Letter pubs.acs.org/JPCL
Water Collective Dynamics in Whole Photosynthetic Green Algae as Affected by Protein Single Mutation Daniela Russo,*,†,‡ Giuseppina Rea,§ Maya D. Lambreva,§ Michael Haertlein,∥,⊥ Martine Moulin,∥,⊥ Alessio De Francesco,† and Gaetano Campi§ †
CNR Istituto Officina dei Materiali c/o Institut Laue Langevin, 38042 Grenoble, France Institut Lumière Matière, Université de Lyon 1, 69100 Lyon, France § CNR Istituto di Crystallografia 00015 Monterotondo Scalo, 70126 Roma, Italy ∥ ILL Deuteration Laboratory, Partnership for Structural Biology, 38042 Grenoble, France ⊥ Life Sciences Group, Institut Laue-Langevin, 38000 Grenoble, France ‡
S Supporting Information *
ABSTRACT: In the context of the importance of water molecules for protein function/ dynamics relationship, the role of water collective dynamics in Chlamydomonas green algae carrying both native and mutated photosynthetic proteins has been investigated by neutron Brillouin scattering spectroscopy. Results show that single point genetic mutation may notably affect collective density fluctuations in hydrating water providing important insight on the transmission of information possibly correlated to biological functionality. In particular, we highlight that the damping factor of the excitations is larger in the native compared to the mutant algae as a signature of a different plasticity and structure of the hydrogen bond network.
W
In this context, we studied the function/dynamics relationships occurring in Chlamydomonas reinhardtii strains hosting an amino acidic substitution in the photosynthetic D1 protein, and its corresponding reference strain, in order to identify parameters correlated with a more efficient photosynthetic performance. The D1 protein constitutes the reaction center core of Photosystem II (PSII) as a heterodimer with the D2 protein, and plays key roles in the photosynthetic energy conversion process and its regulation (see Supplementary Figure S1.A,B). The D1 primary structure is highly conserved among photosynthetic organisms to guarantee the proper D1 functionality in physiological conditions.26 Recently, by combining an in vitro molecular directed evolution strategy with in silico studies, we found that in the unicellular green alga C. reinhardtii, even single amino acidic substitutions in the D1 protein enable the cells to face stressful environmental conditions.27,28 This experimental approach allowed the selection of a mutant hosting an amino acid replacement in a crucial region of the D1 protein mediating the electron transport and oxygen evolution processes: the Isoleucine 163 Asparagine (I163N) mutant (see Supplementary Figure S1.C). The main distinctive traits of I163N were the higher rate of oxygen production under saturating light intensity,29 and the ∼50% reduction of chlorophyll a (Chl a) per cell content
ater molecules are intimately connected to biological systems and are associated with life. In most biological conditions, water molecules form hydrogen bonds with the heterogeneous biological interface, with other water molecules close to the surface, or simply accummulate in isolated small pools. Removal of water molecules by dehydration can yield structural, dynamics, and functional alterations. In this picture it has been established that a critical amount of water content is necessary to induce large amplitude dynamical fluctuations ,which may be necessary for protein activity.1−5 For this reason, most investigations have focused on the structural and dynamical properties of the first hydration layer (water molecules that cover the exposed biosurface) spanning from protein hydrated powders to living cells.6,7 External parameters such as temperature,8−12 solvent composition,13−17 and pressure18−21 have been widely exploited to investigate protein and water dynamics with the aim to understand whether there is an intrinsic dynamics of all proteins and/or a f unctional dynamics characterizing the biological function. A new and original way to examine the problem has been to play directly with the activity parameter introducing single point mutations able to switch on and off the functionality of the protein without perturbing the structure. Among a variety of biological possibilities, photosynthetic complexes are of particular interest;22−25 it was in fact demonstrated that mutation type and localization impacted photosynthetic performance in a different manner. © XXXX American Chemical Society
Received: May 3, 2016 Accepted: June 14, 2016
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Figure 1. Coherent inelastic spectra of intracellular water of intact wild type at selected Q-values. The black thick line shows fits of the data with two DHOs model (details are described in the Supporting Information). The black thin line shows the experimental resolution function. The blue and green dotted lines respectively represent the resulting low- and high-frequency DHO. Finally, also the calculated multiple scattering is shown (dashed magenta line).
Figure 2. Experimental dispersion curves of THz collective modes in hydration water of (a) hydrated wild-type and I163 mutant cells, (b) 60% dehydrated wild-type and I163 mutant cells, and (c) highly hydrated powders. The dispersion curve of bulk water is reported for comparison.
