perspective of energy transfer from light energy into biological energy

+ MODEL Available online at www.sciencedirect.com ScienceDirect Green Energy & Environment xx (2017) 1e5 www.keaipublishing.com/gee Feature article Perspective of energy transfer from light energy into biological energy Mingjun Xuan a, Jie Zhao a, Jingxin Shao a, Qi Li a,b, Junbai Li a,b,* a Beijing National Laboratory for Molecular Sciences (BNLMS), CAS Key Lab of Colloid, Interface and Chemical Thermodynamics, Institute of Chemistry, Chinese Academy of Sciences, China b University of Chinese Academy of Sciences, China Received 10 November 2016; revised 16 November 2016; accepted 16 November 2016 Available online ▪ ▪ ▪ Abstract Energy has always been the most concerned topic in the world due to the large consumption Various types of energy have been exploited and developed to enhance the output amount so that high requirements can be met Like the hydro-energy, wind energy, and tidal energy, light energy as a renewable, clean, and widespread energy can be easily harvested In microcosmic scale, some specific proteins and enzymes in green plants and bacteria play an important role in light harvest and energy conversion via photosynthesis Inspired by the biomimetic sparks, these bioactive macromolecules and some artificially synthetic unites have been integrated together to improve the light-harvesting, and enhance their utilization efficiency In this feature article, we primarily discuss that how to create the bio-inorganic hybrid energy converted system via biomimetic assembly strategy and artificially achieve the transformation from light into bioenergy, meanwhile highlight some promising works © 2016, Institute of Process Engineering, Chinese Academy of Sciences Publishing services by Elsevier B.V on behalf of KeAi Communications Co., Ltd This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/) Keywords: Biomimetic; Molecular assembly; Energy conversion; Light; Bioenergy Introduction The sunlight as a green energy provides us with an inexhaustible power source, and interestingly inspired the design of light-responsive materials and the newly sustainable energy strategy [1,2] For a long time, many efforts have been devoted to transfer light energy artificially into biological energy, further convert to electronic power or mechanical works for the creation of new-type energy sources [3,4] This challenge has been currently appeared and faced to all the researchers coming from interdisciplinary sciences Photophosphorylation is a classic prototype of light-to-bioenergy converter in chloroplast [5] During this complex process, photosystem II (PSII) protein in chloroplasts can catalyze the oxidation of * Corresponding author Beijing National Laboratory for Molecular Sciences (BNLMS), CAS Key Lab of Colloid, Interface and Chemical Thermodynamics, Institute of Chemistry, Chinese Academy of Sciences, China E-mail address: jbli@iccas.ac.cn (J Li) water, resulting in the generation of four protons, four electrons, and dioxygen in the aerobic condition [6e8] These provided products can be directly utilized and enable the next energy conversion feasible as mechanical works, heat, and electronic energy, significantly providing the inspiration for the design of newly developed energetic materials and their applications [9e11] Recently, substantial research works report that some artificially synthetic unites and biologically active components can be integrated together to assembly the biomimetic structures for the enhanced light harvest and further energy conversion It shows that there will be a great potential in application [12e15] Unlike the traditional light mediated devices, the natural chloroplasts exhibit strong preponderance in the light absorption and energetic transduction [16,17] The natural components from biological entities also have glorious biocompatibility and high-efficiency biocatalytic property, significantly inspired the preparation of biohybrid materials Some life-like light-mediated hybrid systems can be http://dx.doi.org/10.1016/j.gee.2016.11.005 2468-0257/© 2016, Institute of Process Engineering, Chinese Academy of Sciences Publishing services by Elsevier B.V on behalf of KeAi Communications Co., Ltd This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/) Please cite this article in press as: M Xuan, et al., Perspective of energy transfer from light energy into biological energy, Green Energy & Environment (2017), http://dx.doi.org/10.1016/j.gee.2016.11.005 + MODEL M Xuan et al / Green Energy & Environment xx (2017) 1e5 constructed via introducing PSII proteins to