely charged ions.24-26 Therefore, in this study, MD simulation of the adsorption of SCA-1 on calcite (104) surface were performed to explore the SCA-1 adsorption behaviors on calcite surface and the fundamental mechanism of protein-mineral interaction. The knowledge of these basic issues could greatly improve the understanding of mineralization controlled by protein and other biomacromolecules. 2. METHODS 2.1. Simulated System and Force Field. In the current work, the simulation system was comprised of protein SCA-1 placed on calcite (104) surface. The three dimensional structure of SCA-1 was obtained from the protein data bank (ID = 4UWW/4UXM).8 SCA-1 is a compact domain composed of 132 amino acids involving an α/β fold characteristic of the C-type lectin-like domain.27,28 Residues Asp94 and Asp95 located in an acidic patch of the molecule in a flexible loop region and were not built in the structure 4UWW owing to lack of electron density. Meanwhile, residue Asp1 was lost in the structure 4UXM. The coordinates of 4UXM and 4UWW were adjusted by VMD29 to make sure that residues of Asp93 and Asp96 in both structures were overlapped, then the coordinates of Asp94 and Asp95 in 4UXM were added into 4UWW to obtain the actual structure used in this work. The actual structure of SCA-1 used in this work was shown in Figure 1(a) and it involves a α/β fold characteristic of the C-type lectin-like domain.8 Six cysteine residues conserved in the long-form C-type lectin family27 form three disulfide bonds, which impose a large degree of stability on the structure. The protein sequence includes a 5


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large number of negatively charged residues (see Table S1) which give the protein an overall negatively charge of -3e, so three sodium ions were added to the system to maintain charge neutrality in all simulations. The GROMOS53A6 force field were used for protein.30

Figure 1. (a) Overall structure of SCA-1 displayed by the new carton model in VMD. The structure involves two separate regions: a β-strand subdomain and a mixed α/β subdomain containing the N-terminal and C-terminal residues, in which two α-helixes were colored in purple and eight β-sheets were colored yellow. The cysteine residues were represented in VDW mode with the disulfide bridges in yellow. (b) A side view of the calcite (104) surface (Ca2+ ions, cyan spheres; CO32− ions, cyan and red lines). The calcite (104) surface was constructed in Materials Studio 6.1.31 The surface was modeled as a 10-layers slab with a surface area of 9.715 × 9.980 nm2 giving a total of 4800 CaCO3 formula units. Figure 1(b) shows that Ca2+ and CO32− were located in the same layers. The force field parameters of calcite (including the interaction between the solvent and the mineral) were taken from our previous work.32 In all simulations, the SPC/E water model was used for the solvent.33 These force

6


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field parameters had been proven to match the dissociation free energy profile for the Ca2+−CO32− ion pair accurately and were capable of reproducing the water structure and density profile on the calcite (104) surface correctly (see Figure 2(a)) when comparing the data of our previous paper32 and the work of Raiteri et al.,34,35 respectively. In all simulations, the calcite (104) surfaces were placed parallel to the xy plane of the simulation boxes. These simulations adopted the following strategy: the SCA-1 module was firstly embedded in a cubic box with a size of 10 nm, and then it was solvated with SPC/E water. This system underwent an equilibration for 2 ns to allow SCA-1 to relax to a solvated conformation. After preliminary equilibration, the model protein was simply described in a rectangular prism. Six different initial orientations corresponding to each face of the prism were selected lying on the calcite (104) surface, denoted as A to F, respectively. Meanwhile, we noted that most of the protein's carboxyl groups were on one face (see Figure S1(h)). In order to test the fundamental role of the carboxylates in calcite surface adsorption, the face rich in carboxyl groups was placed near the calcite (104) surface and denoted as G system. To avoid the protein being trapped in a potential well, all protein atoms was initially placed at least 0.878 nm away from the first Ca2+ layer in all seven cases, and this distance ensures that there was enough space to contain several layers of water molecules between the proteins and surfaces, as illustrated in Figure S1. In order to ensure that the interaction across the periodic image is negligible for protein adsorption, all systems were built with a sufficiently large space in z direction 7