compared to the wild type (WT)30 (see Supplementary Table S1). Chl a is one of the main constituents of the antenna complexes involved in light harvesting and energy conversion reactions. This important modification points out the relevance of single amino acid substitution in the remodeling of specific algal metabolic pathways, and led to hypothesize the onset of either local or large scale modifications underlying the stresstolerant phenotype. The differences between the WT and mutant strains to the harsh environment stand out during low earth orbit space missions characterized by the occurrence of both microgravity and complex cosmic radiation.29,30 In flight, C. reinhardtii mutants featured a higher photochemical efficiency compared to the wild type. After landing, in addition to a better photosynthetic performance, the mutant displayed a faster rate of regrowing compared to the wild-type, both indicating an improved capacity of recovery from stressful conditions (see Supplementary Table S2). This trait was correlated, among other factors, to the nature of the single point mutation that led to replacement of amino acid more sensitive to oxidative damage (Isoleucine) with less sensitive ones (Asparagine), supporting a pivotal role of the D1 primary structure in modulating PSII functioning. However, molecular mechanisms underlying stress tolerance rely on a complex interplay of signal networks affecting multiscale properties from molecular scale in DNA mutation up to macroscopic scale in the whole-cell behavior. At the molecular level, most biological processes happen at interfaces where water contacts other macromolecules. This is due to the cooperative mechanism of the dense H-bond network able to transmit dynamic perturbations much larger
than the structural perturbation. The analysis of hydrogen bond network has been shown to constitute an indirect way to attempt a comprehensive description of function/dynamics correlation. To shed light on the impact of structural fluctuations (effects) due to single point mutation on larger scale properties, we investigated intracellular water collective dynamics in whole photosynthetic algae cells. It is a reasonable assumption to imagine that, since these collective excitations exist31−36 and propagate with thermal energies, they will have an effect on the overall dynamics of the hydrated macromolecule and its biological activity. In this Letter we present neutron Brillouin measurements on completely deuterated wild-type and I163N algae with variable intracellular water content (details are described in the Supporting Information). The method gives a detailed description of dispersion curves, providing a picture of the physical characteristics of active collective motions (optic-like, acoustic-like, dispersive). The analysis of the related damping factor gives access to the lifetimes or propagation lengths, of those motions, somehow related to the local structure of the propagating medium. The experiments were performed on completely deuterated Chlamydomonas algae (including intracellular water). The wild type and I163N mutant were measured as a function of intracellular water content (details are described in the Supporting Information). Therefore, intact cells with physiological amount of water, 60% dehydrated cells, and highly hydrated powders were measured at room temperature. 2430
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Figure 3. (a) Damping factors for the intact wild-type and I163N Chlamydomonas. (b) Damping factors for the 60% dehydrated WT and I163N Chlamydomonas. In panel c we show the damping factor of the highly hydrated powders. Damping factor of the bulk water is shown (dashed line) for comparison.
In general, taking into account as well previously published results,37 it is clear that an absolute and precise measurement of the velocity of collective motions in biological solutions is challenging. The similar behavior of hydration water dispersion curves37 of biomacromolecules shows that the collective excitations are correlated to the general average chemical heterogeneity of the biointerface (i.e., hydrophilic, hydrophobic, polar sites). To this direction, it has also been demonstrated that completely homogeneous hydrophilic or hydrophobic interfaces shape the high frequency mode in a major way.37,39 Then, to shed light on whether single point mutations in the PSII D1 protein are able to affect the function of the system, leaving a fingerprint in the collective dynamics, we further analyzed the damping factor of the excitations, since it was previously suggested that it can bring complementary and significant information on the properties of local water structure. In the case of a whole protein, this will result in an averaged distortion, which will appear like an average lifetime of the collective excitations. It is worth remarking that, in the intact cell, hydration water molecules also interact with other water molecules within an extended hydrogen bond network and three-dimensional space. By contrast, in the dehydrated cells and hydrated powders, hydration water interacts almost exclusively with the biomolecular interface; given the small number of neighboring water molecules (likely none in the case of hydrated powders) ,the interaction range is limited to a surface and a two-dimensional space. Figure 3 reports the damping factor of the (a) intracellular water of the wild type Chlamydomonas and I163N mutant and (b) 60% dehydrated cells together to bulk water. Despite the similarity of the dispersion curves, the interaction of water with a biomolecule affects the damping factors associated with the propagating high frequency showing a distinct behavior for the wild type and the mutant. As in the case of DHO frequencies, the damping factors associated with the low energy mode do not depend on the sample characteristics, depicting a similar behavior. Therefore, we will discuss only the damping of the high frequency mode. Figure 3a,b reports the damping for the intracellular water as inferred for the wild-type Chlamydomonas cell and the mutant in both intact and dehydrated configuration. In both cases, the trend is consistent and does not change with the dehydration. In particular, we observe that the wild-type damping factor is larger compared to the mutant as a signature of a different
