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The Mechanism, Progress and Prospect of Biohybrid Mediated Semi-Artificial Photosynthesis

Andong Hu , Shungui Zhou , Jie Ye

Progress in Chemistry ›› 2021, Vol. 33 ›› Issue (11) : 2103 -2115.

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Progress in Chemistry ›› 2021, Vol. 33 ›› Issue (11) : 2103-2115 DOI: 10.7536/PC200877
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The Mechanism, Progress and Prospect of Biohybrid Mediated Semi-Artificial Photosynthesis
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Abstract

Semi-artificial photosynthetic system could realize the solar-to-chemical energy conversion by utilizing the synergistic effects of key functional components of artificial and natural photosynthetic systems. The biohybrid mediated semi-artificial photosynthetic system(BMSAPS) can effectively trigger the specific solar-to-chemical conversion due to the excellent light-harvesting properties of photosensitizers and highly-efficient biological catalytic abilities of biocatalysts. Enhancing the photoelectron generation, transfer and utilization on the micro-interface of photosensitizer-biocatalyst hybrids is considered to be crucial for improving the performance of BMSAPS. This review innovatively concludes the key scientific issues and research status on the BMSAPS construction based on its constituent elements. Meanwhile, the relevant mechanisms and research methods for the photogenerated electron transport in the BMSAPS are also described. In addition, the research progress of the BMSAPS on different fields such as the renewable energy conversion and CO2 emission reduction are summarized, followed by the future research directions. This review is expected to deepen the understanding of the BMSAPS, thereby providing the theoretical foundation and technical support for further optimizing its application in the field of energy production and environmental restoration.

Contents

1 Introduction

2 The basic principles of BMSAPS

3 The BMSAPS construction

3.1 Photosensitizers

3.2 Biocatalysts

4 The typical BMSAPS

4.1 Photoelectrode-biohybrid system

4.2 Inorganic semiconductor-biohybrid system

4.3 Plasmon-biohybrid system

4.4 Research methods for typical biohybrid system

5 The BMSAPS application

5.1 Carbon dioxide fixation

5.2 Nitrogen fixation

5.3 Hydrogen production

6 Outlook

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Keywords

semi-artificial photosynthesis / electron transport / photosensitizers / biocatalysts

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Andong Hu, Shungui Zhou, Jie Ye. The Mechanism, Progress and Prospect of Biohybrid Mediated Semi-Artificial Photosynthesis. Progress in Chemistry, 2021, 33(11): 2103-2115 DOI:10.7536/PC200877