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(perpendicular to the surface). The simulation boxes in z direction were approximately 12.4~13.7 nm depending on the different orientations of the proteins, resulting in a total of roughly 29 000 to 34 000 water molecules. All of the seven systems were minimized for 50 000 steps or until no instabilities presented. After energy minimization, all systems were pre-equilibrated for 250 ps under NVT ensemble and successive 250 ps under NPT ensemble with the protein backbone restrained to prevent its adsorption before equilibration. Following the pre-equilibration, 100 ns MD simulations were carried out and simulation trajectories were saved every 10 ps. The snapshots were rendered using VMD program29 and Tachyon method.36 2.2. Simulation Details. In this study, all the molecular dynamics (MD) simulations were carried out using the GROMACS version 4.5 package37 with periodic boundary condition set in all directions. The time step was set to 2 fs and the neighbor list was updated every 10 fs. Bond lengths constraints in the CO32− ions were handled with the LINCS method,38,39 while water molecules were constrained using the SETTLE algorithm.40 The cut-off distance of van der Waals interactions was chosen as 1.2 nm. For calculating the long-range electrostatic interactions, the Particle-Mesh Ewald (PME) summation method41 was used with a grid spacing of 0.16 nm, beta-spline interpolation of order 4 and a real space cutoff distance of 1.2 nm. All production MD simulations were performed in NPT ensemble. The temperature was conducted at 310 K via a Nose−Hoover thermostat with a time coupling constant of 0.4 ps. The Parrinello−Rahman barostat was used to maintain pressure at 1 bar, allowing only the z-dimension (normal to the surface) of the simulation box to 8


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fluctuate, with a coupling parameter of 2 ps. 2.3 Analysis Methods. The root mean-square deviation (RMSD) of the backbone atoms (without hydrogen) of SCA-1 was calculated. Several methods were used to analyze the stable interactions among the protein, calcite surface and water which are described below. 2.3.1. Binding Residues and Interaction Energy. This investigation of residues binding to the calcite surface was performed by calculating the distance of all the protein residues from the surface every 10 ps throughout the simulation. The criteria of binding residues was similar to the criteria as reported in Freeman’s work,19 but we chose a longer residence time (5 ns during final 15 ns) to ensure that the residue interacted with the surface steadily. As for the criteria of distance, the existence of the water layers (see Figure 2) provides good standards in this system. If any atom of the residue locates within 0.363 nm (the position of the end of the second water layer on the surface) of the outermost Ca2+ ion layer of calcite (104) surface for 5 ns, it was assumed that this residue is strongly bound. It was considered to be weakly absorbed if this residue located between the second and third water layer for at least 5 ns. The interaction energy, Etot, quantifies the strength of interaction between the calcite surface and the protein (or residue). It was calculated in the conventional way, as show in equation (1) to (3):

Etot = Eele + EvdW

(1)

cal + pro cal pro Eele = Eele − Eele − Eele

(2)

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cal + pro cal pro EvdW = EvdW − EvdW − EvdW

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(3)

cal + pro represents the coulomb potential of the calcite with the protein where Eele

cal pro adsorbed, while Eele and Eele are the coulomb potential of the bare calcite slab cal + pro and free protein. EvdW represents the Lennard-Jones potential of the calcite with cal pro the protein adsorbed, while EvdW and EvdW are the Lennard-Jones potential of the

bare calcite slab and free protein. According to the definition of interaction energy, more negative interaction energy implies stronger adsorption. 2.3.2. Hydrogen Bond. Hydrogen bond analysis has been proved its significance in

the study of organic-inorganic interactions in many previous studies.42,43 In this work, the geometrical criterion of hydrogen bond was defined as: the donor-acceptor distance is lower than 0.35 nm with a maximum donor-H…acceptor angle of 30°. The value of 0.35 nm corresponds to the first minimum of the RDF of SPC water. These criteria were similar to the criteria that Freeman et al. used in their work.19 To analyze the interactions between the protein and surface, the number of hydrogen bonds was counted between the protein and the surface carbonate oxygen every 10 ps. The number of hydrogen bonds between protein and surrounding water as well as the hydrogen bonds within the protein were also calculated. 2.3.3. Protein Structure. The structure of the protein was also examined during the

simulation with various methods. The secondary structure analysis was performed by define secondary structure of proteins (DSSP) method44 in order to discuss the structural changes of SCA-1 during adsorption process.