perform the mimicking of chloroplasts for the generation of biological energy upon the light illumination [18] To convert other types of energy from light, some special assembled elements have been employed, such as cytochrome oxidase, bacteriorhodopsin, and ATP synthase (ATPase) ATPase is a membraneassociated protein and widely exists in thylakoid membrane, which is responsible for the regulation of proton concentration [19,20] The mechanical rotation of ATPase for ATP synthesis can be triggered in the presence of proton gradient Inspired from this, several biohybrid systems in vitro have been assembled according to the actual benefit, and furthermore one can consider the construction of light-to-bioenergy converted device Here, we mainly talk about the perspective of energy transfer from light energy into biological energy Bionic assembly of molecules has been proved as a bright strategy to construct functional structure Some artificially synthetic unites and light-responsively bioactive macromolecules can be hybridized to form the light-to-bioenergy converted systems This approach provides us with a novel assembled strategy for the construction of biomimetic devices, significantly demonstrate that how to enhance the energy utilization efficiency from light energy in microcosmic scale Calvin cycle, light reaction occurs in the thylakoid, and carries out the biocatalytical photolysis of water to generate the oxygen and proton through the photosystems The generated adenosine triphosphate (ATP) and NADPH can be utilized directly by the Calvin cycle As compared with other organelles, chloroplast is the self-feeder that can make the consuming food for its own The thylakoid membrane contains two classes of light-responsive proteins, photosystem I (PSI) and photosystem II (PSII) (Fig 1c), which are in charge of the electron transfer and light-to-bioenergy transformation [25] The water is split via the light mediated catalysis of PSII The generated protons are encapsulated in the chamber of the thylakoids, and used to trigger the rotation of ATPase to synthesis ATP [26] Thus, the light are transformed into the biological energy, further provide the possibility to the conversion of mechanical work and electric energy The photosystem of chloroplast as the one of most intelligent system made by nature, the researchers spend many efforts to investigate their working mechanism and introduce this inspiration to optimize the currently man-made light-toenergy converted devices Such a bionic strategy offers the astounding and great potential to improve the efficiency of light harvest and further energy transformation, importantly pave a way to settle the mass utilization of fossil fuels Assembled systems for the transformation from light into bioenergy 2.2 In vitro assembly of artificial light-to-bioenergy converted devices 2.1 The conversion in nature from light to bioenergy To simulate the natural photosynthesis, many efforts have been devoted by the interdisciplinary scientists to perform the separation of photosystem components from green plants and photosynthetic bacteria, such as PSI, PSII, ATPase, bacteriorhodopsin (BR), and deltarhodopsin (dR) [27e31] However, how to integrate these biological unites with the synthesis devices to reconstruct a biomimetic platform that it is still a challenge Molecular assembly of bionic inspired a new strategy to conjugate these light-responsive unites with the introduced components, subsequently achieve the hybridization of naturally biological macromolecules and their applications in vitro As compared to the purely synthetic platforms, natural active components as assembled materials represent strong functionality and well biocompatibility [32e36] Recent studies of natural biological hybrid with express pronounced performance at the energy conversion, especially light energy transform into the biological energy [37] The introduced naturally assembled parts can significantly enhance the light harvest mass and further transferred efficiency, simultaneously achieve the desired “on/off” conversion by the open/close light source Thus, the scientists pay more attention on the development of the light-driven bioenergy synthesis To assemble converted platform from light to bioenergy, several light-responsive unites have been introduced to reconstitute biomimetic devices Moore and coworkers prepared a light-driven photosynthetic membrane for the ATP synthesis This artificial membrane contains ATPase protein incorporated liposomal bilayer and proton-pumping Photosynthesis is a fantastically physiological-biochemical process in the chloroplasts