Solar energy conversion: From natural to artificial photosynthesis

https://doi.org/10.1016/j.jphotochemrev.2017.02.001Get rights and content

Highlights

  • This review summarizes the research trends of natural, semi-artificial and artificial photosynthesis in terms of concepts, design, and examples.

  • Biohydrogen production via photosynthesis and direct energy production, and production of hydrogen in natural systems in vivo.

  • Semi-artificial system in vitro and the ways of producing biohydrogen in semi-artificial devices.

  • Relations between structures and photoinduced reactivities of the reported artificial photosynthetic donor-acceptor systems are discussed in relation to the efficiency.

  • Photocatalytic production of hydrogen peroxide as a more promising solar fuel than hydrogen is discussed in relation with the natural photosynthesis.

Abstract

Solar energy has a great potential as a clean, cheap, renewable and sustainable energy source, but it must be captured and transformed into useful forms of energy as plants do. An especially attractive approach is to store solar energy in the form of chemical bonds as performed in natural photosynthesis. Therefore, there is a challenge in the last decades to construct semi-artificial and artificial photosynthetic systems, which are able to efficiently capture and convert solar energy and then store it in the form of chemical bonds of solar fuels such as hydrogen or hydrogen peroxide, while at the time producing oxygen from water. Here, we review the molecular level details of the natural photosynthesis, particularly the mechanism of light dependent reactions in oxygen evolving organisms, absorption efficiency of solar energy and direct energy production. We then demonstrate the concept and examples of the semi-artificial photosynthesis in vitro. Finally we demonstrate the artificial photosynthesis, which is composed of light harvesting and charge-separation units together with catalytic units of water oxidation and reduction as well as CO2 reduction. The reported photosynthetic molecular and supramolecular systems have been designed and examined in order to mimic functions of the antenna-reaction center of the natural process. The relations between structures and photochemical behaviors of these artificial photosynthetic systems are discussed in relation to the rates and efficiencies of charge-separation and charge-recombination processes by utilizing the laser flash photolysis technique, as well as other complementary techniques. Finally the photocatalytic production of hydrogen peroxide as a more promising solar fuel is discussed in relation with the natural photosynthesis, which also produces hydrogen peroxide in addition to NADPH.

Introduction

There is unprecedented interest in renewable energies that are collected from natural resources as alternative to fossil fuels [1], [2], [3], [4], [5], [6]. Among them, solar energy has an enormous potential as an abundant, cheap, clean and sustainable energy source [7], [8], but it cannot be employed as such, so it must be captured and transformed into useful forms of energy as plants do. An especially attractive approach in the recent years is to convert this solar energy to chemical bonds and store it in stable organic molecules as performed in natural photosynthetic process [9], [10], [11], [12]. Simply, natural photosynthesis is the process by which sunlight is absorbed, transferred and converted into the energy of chemical bonds of organic molecules that are used for building up the body of all living organisms [7], [8], [9], [10], [11], [12]. Compared to the total arriving solar energy to the earth surface (about 24 × 1020 kJ/year), the amount of absorbed energy is considered to be very limited (0.1%) [13], [14]. Beside the production of billion tons biomass per year, more than 10% of the total atmospheric CO2 are consumed and substituted by oxygen [13], [14].

The idea of using the basic science underlying photosynthesis in the design of solar fuels has been discussed for over 100 years ago by an Italian scientist, Giacomo Ciamician [15], in a famous lecture entitled “The photochemistry of the future”, when he stated: “Photochemistry will artificially put solar energy to practical uses. To do this, it would be sufficient to be able to imitate the assimilating processes of plants”. Nowadays Ciamician’s idea for production of ‘solar fuel’ from inexpensive and abundant material such as water that could be split into oxygen and hydrogen has attracted increasing attention [16], [17], [18], [19]. Hydrogen is often called a fuel of the future since its combustion generates water as the product. A highly attractive way for the light driven water splitting in newly designed devices would be to mimic the molecular and supramolecular organization and functions of the natural photosynthetic system, i.e., “artificial photosynthesis” [20], [21], [22], [23], [24], [25], [26], [27], [28], [29], [30], [31], [32], [33], [34], [35], [36], [37], [38], [39], [40], [41], [42], [43], [44], [45], [46], [47], [48], [49], [50], [51], [52], [53], [54], [55]. In the last decades, the artificial photosynthesis has been fascinating scientists in chemistry and biology[w1], who hope to construct efficient photosynthetic systems that are able to capture solar energy efficiently and then, convert and store it in the form of chemical bonds of solar fuels such as hydrogen and hydrogen peroxide, while at the time producing oxygen from water [16], [17], [18], [19].

This review summarizes the recent research trends of natural, semi-artificial and artificial photosynthesis in terms of concepts, design, and examples. We focus at the beginning on the molecular level details of the natural photosynthesis, particularly Photosystem I (PSI), Photosystem II (PSII), mechanism of light dependent reactions in oxygen evolving organisms, biohydrogen production via photosynthesis and direct energy production, and production of hydrogen in natural systems in vivo. In the second part, we describe the concept of the semi-artificial systems and the ways of producing biohydrogen in semi-artificial devices. At the third part, we demonstrate the concept of artificial photosynthesis and examples of the recently reported photosynthetic molecular and supramolecular systems, from our laboratories and others, in order to mimic functions of the antenna-reaction center of the natural process. The relations between structures and photoinduced reactivities of the reported artificial photosynthetic donor-acceptor systems are discussed in relation to the efficiency of the intramolecular electron-transfer/energy-transfer processes by utilizing the laser photolysis technique and other complementary techniques. Finally, the photocatalytic production of hydrogen peroxide as a more promising solar fuel than hydrogen is discussed in relation with the natural photosynthesis, which also produces hydrogen peroxide in addition to NADPH.