10


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Furthermore, the orientation of SCA-1 on surface was quantitatively defined as the angle between the normal vector to the surface and the unit vector along the protein dipole.45,46 To investigate this issue in depth, we depicted the electrostatic potential isosurfaces around the proteins at values of ±1 kBT/e computed by the APBS program47,48 and showed with VMD29. The dielectric constant was set to 80.0 for water and 2.0 for the proteins.

Figure 2. Water structure at the calcite (104) surface. (a) The density profiles of water oxygen atom normal to the calcite (104) surface. The zero point was defined by the average z coordinate of Ca2+ ions in the outmost layer of the surface. (b) The first solvation layer was highlighted in blue and the second layer was highlighted in green, while the third layer was colored in orange. The hydrogen bonds between each layer of water molecules and surface were shown in the same color dashed lines in this figure. 3. RESULTS AND DISCUSSIONS 3.1 Interface Water Structure. On the calcite (104) surface, water forms three ordered layers (see Figure 2), which is consistent with the results reported in previous

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studies for different models of H2O and CaCO3.26,34,49-54 Three water layers located at 0.230, 0.363 and 0.589 nm away from the surface, respectively. In the highly ordered layer closest to the (104) surface, water molecules preferentially lie flat on the surface with the OH bonds oriented parallel to the surface, forming hydrogen bonds with the outermost CO32- ions. The second layer of water molecules is less ordered, and water forms directional hydrogen bonds with the surface CO32- ions. The third layer of water molecules is relatively far away from the surface and could not form direct hydrogen bonds with the surface. In a sense, these structured layers of water near the flat surface create big energy barrier for protein adsorption on inorganic material surface.55 The protein cannot adsorb on the surface unless it displace the structured water on the calcite surface. 3.2. Adsorbed Residues and Interaction Energy. During MD simulations, the protein adsorption in all seven cases showed very similar behaviors. SCA-1 approached to the calcite surface gradually with orientation rotated intensely because of the weak attractive interactions when the protein was far from the surface. But soon a few residues were adsorbed on surface and the rotation of protein was highly restricted. As to the curve of RMSD (see Figure S2), it suggested that the systems were stable, because the major structural changed mildly and fluctuated in a narrow range during the final 15 ns of MD simulation except for E system. The special behavior of E system was further discussed in Figure S3 of the Supporting Information. Figure 3 shows the snapshots of final adsorption structure of seven systems with different starting orientation at the end of 100 ns MD simulations in 12


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detail.

Figure 3. (a)-(g) Final states of seven systems with different starting orientation after 100 ns MD simulations. Water molecules and sodium ions were omitted for clarity. SCA-1 was displayed by the new carton model. The strongly adsorbed residues to calcite surface were marked by the VDW model while the weakly adsorbed residues were marked by the CPK model. (h) Final state of G system. The face rich in carboxyl groups was presented in red. In C configuration, SCA-1 bound strongly to the surface in its final state. The groups most adjacent to the surface were positively charged amino groups in Lys2, Lys5 and Lys54, guanidine groups in Arg11 and Arg50, phenolic hydroxyl group in Tyr59 and amide group in Gln58. From the trajectory, it was obviously observed that the guanidine group of Arg11 and Arg50 moved from distant area to the adjacent area to the surface within 20 ns. The interaction between the guanidine groups and the crystalline surface was strong enough to keep these positively charged groups stay on the surface. Meanwhile, the immobility of these two groups facilitate the adsorption