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1 Introduction

In order to cope with the dual challenges of energy shortage and environmental protection, the search for natural renewable energy has attracted widespread attention[1]. Solar energy, as an abundant, cheap and clean renewable energy, has great application potential. Therefore, the effective collection and utilization of solar energy is one of the important ways to solve the global energy and environmental problems[2]. Natural photosynthesis provides a perfect example for human beings to use solar energy efficiently. It is not only the material and energy source for human survival, but also an important way to maintain the balance of carbon and oxygen in the atmosphere. In general, natural photosynthesis is able to use chlorophyll to convert solar energy into adenosine triphosphate (ATP) and nicotinamide adenine dinucleotide phosphate (NADPH) for energy storage to drive water splitting for oxygen production and carbohydrate synthesis. However, the natural photosynthetic system has some shortcomings, such as narrow spectral absorption range, low light harvesting and conversion efficiency (1% ~ 2%) and complex self-assembly system[3].
Inspired by natural photosynthesis, researchers have proposed an artificial photosynthetic system that converts solar energy into chemical energy[4]. The basic principle of the system is that the photosensitizer is used to capture solar energy efficiently and drive the separation and transfer of photogenerated electrons and holes, thus realizing multi-electron catalytic water splitting and carbon dioxide (CO2) fixation. At present, there are three kinds of artificial photosynthetic systems reported: photocatalysis, photoelectrolysis and photovoltaic electrolysis[5,6][7][8]. Artificial photosynthetic system can effectively overcome the shortcomings of natural photosynthetic system, such as low efficiency of light harvesting and conversion[9⇓⇓~12]. For example, some researchers have chemically synthesized inorganic semiconductor heterostructure materials similar to leaves, namely "artificial nano-leaf structure". The novel nano material has strong light harvesting property and excellent electron-hole pair separation efficiency, and is effectively applied to the fields of photocatalytic hydrogen production, artificial nitrogen fixation and the like[13,14][15]. At present, "artificial nano-leaves" used for photocatalytic hydrogen production include Te/SnS2/Ag, TiO2/ZnTe/Au, perovskite /BiVO4 and so on[13][14][16]. The "artificial nano-leaves" used for artificial nitrogen fixation include VO-BiOBr, Bi2MoO6/OV-BiOBr, H-Bi2MoO6, etc[17][18][19]. In particular to a Bi2MoO6/OV-BiOBr material, and the nitrogen fixation and ammonia production rate of the material can reach 90.7μmol·g-1·h-1 under the environment of normal temperature and normal pressure. Secondly, it has been reported that the solar energy conversion efficiency can reach 6.5% by using tandem photovoltaic perovskite and high-performance electrocatalyst for CO2 reduction[20]. In addition, the conversion efficiency of solar hydrogen production by photovoltaic electrolysis system can reach 12.3%[21].
However, it should be pointed out that although artificial photosynthetic systems have good light harvesting performance and show high solar energy conversion efficiency, their shortcomings in product selectivity, specificity and system stability still limit their large-scale application[22]. In order to solve this technical bottleneck, researchers have innovatively proposed a semi-artificial photosynthetic system based on photosensitizers and unique macromolecular enzymes or microorganisms, namely biohybrid mediated semi-artificial photosynthetic system (BMSAPS)[23,24]. The system has attracted much attention because it integrates the excellent light harvesting performance of photosensitizers and the bio-efficient catalytic ability, and has dual advantages in the capture and utilization of solar energy[25].
In this paper, the basic principles of BMSAPS are introduced, and the key scientific issues for the construction of BMSAPS are reviewed.Representative photosensitizers and biocatalysts are summarized, and the electron transfer mechanism and research status of typical BMSAPSs are expounded.In addition, the applications of this system in renewable energy conversion and carbon dioxide emission reduction are summarized.In addition, the future research directions of BMSAPSs are proposed.

2 Fundamentals of BMSAPS

The basic principle of BMSAPS is that under the illumination of a specific wavelength, when the photon energy absorbed by the photosensitizer in the biohybrid system is equal to or higher than the forbidden band width, the electrons (e-) in the valence band are excited to jump to the conduction band.The photogenerated electrons can be transferred to the active site of the biocatalyst through direct transfer, redox mediator and hydrogen/formic acid mediation, and then drive the energy metabolism of organisms. Taking water splitting and hydrogen production driven by biological hybrid system as an example, cadmium sulfide photosensitizer (CdS) was loaded on the surface of Escherichia coli (E. coli) in situ, and under visible light irradiation, the electrons generated by CdS excited by light could be transferred to the [Ni-Fe] -hydrogenase reaction center of E. coli, thus driving E. coli to split water and produce hydrogen[26].
The research of BMSAPS is a frontier research that integrates materials, chemistry, biology and other disciplines, and its core task is to improve the energy conversion efficiency and product selectivity of photosynthetic system[27]. At present, BMSAPS is mainly used in water splitting, CO2 reduction, hydrogen production and nitrogen fixation[28⇓~30][25,31][23,32][33]. In these studies, the light harvesting materials used are mainly inorganic semiconductors, such as CdS, titanium dioxide (TiO2), indium phosphide (InP) and so on[24,34][35][28]. Although inorganic semiconductors can achieve a wide range of solar absorption, these materials generally have some shortcomings, such as low electron separation efficiency caused by the easy recombination of electrons and holes, heavy metal toxicity and strong photocorrosiveness, which restrict their application in BMSAPS. In addition, organisms involved in BMSAPS need to capture electrons through different electron transport pathways to drive physiological metabolism and energy conversion. However, the energy loss in the process of electron transfer and the competition of other electron acceptors will reduce the efficiency of electron transfer and electron capture in organisms. Therefore, how to improve the "excitation-transition-capture-utilization" of photogenerated electrons is a key scientific issue for the construction of high-performance BMSAPS.

