PSIIâLHCII Supercomplex Organizations in Photosynthetic Membrane

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PSII-LHCII Supercomplex Organizations in Photosynthetic Membrane by Coarse-Grained Simulation Cheng-Kuang Lee, Chun-Wei Pao, and Berend Smit J. Phys. Chem. B, Just Accepted Manuscript • DOI: 10.1021/jp511277c • Publication Date (Web): 13 Feb 2015 Downloaded from http://pubs.acs.org on February 18, 2015

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The Journal of Physical Chemistry

PSII-LHCII Photosynthetic

Supercomplex Membrane

Organizations by

in

Coarse-Grained

Simulation Cheng-Kuang Lee,a,b Chun-Wei Pao,a* and Berend Smitb,c,d*

a

Research Center for Applied Sciences, Academia Sinica, Taipei 11529, Taiwan

b

Department of Chemical and Biomolecular Engineering, University of California, Berkeley, CA

94720, United States c

Department of Chemistry, University of California, Berkeley, CA 94720, United States

d

Materials Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, United

States

ABSTRACT: Green plant photosystem II (PSII) and light-harvesting complex II (LHCII) in the stacked grana regions of thylakoid membranes can self-organize into various PSII-LHCII supercomplexes with crystalline or fluid-like supramolecular structures to adjust themselves with external stimuli such as high/low light and temperatures, rendering tunable solar light absorption spectrum and photosynthesis efficiencies. However, the mechanisms controlling the PSII-LHCII supercomplex organizations remain elusive. In this work, we constructed a coarse-grained (CG) model of the thylakoid membrane including lipid molecules and PSII-LHCII supercomplex considering association/dissociation of moderately-bound-LHCIIs. The CG interaction between CG beads were constructed based on electron microscope (EM) experimental results, and we were able to ACS Paragon Plus Environment

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simulate the PSII-LHCII supramolecular organization of a 500 × 500 nm2 thylakoid membrane, which is compatible with experiments. Our CGMD simulations can successfully reproduce order structures of PSII-LHCII supercomplexes under various protein packing fractions, free-LHCII:PSII ratios, and temperatures, thereby providing insights into mechanisms leading to PSII-LHCII supercomplex organizations in photosynthetic membrane.

KEYWORDS: photosynthesis, photosystem II, light-harvesting complex II, thylakoid, supercomplex organization, coarse-grained simulation

INTRODUCTION

The supramolecular structure in the photosynthetic membrane, which is analogous to the photoactive layer of solar cells, is highly correlated to photosynthetic efficiency.1,2 In the past two decades, several membrane proteins closely related with photosynthetic processes have been identified, namely, photosystem I, II (PSI, II),3,4 light-harvesting complex I, II (LHCI, II),5-7 ATPase8 and the cytochrome b6/f complex.9,10 In particular, the PSII and LHCII complexes, comprising 90% of the membrane proteins in the stacked grana region, play an essential role in energy and electron transfer in photosynthetic reactions. Interestingly, PSIIs and LHCIIs can self-organize themselves into order/disorder phases, rendering tunable photosynthetic efficiencies to adjust environmental fluctuations.11-16 Understanding the underlying mechanisms of modulating the order/disorder transitions of PSIIs and LHCIIs can be of importance for developing next-generation biomimetic, solar energy harvesting devices that can balance both solar energy conversion efficiencies and device life time. ACS Paragon Plus Environment

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Many PSII-LHCII supercomplexes in the grana membrane have been identified in spinach or in Arabidopsis thaliana by single particle electron microscope (EM) studies.11-16 Figure 1a shows an example of such an EM image and the corresponding structure of the C2S2M2 supercomplex which is defined as a dimeric PSII core (C2), two LHCII trimers (S2) strongly bounded to the PSII core on the antenna complexes CP26 and CP43, and two additional LHCII trimers (M2) moderately bound to the PSII core on antenna complexes CP24 and CP29. For the present study, it is important that the two additional LHCII trimers (M2) are moderately attached to this supercomplex, and can leave the supercomplex to form C2S2M1 and C2S2. These supercomplexes can form random, crystalline, or semi-crystalline domains in the thylakoid membrane under certain conditions that still remain elusive. Potential external stimuli that can lead to the PSII-LHCII supercomplex self-organizations include cold acclimation,17,18 low light acclimation,19 lack of PsbS proteins and absence of specific Lhcb antenna proteins20-22 or interaction between PSII-LHCII supercomplexes in adjacent layers of thylakoid membranes.14,23 There have been a few attempts to investigate the thylakoid membrane proteins’ properties (e.g., diffusion, organization, phase behavior, etc.) by developing coarse-grained (CG) models.24-27 Nevertheless, it is extremely difficult to create a CG model that can study the PSII-LHCII supercomplex organizations with the lateral size of grana membrane compatible with those from EM experiments (ca. 0.5 µm).28