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of other charged groups (amino group in Lys2, Lys5, Lys54) and polar groups (hydroxyl group in residue Tyr59) at about 50 ns. On the other hand, the final minimum distance of negatively charged carboxyl group in Glu47 binding to the surface was 0.474 nm, and it was larger than that of the positively charged residues. After 50 ns, residue Asp9 exhibited the similar trend as Glu47 to be adsorbed on the surface. The final adsorption sites in B and G configurations were same, i.e. amide group in Asn76, hydroxyl group in Ser77 and positively charged amino group in Lys86. The residue Val78 was also adsorbed although it was at a little distance from the surface, which was primarily attributed to the sequence of this residue: the adjacent Asn76 and Ser77 both stay very close to the surface. While in D configuration, the number of adsorption sites was less than that in B, G at the end of the simulation. The protein bound to the surface through two clusters of lysine residues (Lys2 and Lys5) which located in two loops of the protein, creating a “clamp” to the surface. Another residue Asp1 was also closely contacted to the surface for the same reason of Val78 in G configuration (neighboring to Lys2), and the minimum distance of Asp1 from surface was 0.479 nm, which is very close to the distance of Glu47 from surface in C configuration. In conclusion, the contact area between SCA-1 and calcite (104) surface was rather small in B, G, D configurations compared with C configuration. To clearly illustrate our data, all residues of protein adsorbed on the surface and the interaction energy between these residues and surface in all final systems with different starting orientations were presented in Table 1. When classifying the type of 14


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all these residues, we can conclude that most of the binding residues in all seven systems were charged or polar residues, such as arginine, lysine, serine etc. From Table 1, it is apparent that the initial orientation of the protein has large effect on its final adsorption residues. Generally, the configurations with more strongly adsorption sites have relatively larger interaction energies with the calcite surface. It is noticeable that the electrostatic interaction is the driving force of the interaction between the protein and the calcite surface, which agrees well with the simulations of protein adhesion to nanoparticles of amorphous calcium carbonate56 and calcite.19 As to A system, though the contact area of the protein to the calcite in this configuration was rather small, there were three positively charged groups in Arg26, Lys99 and Arg123 strongly adsorbed on the surface. The interaction energy in this system was even larger than that in F system (totally eight residues adsorbed on surface). The situation in D system was quite similar to A system. The C system which possesses strongest interaction energy also indicates the dominant role of the electrostatic interaction between SCA-1 and the calcite surfaces: the overall interaction was notably large due to the strong electrostatic interaction between five positively charged residues (three lysines and two arginines) and the surface. Combined with inspection of all the surface binding scenario discussed before, we conclude that charged and polar residues play a notable role in protein adsorption on calcite surface.

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Table 1. Summary of Binding Residues and Interaction Energiesa between SCA-1 and Calcite (104) Surface for All Systems. Configuration

A

Strongly adsorbed

Weakly adsorbed

Eele

EvdW

Etot

residueb

residuec

kJ/mol

kJ/mol

kJ/mol

-385.95

-3.45

-389.40

Val78

-377.32

5.69

-371.63

Asp9, Glu47

-798.95

-5.62

-804.57

Asp1

-329.59

-7.53

-337.12

Glu47

-582.08

-33.77

-615.85

-354.18

-27.92

-382.11

-337.78

10.78

-327.00

Arg26, Lys99, Arg123

B

Asn76, Ser77, Lys86 Lys2, Lys5,

C

Arg11, Arg50, Lys54, Gln58, Tyr59

D

Lys2, Lys5 Arg11, Ser46,

E

Arg50, Lys86, His88, Tyr89, Ser90

F G a

Asn76,

Val78, Lys87,

Ser77, Lys86, His88

Asp94, Asp96

Asn76, Ser77, Lys86

Val78

the average value of last 15 ns MD simulation; bany atom of the residue located

within 0.363 nm (the position of the end of the second water layer) of the outermost Ca2+ ion layer of calcite (104) surface for a period of time (~5 ns) during last 15 ns; c

any atom of the residue located within 0.589 nm (the position of the end of the third

water layer) of the outermost Ca2+ ion layer of the calcite surface for a period of time (~5 ns) in the last 15ns.