contented green plants and bacteria [21] The solar light can be harvested during this process, and then is converted to the biological energy Most of the nature systems alive in this way to obtain energy, which guarantees the power source requirement a continuous supplying for the organelles using in cellular level Chloroplasts are the photosynthesizing organelles, and are much more efficient than any power systems made by human beings As a power generated organelle that chloroplast performs a series of biochemical reaction and energy conversion Many grana are organized together and encapsulated by the inner and outer membrane (Fig 1a) to enhance the surface area to trap much more sun light Several thylakoids are packed to form the stack-like structure (Fig 1b), granum, which block plenty of the green chlorophyll molecules in the sacs as the solar power packs The granum can be connected to the adjacent grana and immobilized to keep stable by the stroma lamellae This smart skeleton can keep the all the sacs with a moderate distance and avoid overlapping and bunched together, which maximize the efficiency of chloroplasts to trap sun light [22] Overview the complex process of photosynthesis, it can be divided into two stages, Calvin cycle and light reactions [23] The carbon fixation occurs in the stroma of chloroplast accompany with energy consuming, which contain series cycles of many sugar molecules assembly by using carbon dioxide and productions of light reactions [24] Unlike the Please cite this article in press as: M Xuan, et al., Perspective of energy transfer from light energy into biological energy, Green Energy & Environment (2017), http://dx.doi.org/10.1016/j.gee.2016.11.005 + MODEL M Xuan et al / Green Energy & Environment xx (2017) 1e5 Fig Chloroplasts and photosynthesis system in green plants: The structure pictures of (a) chloroplast and (b) thylakoid (c) Thylakoid membrane and the corresponding light-responsive mechanism photocycle system made of porphyrinenaphthoquinone molecular triad (1, C-P-Q) and lipophilic quinone (Qs) [38] Upon the excitation of visible light, photon-induced electron transfer and proton delivery into the chamber of liposomes can be achieved by the cooperation of C-P-Q and Qs, resulting in the proton gradient for the ATP synthesis As Fig 2a shown that a photoactive protein, BR, is incorporated into the ATPase modified polymersomes for the formation of light-driven ATP synthesis system BR as the energy-transducing protein sever as a proton channel that the crossing stream of protons into the polymersomes can be controlled by the light switch on/off [39] The increase concentration of proton in the polymersomes causes the proton gradient, and triggers the rotation of the ATPase enzyme to synthesis ATP To improve the conversion efficiency from light to bioenergy, an artificial frame works of photosynthesis was reconstituted that photophosphorylation unite are concentrated into bioactive architecture of the Tu´ngara frog surfactant protein Ranaspumin-2 (Fig 2b) This photophosphorylation unite as the light-responsive component is made of lipid vesicles with the incorporation of ATPase and BR In the presence of sunlight, the light energy can be directly converted into the biological energy Due to the concentrated integration of foam channel, the photonderived conversion of biological energy from light is significantly improved [40] The bionic assembly inspires biomimetic sparks of photosynthetic organelle An artificially assembled chloroplast is made of ATPase proteoliposome-coated PSII particles, which is prepared by the Li's group [41] This hybrid system can effectively maintain bioactivity of these biological macromolecules, and achieve the in vitro ATP synthesis by using the light The assemble strategy can also be used for the bionic construction of mitochondria As Fig 2c shown that a hybrid photosynthetic-respiratory chain is present, which is made of polymersome membrane contain ruthenium(II)-terpyridine linked cytochrome c (Ru-cytc) and cytochrome c oxidase [42] Similar as the ATPase, cytochrome c oxidase is also a pump protein, which can translocate the proton across the biological membrane Upon light accompany with pH ¼ 7.2 in solution, the photon is harvested by Ru-cytc receptor and subsequently transferred to the cytochrome c oxidase for the formation of water and proton generation During this process, a proton gradient is formed across the polymer membrane and enable cytochrome c oxidase pump proton to outside Thus, this hybrid system not only can generate the proton for light-to-chemical energy conversion, but