In the present study, a coarse-grained (CG) model based on experimental EM data was constructed to carry out a series of computer experiments of PSII-LHCII supercomplex reorganizations in the thylakoid membrane to study the effects of temperatures and PSII/LHCII

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compositions on the order/disorder transitions of PSII-LHCII organizations. Our CG model of the thylakoid membrane explicitly includes lipid molecules and PSII-LHCII supercomplexes, and is capable of simulating the PSII-LHCII supramolecular organization of a thylakoid membrane of 500 × 500 nm2 in lateral dimensions – compatible with experimental sample size. Our CG molecular dynamics simulations can successfully reproduce several ordered PSII-LHCII supramolecular structures reported in experiments; furthermore, we were able to reveal the underlying correlations of thylakoid membrane protein packing fractions, free-LHCII:PSII ratios, and the order/disorder transitions of PSII-LHCII supercomplex structures, potentially helpful for understanding fundamental photosynthetic processes, and designing next-generation bio-mimetic solar cells.


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Figure 1. Coarse-graining schemes for PSII-LHCII supercomplex and lipid bilayer. (a) CG model of PSII-LHCII supercomplex constructed in the present study. C2S2M2 supercomplex from Arabidopsis thaliana obtained from single particle EM (upper-left panel)12 and corresponding individual parts/subunits (lower-left panel), which can detach from the C2S2M2 supercomplex (two


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moderately-bound-LHCIIs, upper-middle panel) and form two more PSII-LHCII supercomplexes, namely,

C2S2M1

(one

moderately-bound-LHCII,

lower-middle

panel),

and

C2S2

(no

moderately-bound-LHCII, lower right panel). The C2S2M2 supercomplex in CG model representation is displayed in the upper-right panel. Note that the length unit l0 is approximately 1 nm. (b) Lipid bilayer in atomistic (left) and CG model representations constructed in the present study (right). Note in the CG model, beads colored in blue and gray represent hydrophilic and hydrophobic beads, respectively. (c) Typical CGMD simulation system of a single photosynthetic membrane in the present study.

MODEL AND METHODS Construction of coarse-grained model. Our CG model of thylakoid membrane comprises CG

models of the PSII-LHCII supercomplex (the right two panels of Figure 1a), and the lipid bilayer (Figure 1b). For the CG model of the PSII-LHCII supercomplexes, each parts/subunits was mapped into respective CG beads (the upper middle panel in Figure 1a). Each PSII-LHCII C2S2M2 supercomplex contained ten beads, and two of these ten CG beads (beads e and e’) were not topologically connected by CG bonds to mimic moderately-bound-LHCII complexes, which can detach from the C2S2M2 supercomplex to form C2S2M1 (lower middle panel of Figure 1a) or C2S2 (lower right panel of Figure 1a) supercomplex under certain conditions. The upper right panel in Figure 1a depicts the C2S2M2 supercomplex in CG representation. For the CG model of lipid bilayer, we coarse-grained the whole lipid molecule into two CG beads – namely, the hydrophilic and hydrophobic beads (right panel of Figure 1b), based on a CG model derived from dissipative particle


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dynamics (middle panel of Figure 1b).29-31 This CG scheme for the PSII-LHCII supercomplexes and lipid bilayer allowed us to model the order/disorder packings of PSII-LHCII supramolecular structures under various free-LHCII (M):PSII (C2S2) ratios, protein packing fractions, and temperatures of the thylakoid membrane with lateral size of 0.5 × 0.5 µm2, see Figure 1c, thereby providing direct comparisons with experimental results. Note that the spatial resolution of the CG model in the present study is good for studying the supramolecular organizations in the thylakoid membrane, and therefore, is too coarse for taking the orientation dependencies of moderately-bound-LHCII trimmer association/dissociation with the PSII complexes. In the following, we will describe in detail about the parametrization of the CG model depicted above.