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3.3 Residues Binding Modes. Detailed examination of the interaction energies reveals that the strength of interaction between protein and the surface closely relate to not only the number of adsorbed residues but also the type of them. The binding conformation for each kind of residue was stable in seven systems. Table 2 shed light on the effect of different kinds of adsorbed residues, which was essential to understand the behavior of a surface-bound protein. We selected the time-averaged minimum distance to the surface (the minimum distance between any pair of atoms from the protein and surface) and energy contribution of each kind of residue in all seven systems as the quantitative reference to evaluate the strength of interaction between these residues and calcite (104) surface. We note that there were two types of residues binding to surfaces classified by energy contribution. Noticeably, same result could be obtained when classified by their location in solvation layers of the surface (see Table 1). The first class of adsorbed residues (see Figure 4) which always bind very strongly include positive charged residues like lysine and arginine, histidine, residues with amide group like asparagine and glutamine and residues with hydroxyl group like serine and tyrosine. The minimum distance of these residues from surface varied from 0.298 nm to 0.341 nm, which suggests that the adsorbed groups were mainly located in the second water layers near the surface. The side chains of these residues were able to penetrate the third and second layers of water while the functional groups may strongly interact with the calcite but keep the first ordered water layer intact. During this process, the direct hydrogen bonds formed between these functional groups and outmost CO32- of the surface. 17


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Table 2. The Average Minimum Distancea and Energy Distributionb of Significant Residues in Protein that Bind to the Calcite Surface in Seven Systems Minimum distance Energy contribution Residue

Functional groupc

nm

kJ/mol

Lysine

0.326

-153.14

Arginine

0.298

-120.20

Histidine

0.320

-93.68

imidazole

Serine

0.314

-82.63

hydroxyl group : -OH

Tyrosine

0.317

-96.38

amino group : -NH3+ guanidine group : -C(NH2)2+

phenolic hydroxyl group : -OH

Asparagine

0.315

-86.30

Glutamine

0.341

-69.44

Aspartic acid

0.455

12.85

Glutamic acid

0.472

7.92

Valine

0.539

-7.86

a

amide group : -CO(NH2)

carboxyl group : -CO2-

the minimum distance between any pair of atoms from the protein and surface; bthe

average value of the last 15 ns; cthe functional groups in the side chain of each amino acid were listed. It is necessary to point out that the strong interaction between lysine/arginine and surface is attribute to the fact that positive charged amino groups and guanidine group of SCA-1 bind preferentially to the outmost CO32- of calcite (104) surface (see Figure 4(a) and 4(b)). In these simulations, positive charged residues made a major contribution to the energy due to the electrostatic interaction. Although OC-17 dominated by a basic patch and SCA-1 dominated by an acidic patch, the results of 18


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this study also showed the importance of positively charged residues. Moreover, these simulation results consist with an electrochemical experiment in which SCA-1 was found interacting directly with carbonate anions.10 The selectivity for carbonate was also measured using atomic force microscopy with an electrochemical cell (EC-AFM).7

Figure 4. Snapshots of binding modes for first class of residues. (a) lysine. (b) arginine. (c) histidine. (d) serine. (e) tyrosine. (f) asparagine. (g) glutamine. The residue binding to calcite surface and the donor and acceptor of hydrogen bonds were marked by the CPK model. The red and blue dashed lines represented hydrogen bonds. Water molecules and sodium ions were omitted for clarity. In addition, the oxygen and nitrogen atoms of polar residues such as serine and asparagine could form not only strong hydrogen bonds directly with outmost O atoms, but also indirectly hydrogen bonds with these O atoms via one or two highly polarized water molecules in the first or second solvation layers (see Figure 4(d)-(g)). As a result, the hydrogen bond network here plays a role like bridge that links these polar 19