also simulate a model artificial protocell In addition, the scientists can use other smart biological pumps to perform the light harvesting, and perform the promising application As Fig 2d shown that the bacterial efflux pump AcrB can be coupled with a light-driven proton pump, Deltarhodopsin (dR), via the glycophorin A transmembrane domain in the proteovesicle system [43] Using this AcrB-dR vesicle, the antibiotics in the water can be effectively removed as twice as the active carbon, demonstrating a great potential in bioremediation of surface waters Please cite this article in press as: M Xuan, et al., Perspective of energy transfer from light energy into biological energy, Green Energy & Environment (2017), http://dx.doi.org/10.1016/j.gee.2016.11.005 + MODEL M Xuan et al / Green Energy & Environment xx (2017) 1e5 Fig Assembled strategies for the reconstruction of light-driven proton pump and performing in vitro ATP synthesis (a) BR protein and ATPase enzyme incorporated polymersome as the artificial organelle for light-driven ATP synthesis Copyright (2005), American Chemical Society (b) The foam proton concentrated light-to-bioenergy converted platform Copyright (2010), American Chemical Society (c) Artificially assembled light-driven pump for the generation of chemical energy Copyright (2013), Royal Society of Chemistry (d) The AcrB-dR vesicle for the light mediated bioremediation of surface waters Copyright (2013), American Chemical Society Conclusion We have summarized the perspective of energy transfer from light energy by the artificial design into biological energy Solar light is an inexhaustible power with the renewable property, which inspires the generation of series of devices to achieve light harvest and utilization Comparing with the traditional solar cells, we found that the green plants and photosynthetic bacteria exhibit elegant performance in trapping light and further conversion to other type of energy These light-responsive biological unites such as PSII, BR, cytochrome c oxidase, and dR are specially separated and integrated with synthetic agents to constitute the hybrid systems In the presence of light, these reconstituted platforms can generate a proton gradient to trigger the work of some biomacromolecules, resulting in the energy conversion from light to bioenergy by using the proton motion force [44e47] Thus, bioactive macromolecules mediated light-to-bioenergy conversion sparks a novel strategy for light transfer to bioenergy However, we have to point out that these naturally biological components in current hybrid systems have obvious weaknesses The main problem is the quantum efficiency of the energy transfer This might be due to the stability of bioactivity in vitro, and the capability to persistent working for a long time The cooperated mechanism between synthetic materials and energy-linked biological ligands that need to be deeply investigated, extremely present the high-efficiency on the energy transformation In addition, the current type of Please cite this article in press as: M Xuan, et al., Perspective of energy transfer from light energy into biological energy, Green Energy & Environment (2017), http://dx.doi.org/10.1016/j.gee.2016.11.005 + MODEL M Xuan et al / Green Energy & Environment xx (2017) 1e5 energy-linked enzyme or protein is less so that leads to inevitable limitation in selection for matching the synthetic materials Therefore, many efforts are still devoted to improve the performance of these bio-inorganic hybrid systems, explore and introduce more other proteins or enzymes to the light-tobioenergy converted platforms Conflict of interest The authors declare no competing financial interest Acknowledgement This project was finically supported by the National Natural Science Foundation of China (Nos 21303219, 21433010, 21320102004, and 21273250) and the National Basic Research Program of China (973 program, No 2013CB932802) 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http://dx.doi.org/10.1016/j.gee.2016.11.005 ... the construction of light- to-bioenergy converted device Here, we mainly talk about the perspective of energy transfer from light energy into biological energy Bionic assembly of molecules has... al., Perspective of energy transfer from light energy into biological energy, Green Energy & Environment (2017), http://dx.doi.org/10.1016/j.gee.2016.11.005 + MODEL M Xuan et al / Green Energy. .. potential in bioremediation of surface waters Please cite this article in press as: M Xuan, et al., Perspective of energy transfer from light energy into biological energy, Green Energy & Environment