3 BMSAPS Build

In recent years, semi-artificial photosynthetic system has been widely used in the field of energy production and environmental remediation, and how to construct efficient BMSAPS has become the core of research[36]. The system contains two key elements: photosensitizer and biocatalyst, both of which are indispensable. Table 1 lists common BMSAPS. Among them, the photosensitizer acts as a light harvesting platform to generate photogenerated electrons and holes under specific illumination radiation. Photogenerated electrons have strong reduction ability, while holes have strong oxidation ability, which can be separated and migrated on the surface of photosensitizer, and then combined with biocatalyst or cocatalyst to achieve redox reaction (Fig. 1)[37]. Furthermore, as a platform for light-chemical energy conversion, organisms can use photogenerated electrons to fix CO2, H2O, H2 and so on, which exist in nature, so as to convert these inorganic substances into organic compounds[22]. In addition, organisms can self-repair and replicate, thus ensuring the efficient cycle of inorganic-organic metabolism and transformation of organisms[38]. Therefore, photosensitizers and biocatalysts are the core components of BMSAPS.

3.1 Photosensitizer

Photosensitizer, also known as photocatalyst, is a general term for semiconductor materials with photocatalytic function. Photosensitizer determines the light absorption efficiency of BMSAPS, and its biocompatibility is also an important basis for the construction of BMSAPS[51]. Fig. 2 lists images of some photosensitizers with good biocompatibility binding to organisms. At present, photosensitizers in BMSAPS can be divided into inorganic semiconductors and organic semiconductors.
The band structure of inorganic semiconductors is mainly composed of three parts: valence band (VB), band gap and conduction band (CB). Fig. 3 lists the bandgap widths of some semiconductors currently used in BMSAPS. The most representative one is CdS, which has a band gap of 2. 4 eV at room temperature and good visible light response characteristics, and the appropriate band structure can meet the requirements of CO2 reduction and water photolysis. In addition, the simple preparation of CdS and its ability to bind tightly to organisms through in situ precipitation provide a powerful basis for the construction of BMSAPS[45,55,56]. Therefore, in recent years, there have been many reports on the construction of BMSAPS using CdS as a photosensitizer[57⇓~59]. However, the separation efficiency of photoexcited electrons and holes in inorganic semiconductors is low, and their photochemical properties are difficult to control. In addition, heavy metals in semiconductors are toxic to organisms. These factors limit their large-scale application[25].
Organic semiconductor photosensitizer has become an important photosensitizer for the construction of BMSAPS because of its adjustable optical band gap, good biocompatibility, efficient extracellular electron transport capacity and low biological toxicity[60][61][62]. In recent years, organic semiconductor photosensitive materials reported mainly include organic dyes (eosin Y, methyl blue), photosensitive proteins (green fluorescent protein, phycoerythrin), organic conjugated semiconductors (perylene diimide derivatives (PDI) and Polyfluorene phenylene (PFP)) and so on[63⇓~65][66⇓~68][53]. These organic semiconductors are directly combined with organisms to construct BMSAPS through synthesis, transformation, polymerization and surface modification. However, the preparation process of these materials is difficult and complex, and they can not be directly synthesized in situ in organisms. Therefore, the development of efficient, cheap and green photosensitizers is still an important research direction to further improve the biological hybrid system in the future.