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groups and surface. After the adsorption of protein, the hydrogen bond bridge formed and broke in a dynamic balance. The importance of water-bridged hydrogen bond for defining distinct binding geometries has previously been recognized for charged amino acids interacting with metaloxides.55 Therefore, in combination with interaction energy demonstrated in Table 1, our results clearly elucidate that the binding of SCA-1 to planar calcite surfaces is dominated by optimal contacts between the first class of residues and the calcite surface. These residues contribute considerable energies to the total interactions between protein and the calcite surface. In contrast, the average minimum distance between the negatively charged residues and surface in these stable configurations was larger than the adsorption distance of first class residues, ranging from 0.455 nm to 0.472 nm. The aspartic acid or glutamic acid occupied positions separated by second and third layers of structured water molecules, preferring an indirect binding state to surface. Similar results had been reported for aspartic acid near the calcite surface by Nada,52 and acrylic acid dimer adsorbed on calcite surface by Zhu et al.,50 and polystyrene sulfonate binding to calcite surface by Shen et al.32 The electrostatic repulsion between the negatively charged R-COO- groups and the negatively charged O atoms of CO32- in the outmost layer of calcite (104) surface is probably the main reason for larger adsorption distance. The water molecules in solvation layers can also block direct interaction between the negatively charged carboxylate groups (R-COO-) and the surface Ca atoms. Presumably the solvent-mediated hydrogen bonds bridge results in adsorption 20


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because the carboxyl group has two electronegative O atoms, which facilitates formation of more hydrogen bond bridges to stabilize the adsorption of these two residues (see Figure 5(a) and 5(b)). Valine also shows very weak interaction with the surface due to steric effect as a result of adjacent residue adsorption. It showed that the valine residue was passively pulled close to the surface. The hydrophobic isopropyl group located in a low-density region (between second and third solvation layers) of the surface water (see Figure 5(c)). Therefore, the aspartic acid, glutamic acid and valine were categorized to the second class of adsorbed residues because of larger adsorption distance and weaker binding strength to surface.

Figure 5. Snapshots of binding modes for second class of residues. (a) aspartic acid; (b) glutamic acid; (c) valine. The residue binding to calcite surface and the donor and acceptor of hydrogen bonds were marked by the CPK model. The red and blue dashed lines represented hydrogen bonds. Water molecules and sodium ions were omitted for clarity. Many experiments have shown that the negatively charged residues like Asp and Glu have large influence on the nucleation and crystal growth of calcium carbonate.20,57 In order to explore the role of these negatively charged residues in

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protein binding, the face that rich in carboxyl groups was initially placed to contact the calcite (104) surface (G system) and subsequent MD simulation was performed. However, this face did not preferentially adsorb on the calcite (104) surface in the simulation (see Figure 3(h)). Nada et al. have reported that the binding of ASP to the Ca2+-kink was much stronger than the binding to the (104) surface, (110) surface and the acute step edge.52 This result was caused by the strength of the electrostatic interaction between the negatively charged residues and different calcite surfaces. The outmost layer of perfect calcite (104) surface are rich in negative O atoms of CO32-, thus it is difficult for the adsorption of SCA-1 with orientation that the carboxyl group-rich face contacts the surface due to the repulsive electrostatic interaction. However, negatively charged carboxyl group prefer to interact with Ca2+ exposed surface or Ca2+-kink attribute to the attractive electrostatic interaction. The electrostatic interaction of negatively charged residues was important during the nucleation and crystal growth process or earlier stages before perfect and large calcite surfaces are formed. As we discussed above, the hydrogen bonds network plays a crucial role in protein

adsorption and

behaves

like

the "glue"

on

the

surface.

Thus,

statistical analysis of the total number of hydrogen bonds between protein with different orientations and three ordered layers of surface water were performed. It is remarkable that this number is positively correlated to the total interaction energy (see in Table 3). Larger network of hydrogen bonds lead to stronger interaction energies.