Parameterization of coarse-grained model. For fitting the CG force fields between CG beads of PSII-LHCII supercomplexes, we cannot employ conventional atomistic-MD-based (or, the “bottom-up” approach) CG force field fitting schemes such as iterative Boltzmann inversion (IBI) method32-35 or iterative force matching method,36,37 because the sizes of PSII complex and LHCII complex are about 20 and 7 nm, respectively, which are beyond the capabilities of these atomistic-MD-based CG schemes. Therefore, we employed the “combination of top-down and bottom-up” approach instead, that is, we have fitted our CG force fields phenemologically using experimental EM data of the PSII-LHCII supercomplexes. For intramolecular degrees of freedom in the PSII-LHCII supercomplex, the CG bead characteristic lengths (sizes), and angles between CG beads were determined from EM data,

11-16

and all these CG degrees of freedoms were kept rigid

during CGMD simulations.


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The parameterization of intermolecular interactions between CG beads belonging to neighboring PSII-LHCII supercomplexes is the most crucial part for studying the thylakoid membrane supercomplex organizations. In the present study, all the intermolecular CG interactions are fitted into Lennard-Jones (LJ) or shifted Lennard Jones (SLJ) potentials, whose equations are shown in Table S1 (Supporting Information). In fitting the intermolecular interactions, we considered two EM experimental results on the PSII-LHCII supercomplex organizations: (i) the ordered structures of PSII-LHCII supercomplexes and (ii) the dissociation probability of free-LHCII from the PSII core. EM experiments have revealed that C2S2M2 and C2S2 supercomplexes can aggregate and form large-scale order superstructures, for instances, (C2S2M2)n (left panel of Figure 2), and (C2S2)n (right panel of Figure 2), and our CG model must be capable of reproducing order arrays of PSII-LHCII supercomplexes faithfully. Comparing the CG representation of the PSII-LHCII supercomplex in the present study (see Figure 1a) with the ordered structures of both (C2S2M2)n and (C2S2)n (see Figure 2), we noticed that in order to stabilize both ordered (C2S2M2)n and (C2S2)n structures, we must assume strong attraction between species with identical subunit structures (i.e., beads d,e), which is reasonable because subunits with identical structures usually have strong affinities. Hence, we set the LJ/SLJ potential well depth ε of CG bead pairs c-c, b-b, d-d, e-e and d-e to 1 (where is a reference temperature of 298 K). In contrast, ε for a pair a-a and all cross potentials (except c-d/e pairs, see following) and were set to 0.1 to mimic excluded volume effects. Note that the potential energy function of c-c pairs were set to SLJ potential to accommodate the effect of bead center overlapping of bead c (see the right panel of Figure 2) due to dissociation of subunit CP24 upon dissociation of bead

e (moderately-bound-LHCII), see the lower middle and right panels of Figure 1a. ACS Paragon Plus Environment

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Next, we must fine-tune the intermolecular LJ/SLJ interaction parameters to reproduce the probability of free-LHCII association. The probability of free-LHCII association estimated from experiment is 50 % for thylakoid membrane with the protein packing fraction = 0.7 (which is defined as the total projective area of proteins divided by the total projective area of proteins and lipids; see eq 1 for detail definition) and the free-LHCII:PSII ratio = 5 (which is defined as the total number of free-LHCII divided by the total number of PSII; see eq 2 for detail definition).38 To faithfully reproduce the free-LHCII association probability we must tune the LJ potential well depth ε between bead c and bead d/e, because they are directly correlated with the probabilities of free-LHCII bead (bead e) association/dissociation and resultant order/disorder supramolecular structures, see Figure 1a. In the present study, we computed the probability of free-LHCII association for εc-d/e = 1, 2 and 3 , which corresponded to association probabilities of 32.8, 51.8, and 63.1 %, respectively. Note that the criterion of free-LHCII association is defined as when the distance between centers of bead c and bead e less than 4.2 nm (i.e., σc-d/e) plus 2 nm (i.e., the effective van der Waals interaction range), which are referred by Figure S1 (Supporting Information); otherwise, free-LHCIIs were considered dissociated from PSII complexes. Therefore, in the present study, we picked εc-d/e = 2

. The parameters of all CG force fields constructed in the present study are compiled in Table S1 (Supporting Information).


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Figure 2. Configurations of ordered (a) (C2S2M2)n and (b) (C2S2)n supercomplexes with n = 4.