Section snippets

Natural photosynthesis

Photosynthesis is considered to be an essential biological process by which photosynthetic organisms convert solar energy into ATP and NADPH required for carbon dioxide fixation [56]. This process is achieved through two separate reactions: Light reactions (Light dependent reactions) and dark reactions (light independent reactions). In the light dependent reactions, photons are absorbed by antenna chlorophyll systems leading to excitation of special chlorophyll pair followed by water splitting

Hydrogenase-ferredoxin fusion

It is clear that ferredoxin NADP reductase (FNR) is physically bound to the thylakoid membrane in plant and algae and cyanobacteria, so the presence of membrane PSI bound FNR is the main factor inhibiting efficient electron transfer to soluble HydA, which consequently leads to lowering the hydrogen production rates [130], [158]. Fd-HydA fusion protein could functionally replace HydA [158]. The protein fusion strategy is a matured approach, being successfully applied to several electron donors

Semi-artificial system in vitro

Galvanic cells based on photosynthetic complexes have been designed since 1970 [162]. The charge separation processes in the natural photosystem (Z-scheme) have inspired the design of semi-artificial photosynthesis systems based on organic and inorganic photosensitizers to convert solar energy into chemical energy [162], [163]. So, exploiting the yield in light harvest by photosynthetic proteins may further increase the efficiency of solar to chemical energy conversion in semi-artificial

Artificial photosynthesis

As mentioned earlier, photosynthesis is one of the most effective solar energy conversion systems on earth, where the organisms harvest sunlight and convert it into useful electrochemical energy. In the marvelous artificial photosynthesis process, the antenna units harvest sunlight and the excitation energy is funneled to the reaction center where multistep electron-transfer reactions occur to generate potential that can drive chemical reactions to produce chemical energy that can be used and

Conclusion

Biohydrogen is considered the key of development and civilization, where it is one of the most effective solutions for double crisis (pollution and energy). Studies on natural, semi-artificial, and artificial systems introduced the possibility of continuous hydrogen production even in low rate. Two main factors affect the successful production of hydrogen during the photosynthetic process; the rate of electrons flow and the absence of molecular oxygen. The rate of electrons flow from PSI to

Acknowledgements

This project was supported financially by the Science and Technology Development Fund (STDF, Egypt, Grant Nos. 5537 and 12436). S. Fukuzumi thanks JSPS KAKENHI (Grant no. 16H02268). S. Fukuzumi and M. E. El-Khouly would like to acknowledge Francis D’souza for a long term and fruitful collaboration. E. El-Mohsnawy also acknowledges M. Rögner for the long-term collaboration.

Mohamed E. El-Khouly was born in Egypt and earned his PhD degree in photochemistry from Tohoku University, Japan (2002). After that, he continued his research in Japan funded from Venture Business Laboratory (2003–2004), Center of Excellence (2004–2006), and Japan Society for the Promotion Science (2006–2008). In the period of 2008–2012, he joined the research group of Prof. Shunichi Fukuzumi at Osaka University as a specially appointed Associate Professor. Sine 2013, he has been a Full

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    Mohamed E. El-Khouly was born in Egypt and earned his PhD degree in photochemistry from Tohoku University, Japan (2002). After that, he continued his research in Japan funded from Venture Business Laboratory (2003–2004), Center of Excellence (2004–2006), and Japan Society for the Promotion Science (2006–2008). In the period of 2008–2012, he joined the research group of Prof. Shunichi Fukuzumi at Osaka University as a specially appointed Associate Professor. Sine 2013, he has been a Full Professor at Kafrelsheikh University. His research interests are mainly focused on ultrafast laser photolysis of the molecular and supramolecular light harvesting systems, carbon nanostructures, artificial photosynthesis complexes, material science, and laser chemistry.

    Eithar El-Mohsnawy was born in Egypt and received his PhD degree in the Algal Biotechnology from Faculty of Biology and Biotechnology, Ruhr-University Bochum, Germany (2007). He was hired as a Lecturer at Suez Canal University, Egypt on 2007. Since 2014, he moved to Kafrelsheikh University as an Associate Professor. His research interests involved photosystem 1 structure and function, photosynthetic electron transport chain, native and semi-artificial photosynthesis, and biohydrogen production.

    Shunichi Fukuzumi earned a bachelor’s degree and PhD degree in applied chemistry at Tokyo Institute of Technology in 1973 and 1978, respectively. After working as a postdoctoral fellow (1978–1981) at Indiana University in USA, he joined the Department of Applied Chemistry, Osaka University, as an Assistant Professor in 1981 and was promoted to a Full Professor in 1994. His research interests are artificial photosynthesis and electron transfer chemistry. He was the leader of an ALCA (Advanced Low Carbon Technology Research and Development) project that started in 2011. He is now a Distinguished Professor of Ewha Womans University, a Designated Professor of Meijo University, a Professor Emeritus of Osaka University.

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