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Table 3. Numbers of Hydrogen Bondsa between Protein and Ordered Water Layers in Different Configurations. Configuration

1st layerb

2nd layerc

3rd layerd

Total

Etot kJ/mol

a

A

0.75

1.84

10.16

12.62

-389.40

B

2.31

2.57

9.09

13.81

-371.63

C

5.99

5.80

19.73

31.86

-804.57

D

2.79

5.13

10.55

18.48

-337.12

E

6.50

9.80

21.25

37.19

-615.85

F

5.60

6.74

12.47

24.81

-382.11

G

3.38

2.10

6.56

12.34

-327.00

the average value of the last 15 ns; bhydrogen bonds between protein and first

ordered layer of water molecules; chydrogen bonds between protein and second ordered layer of water molecules; dhydrogen bonds between protein and third ordered layer of water molecules. 3.4. Protein Structure Change. To understand the protein structure change during the adsorption process, DSSP44 and intra-molecular hydrogen bonds analysis were performed for A-F systems. The DSSP maps in Figure 6 showed the secondary structure change of SCA-1 with all orientations during the MD simulation. One could find that the secondary structures of protein with all orientations were preserved during the adsorption process. The α-helix and β-sheet content underwent only slightly change during 100 ns MD simulation due to relative weak interactions between these contents and the surface comparing with the intramolecular interaction. (mainly the intramolecular hydrogen bonds) Moreover, as we mentioned in the section of introduction, SCA-1 consists of three disulfide bonds, which means it 23


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possesses a relatively rigid structure. The fluctuation of the secondary structure mainly appeared in the part of loop region while oscillation between turn, coil and bend were frequently observed. From DSSP maps one could see that the protein structure was relatively rigid, and this is in agreement with an important feature of C-type lectin-like protein.27

Figure 6. (a)-(f) Time evolution of the secondary structures of SCA-1 adsorbed on calcite (104) surface computed by the DSSP method during MD simulations for A-F systems. We compared the number of three types of hydrogen bond (intra-molecular, protein-water, protein-surface) in A-G systems with those in the situation of protein in 24


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bulk water, as shown in Table 4. While the protein is getting close with the surface, some direct hydrogen bonds formed between the adsorbed residues and the external CO32-. At the same time, some water molecules in the solvent shell of protein were replaced by the surface ions and led to the reduction of hydrogen bonds between the water and protein. More importantly, the results of DSSP showed that protein underwent small structural deformation and it could affect the intramolecular interaction such as the breaking of intramolecular hydrogen bonds. Table 4. Numbers of Hydrogen Bondsa for the Different Configurationsb from Intra-molecular Interaction of Protein, Protein-water Interactions and Protein-surface Interaction.

a

Configuration

Intra-proteinc

Protein-waterd

Protein-surfacee

Waterf

97.29

296.82

\

A

88.41

288.24

5.13

B

88.42

286.76

4.06

C

89.11

285.84

8.29

D

91.24

286.54

2.44

E

89.00

285.12

6.82

F

90.57

287.78

4.05

the average value of the last 15 ns; bthe solvation of the protein in bulk water was

also given for comparison; chydrogen bonds from intra-molecular interaction of protein; e

d

hydrogen bonds between protein and surrounding water molecules;

hydrogen bonds between protein and calcite surface; fprotein solvated in water

without surface.

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3.5 Orientation of SCA-1 on Surface. The DSSP map can only display the information about the change of protein secondary structure but cannot describe its orientation evolution. Therefore, the angle between protein dipole and the normal vector to calcite surface in A-F cases were calculated and shown in Figure 7. The dipole moment could be obtained from the trajectory of the MD simulation. To investigate this issue in depth, we also depicted surfaces of equal electrostatic potential around the proteins at values of ±1 kBT/e (or ±25.9 mV) by APBS47,48 program. The dipole moments and electrostatic potential isosurfaces for specific system at the end of MD simulation were displayed in Figure 8. As shown in this figure, SCA-1 was characterized by a clear separation of a positive from a negative electrostatic potential region, which is associated with the direction and strength of the dipole moment. In all systems, the direction of dipole moment usually exhibits a relatively large fluctuation at first, which means large rotation or conformational changes of the protein (see Figure 7). Once specific groups of protein were adsorbed on the calcite (104) surface, its orientation would be adjusted to maximize the interaction between protein and surface. These figures clearly show that in most cases (except for D system) the dipole moment of protein would adjust and rotate to the orientation that perpendicular to the normal vector of calcite (104) surface because of nonpolarity of the surface, which is in agreement with the study by Liao et al.58 It would be different for the polar (001) surface or surface with edges and kinks.32