The CG model for lipid bilayer in the present study was based on a CG model derived from dissipative particle dynamics.29-31 In order to accommodate lipid CG particle sizes with those of PSII-LHCII CG beads, further coarse-graining is required. We further coarse-grained the hydrophobic and hydrophilic parts of a lipid molecule into two CG beads, namely, hydrophilic (bead f) and hydrophobic (bead g) beads. The intermolecular CG force field between lipid CG beads was constructed in the LJ forms with both εff and εgg equal to 0.5 to moderately bound lipid molecules. The lipid bilayer helped fill the volume space of the thylakoid membrane, and in the present study the CG interaction force field between lipid beads and PSII-LHCII beads were set in the LJ form with small ε = 0.1 to mimic the hard sphere interaction. Furthermore, the lateral dimension of the lipid molecule is 1.8 nm, which is not too small comparing with that of the smallest CG bead in the PSII-LHCII complexes (namely, bead b with bead size 5.0 nm); hence, modeling lipid bilayer as implicit solvent might lead to underestimation of interaction between PSII-LHCII supercomplexes and surrounding lipid molecules. Note that the proposed CG model of PSII-LHCII


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supercomplexes without explicit lipids could be employed in Monte Carlo method (e.g., Ref. 27), but it is needed to re-estimate the interaction force field for PSII-LHCII beads; it also be employed in Brownian dynamics simulation, but it is necessary to find a reasonable way to deal with lipids as Brownian and drag forces on of PSII-LHCII beads.

Simulation conditions. In subsequent CG simulations, we simulated the PSII-LHCII supercomplex organizations in the thylakoid membrane with size ca. 500 × 500 nm2, which is compatible with experiments, thereby providing direct comparisons with experimental observations. The CGMD simulations were carried out in NVT ensemble using NAMD2,39 with a temperature range of 298 K ± 20 K. A time step of 0.001 τ was used in the CG simulation for run 20 million steps totally, where the time scale τ is defined as 1 ns by comparison of diffusion coefficient of DLPC lipids (ca. 1-3 × 10−8 cm2/s) with atomic MD simulation.40 Note that despite the lipid compositions of spinach thylakoid membranes is different from DLPC lipids,41 the diffusion coefficient of lipids in thylakoid membrane should still be in the same order of magnitude as DLPC lipids. Hence, in the present study, it is reasonable to rescale the CGMD simulation time based on diffusion coefficients of DLPC lipids. All CG beads of lipids and proteins were restrained in the z direction and simulation cell in the lateral dimensions were periodic. Note that the z direction of photosynthetic membrane is outward stroma or lumen.

RESULTS AND DISCUSSIONS

In this section, we will present our CGMD simulation results of PSII-LHCII supercomplex organizations under various thylakoid membrane protein compositions. The protein packing fraction ACS Paragon Plus Environment

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and the free-LHCII (M):PSII (C2S2) ratio are two of the most important factors that influence the overall supercomplex organizations of the thylakoid membrane. The protein packing fraction is defined as

=

,

(1)

where and !"# are the total projective area of proteins (including PSIIs and LHCIIs) and lipids, respectively. In the present study, a range of 0.6 ≤ ≤ 0.9 was chosen to make direct comparisons with experiments.13,42-44 The free-LHCII (M):PSII (C2S2) ratio is defined as

=

() *+,-- (/) ( 1-- (,2 12 )

,

(2)

where 345!6788 (9) is the total number of free-LHCII and moderately-bound-LHCII (regardless of binding to C2S2 supercomplexes or not), namely, the total number of CG bead e, and the 3:88 (72 :2) is the total number of PSII (C2S2) supercomplexes in the membrane. Note that in this work, the free-LHCII and the moderately-bound-LHCII are of the same beads and they are all labelled as M. A range of similar to experiments (2 ≤ ≤ 5) was chosen.19,44,45 Note that the reason we explored supercomplex organization under such a wide range of is based on the following observations: (i) various plants or conditions provide different amount of free/moderately-bound-LHCIIs19,45,46 and (ii) the free-LHCIIs may move from the PSII-enriched grana regions to the PSI-enriched stroma lamellae regions.47-49