Figure 1 shows selected experimental data set, at three wave vector values, of the wild-type Chlamydomonas algae, together with the best fit using a two-component damped harmonic oscillators (DHO; details are described in the Supporting Information). In order to characterize water collective excitations propagating throughout the system, we analyzed the dependence on the momentum transfer of the proper frequencies, of the DHO’s, defining the dispersion curves (Figure 2). The collective excitations were found to be characterized by a high-frequency mode of dispersive nature, and a low-frequency mode of almost constant energy. The presence of the two distinct modes is a common finding in bulk and hydration water.37 In particular, the so-called low-frequency mode displays an optic-like character with a constant energy of about 5−6 meV, which is related to O−O−O intermolecular bending motions of the hydrogen bond network.37,38 The acoustic-like high-frequency mode is characterized by energies that increase linearly with the momentum Q. Figure 2 shows a comparison of the dispersion curves of the intracellular water of the wild type Chlamydomonas and its I163N mutant in the case of (a) intact whole cells, (b) 60% dehydrated cells, and (c) highly hydrated algae powders, together with bulk water. The low Q slope provides the intracellular propagation velocity of collective excitations which are, for the intracellular water of the wild-type Chlamydomonas algae, on the order of 3150 ± 50 m/s. In the case of intact living algae, the amount of intracellular water represents 80% of the total weight of the organism, and the presence of bulk water dominates the frequencies of the two modes, which seem not to be affected by the mutations and are superimposed to the bulk water behavior (Figure 2a). Upon dehydration, the contribution of the hydration water component is more important, and the collective density fluctuations are characterized by a slightly larger velocity of propagation (average 3400 ± 100m/s, Figure 2b). Actually, despite the large error bars, which are not only related to the quality of the data (reduced water contribution) but also to the fitting modeling, it is possible to remark a smaller but significant agreement between bulk water and algae’s dispersion curves. A small difference between the two samples might be observed, although the large error bars do not allow a precise evaluation and discussion of the velocity of collective excitations. The highly hydrated powders, as represented in Figure 2c, also show a good agreement with the bulk dispersion curve. 2431
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stress conditions. The present results provide significant experimental insights into the protein function/dynamics relationships and its correlation to water dynamics. In particular, improvement in the efficiency of photosynthesis finds valuable applications in different research fields including bioenergy, green chemistry, and agribusiness.43−45
plasticity and structure of the hydrogen bond network. Indeed in both wild-type Chlamydomonas cell and the mutant the damping factor, Γ(q), is well fitted by a power law Cqα. We find that Γ(q) = ∼34q2.1 and Γ(q) = ∼24q1.9 for the wild-type Chlamydomonas and theI163N mutant cells, respectively. This behavior is confirmed in the dehydrated samples. Here we find the same power law exponents, α = 2.1 and 1.9 for the wildtype Chlamydomonas and theI163N mutant cells, respectively, but larger C factors: 40 and 30 for the wild-type Chlamydomonas and the I163N mutant cells, respectively. Taking into account previous published results,37,32 it is possible to speculate that high damping implies a denser and/or stiffer local environment. The higher the damping, the faster the propagating waves die. This corresponds to the idea that a photosynthetic wild-type cell requires a relatively rigid environment to function, and locally propagates the information under physiological conditions. At the same time, the larger flexibility that can be assumed by the mutant environment could be related to its ability to resist stressing conditions. Only a direct comparison of mutants versus wild-type biomolecules could highlight these properties which seem to be confirmed by single-atom dynamics investigation on the same living systems,40 reaction center from bacteria,22 and eventually comparing native to unfolded or intrinsically disordered proteins.41 On the other hand, this picture is not in contradiction with the recognized idea that flexibility, eventually induced from an established water network, is crucial for the protein activity. To this purpose, Figure 3 compares the wildtype Chlamydomonas with the 60% dehydrated algae to the highly hydrated powder. As expected, after decreasing the amount of water molecules, there is evidence of higher damping factors. The propagating waves associated with collective density fluctuations have a trend toward shorter lifetime from whole living cells toward hydrated powders. We naturally assume a strong coupling between protein dynamics and hydration water and that the damping parameter has an important role in transferring density fluctuations from biological molecules to hydration water and vice versa. The presence in the water dynamics of collective modes belonging to the protein was demonstrated by a MD simulation study investigating the longitudinal and transverse modes propagating in the system.42 It was supposed that the protein surface strongly affects the damping because the structure of the hydration water around the biomolecules comes to be more disordered with respect to the bulk water and therefore the excitation modes are sustained in a different way.37,32 In all cases, the damping values are always higher than in bulk water, confirming that protein molecules are a perturbing agent of the aqueous solvent, capable of introducing novelties in the normally well-defined and ordered structure of water molecules and their hydrogen bond network. With this picture in mind, we establish that single-point mutation reveals somehow that collective density fluctuations, through the water network, might provide important insight on the transmission of information possibly correlated to biological functionality. To some extent we are tempted to say that collective modes can provide a measurement of a “functional dynamics”. In summary, this Letter investigates the role of intracellular water dynamics in the dynamics and activity of a well-defined class of proteins. We propose that photosynthetic wild-type cells require a relatively rigid environment to function under physiological conditions and that a larger flexibility that can be assumed by the mutant could be related to its ability to resist to
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpclett.6b00949. Methods and material details that describe the biological material, deuteration of Chlamydomonas algae, Brillouin neutron scattering experiment, and data analysis (PDF)
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AUTHOR INFORMATION
Corresponding Author
*E-mail:.
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS The authors thank A. Laloni for his technical assistance during the experiment on the BRISP instrument and N. Formisano for providing the instrument data reduction routines. The authors also thank COST Action TD1102 for financial support for the STMS in Grenoble (France) and Roma (Italy), and the Italian Space Agency for financial support for the project BIOKISPHOTOEVOLUTION. D.R. is grateful to Dr. J. Teixeira for useful discussion.
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