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Figure 7. (a)-(f) Time evolution of the angle between protein dipole and the normal vector to calcite surface for A-F systems during the MD simulation. Figure 8 shows that the angle between protein dipole moment and the normal vector to calcite surface was 104° for C system and 137° for D system, respectively. Herein, C system was the most energetically favorable system and was selected to represent stable adsorbed systems. As for the case of D system, the value of RMSD

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remained stable since 60 ns (see Figure S2(d)) and the protein secondary structure changed mildly (see Figure 6(d)). However, the angle between protein dipole moment and the normal vector to surface stay around 137° from the very beginning of the simulation (see Figure7(d)), and it is larger than the angle in other stable cases (around 90°). As the interaction energy was relatively low in these systems, protein might be stuck in a metastable state in D system.

Figure 8. The final orientations of SCA-1 over the calcite (104) surface in C (top) and D (bottom) systems. The dipole vector was labeled as a red arrow from the center of mass of the protein to the dipole direction in (a) and (c). Isosurfaces of the electrostatic potential around the proteins at −1 kBT/e and +1 kBT/e were colored in red and blue in (b) and (d), respectively.

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It is need to mention that the ionicity has a significant impact on protein adsorption process and adsorbed protein structure.59 The screening effects of the ions slow down the adsorption process and the concentrated ionic region directly above the surface helps to stabilize the protein structure in its adsorbed state. However, in this study we focus on the impact of different residues, the important role of water-bridged hydrogen bonds and the relation between the dipole moment of protein and surface etc. 4. CONCLUSION In summary, our simulations of SCA-1 adsorbed on calcite (104) surface in explicit water solvent can provide valuable structural and thermodynamic information that uncover the control of proteins on growth of inorganic biominerals. The results of the binding residues and strength of the interaction showed the importance of positively charged residues, and suggested that electrostatic interaction is the dominant factor in the adsorption process. Based on the results obtained by residue binding modes analysis, we found that both of the direct contact with surface ions and indirect interactions mediated by the solvent layers near the surface determine the mechanism and strength of adsorption. Moreover, hydrogen bond bridge is crucial for the adhesion of negatively charged residues to calcite (104) surface. The protein secondary structure of α-helix and β-sheet underwent slight change when it binds to the surface, which implies the structural rigidity of SCA-1. The results obtained by dipole calculations suggest that the dipole of protein kept parallel to calcite in most stable cases, which attribute to the fact that calcite (104) surface is a nonpolar surface. 29


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These information can help us to understand the mechanism of biomineralization and design new biomimetic materials. ASSOCIATED CONTENT Supporting Information The detailed structure of protein SCA-1 (Table S1); the initial configurations of all systems (Figure S1); the evolution of the RMSD of SCA-1 in all systems during MD simulation (Figure S2); The snapshots of system E during final 15 ns of MD simulation. This material is available free of charge via the internet at http://pubs.acs.org. AUTHOR INFORMATION Corresponding Author * Tel: +86-571-2886-5674; Fax: +86-571-2886-9344 E-mail: [email protected], [email protected]. Notes The authors declare no competing financial interest. ACKNOWLEDGMENT We acknowledge financial support by the National Natural Science Foundation of China (Grant Nos. 21403049, 21674032, 21503186, 21673206), Qianjiang Talents Program of Zhejiang Province (Nos. QJD1602011).

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Adsorption Behavior and Mechanism of SCA-1 on a Calcite Surface: A

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