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PSII-LHCII supercomplex organizations. Figure 3a displays the supercomplex organizations of the thylakoid membrane for different values of and from our CGMD simulations. From Figure 3a, it is evident that the PSII-LHCII supercomplex organizations are very sensitive to both and . In the regime of high and (left panel Figure 3a), we notice that the thylakoid membrane protein phase separated into three phases: (i) a large C2S2M2 phase mainly comprised of ordered (C2S2M2)n domain; (ii) an interconnected free-LHCII phase surrounding the large C2S2M2 phase, and (iii) small isolated lipid molecule domains due to high . Such an organization has been revealed in EM experiments.11-16 The structural detail of the ordered (C2S2M2)n PSII-LHCII domain from CGMD simulation is displayed in the upper left panel of Figure 3b, In the upper left panel of Figure 3b, the 2D lattice vectors of ordered (C2S2M2)n domain, a and b, can be easily identified. The upper middle panel of Figure 3b displays the ordered (C2S2M2)n from EM experiments, which is in good agreements with our CGMD simulations. To quantitatively compare our ordered (C2S2M2)n structure with experiments, we plotted the 2D PSII center of mass (CM) distribution scatter plot from our simulations, see the upper right panel of Figure 3b. In this 2D PSII CM distribution scatter plot, points colored in red and blue highlight the PSII CMs in ordered and disordered packing, respectively. We found the ratio of vector length |>|/|@| = 0.90 ± 0.05 with unit vector angle B = 73.9 ± 3.7° , which are in good agreements with the experimental values (|>|/|@| = 0.82 and B = 74.8° ), manifesting that the CG model constructed in the present study can successfully reproduce the experimental ordered (C2S2M2)n structure.


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In the low and regime ( = 0.6 and = 2, see the right panels of Figure 3a), in contrast, the thylakoid membrane phase separated into one large interconnected lipid domain, one large domain of ordered (C2S2)n, and domains of PSII-LHCII supercomplexes comprised of disordered C2S2M2, C2S2M1, and C2S2 supercomplexes. This is exactly what is observed at these conditions.13 The structural detail of the ordered (C2S2)n domain is displayed in the lower left panel of Figure 3b. Once again we analyze the 2D lattice vectors a and b of ordered (C2S2)n structures by plotting the PSII CM distribution scatter plot (lower right panel of Figure 3b), and the ratio of vector length |>|/|@| and angle B are 1.46 ± 0.05 and 88.4 ± 2.8° , respectively, which are in good agreements with those measured from experiments (|>|/|@| = 1.53, B = 87.6° ).

In addition to ordered (C2S2M2)n and (C2S2)n phases, our CGMD simulations revealed an ordered structure of (C2S2M1)n (e.g., = 0.7 and = 3, see the middle panels of Figure 3b). Such an ordered (C2S2M1)n phase has not been identified experimentally. The structural details and corresponding 2D PSII CM distribution scatter plot of (C2S2M1)n are both displayed in Figure S2 (Supporting Information). Note that EM data inferred that it is likely that pure (C2S2M1)n supercomplexes can coexist with both (C2S2M1)n and (C2S2M2)n.16

From Figures 3, we can find that the CG model presented in this study can faithfully reproduce the ordered PSII-LHCII supercomplex structures reported in the EM experiments, which further validates the present CG model for exploring the supercomplex organizations of thylakoid membrane. Next, based on this CG model, we will explore the correlations of PSII-LHCII supercomplex


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organizations with various protein packing fractions, free-LHCII:PSII ratios, and temperature fluctuations, which have not yet been revealed from experiments.

Figure 3. (a) The PSII-LHCII supercomplex organizations from CGMD simulations for type (C2S2M2)n (left panels, = 0.9 and = 5), (C2S2M1)n (middle panel, = 0.7 and = 3), and (C2S2)n (right panels, = 0.6 and = 2 ). The upper and lower panels display the thylakoid ACS Paragon Plus Environment

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membrane from three-dimensional and combination of top-down and bottom-up perspectives, respectively. Note in the CG model, beads colored in red, various green, blue and gray represent PSII cores, LHCIIs/CP24/CP26/CP29, hydrophilic and hydrophobic parts of lipids, defined as same as that in Figure 1a. In the lower panels the lipid molecules are not displayed for clarity. (b) left panels: structural details of ordered (C2S2M2)n (upper left) and (C2S2)n (lower left); middle panels: structural details of (C2S2M2)n (upper middle) and (C2S2)n (lower middle) from EM experiments;13 right panels: the 2D PSII CM distribution scatter plots of (C2S2M2)n (upper right) and (C2S2)n (lower right) from CGMD simulations. Note in the 2D PSII CM distribution scatter plot, points colored in red and blue highlight the PSII CMs in ordered and disordered packing, respectively.

Effects of protein compositions and temperatures on PSII-LHCII supercomplex organizations. We first examined the effects of protein packing fraction and free-LHCII (M):PSII (C2S2) ratio on the number-weighed supercomplex type distribution, which is critical for photosynthetic efficiencies, and has not been studied in detail from experiments. Figure 4 displays the probability distribution of C2S2, C2S2M1, and C2S2M2 supercomplexes as the functions of and . From Figure 4, it is clear that the supercomplex organization is very sensitive to and . For high and we find most of the PSII-LHCII supercomplexes are in the fully associated C2S2M2 form, while for low and we find mainly C2S2. This can be attributed to the shift of chemical equilibrium of the following reaction:

CN SN + 2M ↔ CN SN MS + M ↔ CN SN MN ,


(3)

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because of the dependencies of the chemical potential of free-LHCII on and . Higher and lead to higher free-LHCII concentrations, which in turn raises chemical potential of free-LHCIIs, thereby shifting the chemical equilibrium in eq 3 toward C2S2M2.

It is also interesting to find that the fluctuation in the composition of C2S2M1 is rather small upon fluctuation in thylakoid membrane compositions. This can be attributed to reaction intermediate nature of the C2S2M1: while concentration of free-LHCII rises, despite promoting the association of free-LHCII with C2S2 to form C2S2M1, free-LHCII can also associate with existing C2S2M1 to form C2S2M2, thereby reducing the concentration of C2S2M1. On the other hand, while concentration of free-LHCII drops, the chemical equilibrium shifts toward C2S2 supercomplexes; despite low free-LHCII concentration promoting C2S2M1 dissociation into C2S2, low free-LHCII concentration also promotes C2S2M2 dissociation into C2S2M1 to compensate dissociation of existing C2S2M1 supercomplexes.

The lipid molecules play an important role in the PSII-LHCII supercomplex organizations. From Figure 4, it is evident that for given free-LHCII:PSII ratio, lower protein packing fraction (namely, more lipid molecules in the membrane) tends to hinder association of free-LHCII with C2S2 and C2S2M1 supercomplex to form C2S2M2 supercomplexes. This implies affinity between PSII-LHCII supercomplex and lipid molecules, which can be attributed to entropic effects that promotes mixing of dissimilar species.


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Figure 4. Number-weighed supercomplex type distribution with varying the protein packing fraction, , and the ratio of free-LHCII (M):PSII (C2S2), .

We also monitored the change in ordered domain sizes of PSII-LHCII supercomplexes with respect to CGMD simulation time, and we noticed that in all cases domain size became stable after 20 million steps of CGMD simulations. The stabilization of ordered domain size can be attributed to the balance between supercomplex cohesive energy (promoting formation of ordered domains) and entropic effects (promoting dissociation of supercomplex). Nevertheless, ordered domains are not stable under temperature fluctuations, as will be discussed below.


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All the CGMD simulations above were carried out at 278 K. To examine the effects of temperature on the supercomplex organizations, we carried out CGMD simulations at higher temperatures (298 K and 318 K) of the thylakoid membrane in the low and regime (right panels of Figure 3a). We must stress out that the highest temperature 318 K is critical to be considered in this work, which would not only affect the structural destabilization but also inhibit the oxygen evolving complex or induce permanent damage,50,51 which could not be taken into account in the present CG model. The insets of Figure 5 shows that at low or room temperatures we have the ordered or semi-ordered (C2S2)n phase which is in agreement with experimental observations11-16 and at high temperature we have an amorphous, liquid-like, organization. Such loss of long-range-ordering could also be the potential reason leading to the deterioration of photosynthetic efficiencies under sunlight or elevated temperature. To quantitatively analyze the degree of order of the supercomplexes, we use the averaged local order parameter (ALOP) analysis,52 which has been employed in analyzing degrees of crystallinity in polymer solar cells. The details of ALOP analysis are depicted in the Supporting Information. The PSII-LHCII supercomplex structures are considered in the ordered phase if the ALOP (the vertical axis of Figure 5) is greater than 0.3. From Figure 5 it is clear that the local order parameter undergoes significant drop upon temperature rising and loss of long range order. Nevertheless, such order/disorder transition is reversible upon heating/cooling, as will be discussed below.


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Figure 5. The averaged local order parameter (ALOP) of the PSII-LHCII supercomplexes with respective to temperatures with = 0.6 and = 2. Insets: upper panels: PSII-LHCII supercomplex organizations and lower panels: the PSII CM distribution scatter plots at 278K (left), 298K (middle), and 318K (right). Note in the CG model, beads colored in red and various green represent PSII cores and LHCIIs/CP24/CP26/CP29; in the 2D PSII CM distribution scatter plot, points colored in blue represent the PSII CMs.

Figure 6 displays the (C2S2M2)n supercomplex organizations of the thylakoid membrane (in the high and regime) heated from 278K to 318K, and cooled from 318K back to 278K. It is clear that the PSII-LHCII supercomplexes recrystallize into ordered structure upon cooling from 318 K back to 278 K. Since this order/disorder transition is thermally reversible, we may correlate such


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reversible transition with the order/disorder transition of supercomplexes under sunlight, which is reasonable because the ambient temperature rises under sunlight.

Figure 6. Reversible order-disorder transition of PSII-LHCII supercomplex organizations during heating/cooling cycle between 278 K and 318K, demonstrating that the PSII-LHCII supramolecular structures in the thylakoid membrane are reversible with respect to temperature fluctuations. The crystalline regions are marked as solid black lines.

CONCLUSIONS

In order to investigate PSII-LHCII supercomplex organizations in the thylakoid membrane under various protein composition and temperatures, we constructed a CG model of thylakoid membrane


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including CG models of lipid molecules and PSII-LHCII supercomplexes incorporating association/dissociation of moderately-bound-LHCIIs. The lateral dimensions of the thylakoid membrane were 500 × 500 nm2 in our CGMD simulations, which were compatible with experiments. By carefully tuning the CG force fields, we were able to reproduce EM experimental observations, in particular, the association probabilities of free-LHCIIs on PSII supercomplexes. From a series of CGMD simulations of thylakoid membranes under different protein packing fractions and free-LHCII (M):PSII (C2S2) ratios, we were able to reveal the structural transition of the PSII-LHCII supercomplexes (i.e., CN SN + 2M ↔ CN SN MS + M ↔ CN SN MN ), and reproduce the ordered (C2S2M2)n and (C2S2)n phases, manifesting the validity of our CG model. We systematically explored the supercomplex organizations under various protein packing fractions and free-LHCII:PSII ratios, which has not been studied in detail from experiments, and our CGMD simulation results indicate that PSII-LHCII supercomplex organizations are very sensitive to both protein packing fraction and free-LHCII:PSII ratio. Finally, our CGMD simulations indicated that the PSII-LHCII supercomplexes lose their long-range order as temperature rises, which might be the reason leading to the drop in photosynthetic efficiencies at elevated temperatures; furthermore, such order/disorder transition of PSII-LHCII supercomplexes is thermally reversible upon heating/cooling, which might be able to explain the mechanism behind order/disorder transition of supercomplex organizations with or without sunlight. The present study therefore provided insights into the correlations between membrane

protein

compositions,

temperatures,

and

resultant

PSII-LHCII

supercomplex

organizations, potentially helpful for understanding the structural transitions of membrane protein in the photosynthetic membrane under various environmental fluctuations. ACS Paragon Plus Environment

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ASSOCIATED CONTENT

Supporting Information Additional figure and analytical detail. This material is available free of charge via the Internet at http://pubs.acs.org.

AUTHOR INFORMATION

Corresponding Author *E-mail: [email protected] (C. W. P.); [email protected] (B. S.)

ACKNOWLEDGMENTS

C.-K. Lee thanks S. Katira, Dr. A. Benjamini, Dr. A. R. Schneider, Prof. Y.-C. Cheng and Prof. K. K. Niyogi for helpful discussions about the study and also thanks the support of the talent development program between Academia Sinica of Taiwan R.O.C. and elite American universities and research institutes; C.-W.

Pao

thanks

the

National

Science

Council of

Taiwan

project

No.

99-2112-M-001-004-MY3 and 102-2628-M-001-004-MY3, and Academia Sinica Thematic Project No. AS-103-SS-A02 for financial support, as well as computational support by the National Center of High-Performance Computing of Taiwan, ROC. This research was supported by grant FWP-SISGRKN from the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, U.S. Department of Energy.

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