3.2 Biocatalyst

The artificial photosynthesis system composed of a single photosensitizer requires high thermodynamic and kinetic energy in the process of using solar energy for chemical conversion, and the product selectivity is poor, thus limiting the popularization and application of this technology[69]. In order to solve this technical problem, researchers have introduced biocatalysts to construct BMSAPS, which can effectively regulate the transfer of photogenerated electrons and protons on the active site of photosensitizers, reduce the energy threshold of the reaction, and thus promote the photochemical reaction[70]. In addition, biocatalysts usually contain complete gene coding sequences (such as nitrogenase gene, hydrogenase gene and acetyl coenzyme gene) to promote related reactions, and have self-repair and replication capabilities.Therefore, BMSAPS constructed by photosensitizer-biocatalyst can not only stabilize the intermediate products, but also regulate the selective catalysis of photochemical reactions, thus promoting the formation of specific products[59][35][47]. Therefore, biocatalysts have broad application prospects[71⇓~73]. Common biocatalysts include the following two. (1) Macromolecular enzymes: carbon monoxide dehydrogenase (CODH, active site [Ni4Fe-4S]), nitrogenase (active site MoFeP), hydrogenase (active site [NiFeSe]), and photosynthetic membrane protein (active site WO3) (fig. 4). (2) Microorganisms: Moorella thermoacetica (M. thermoacetica), Escherichia coli (E. coli), Methanosarcina (M. barkeri), and Rhodopseudomonas palustris (R. palustris), etc. (Fig. 2). In the hybrid system, the biocatalyst showed highly efficient catalytic performance with a quantum efficiency of 5.8%[41]. In addition, selective product synthesis (e.g., acetic acid, hydrogen, methane, methanol, etc.) Can be achieved using different biocatalysts. Therefore, biocatalysts (microorganisms and macromolecular enzymes) play an important role in semi-artificial photosynthetic systems.
The core problem of matching between photosensitizer and biocatalyst is their compatibility, which is mainly based on the effective binding between the active site of photosensitizer and the outer membrane of biocatalyst, which has a vital impact on the generation, capture and utilization of photogenerated electrons in BMSAPS[75]. Usually, the outer membrane of biocatalyst contains a large number of special functional groups such as hydroxyl and ether, which can effectively combine with metal ions, which provides an opportunity for the in-situ synthesis of nano-metal semiconductors[76]. For example, M. thermoacetica can adsorb M. thermoacetica on the surface of cell membrane and synthesize CdS nanoparticles in situ under the condition of appropriate sulfur source, thus realizing the direct contact between photosensitizer and biocatalyst[24]. In addition, some researchers first chemically synthesize photosensitizers with good biocompatibility, and then combine them with biocatalysts to achieve a good match between photosensitizers and biocatalysts. For example, Gai et al. Have effectively synthesized PDI/PFP organic heterojunction photosensitizers[53]. Because the pi-conjugated molecules contained in the photosensitizer can be effectively embedded into the cell membrane of the M. thermoacetica, the effective transmission of photogenerated electrons is ensured.
However, it can not be ignored that photosensitizers with good biocompatibility in BMSAPS generate photogenerated electrons accompanied by the generation of radicals such as reactive oxygen species (ROS) and reactive nitrogen species (RNS)[25]. These substances have strong oxidizing properties and can directly act on the biocatalyst in close contact with the photosensitizer, causing its outer membrane to shrink or even break, thus seriously affecting the activity of the biocatalyst[24,77]. In addition, the commonly used metal photocatalysts are easy to dissolve metal ions due to photocorrosion, and these metal ions may have toxic effects on biocatalysts, resulting in the decline of the activity of biocatalysts, and ultimately affect the stability of BMSAPS. In order to maintain the stability of BMSAPS, researchers have carried out a lot of research work, including the use of Fe (Ⅲ) -TA-MOC encapsulation, metal-organic framework (MOF) encapsulation, biomimetic ZIF-8 encapsulation and polydopamine/laccase encapsulation[78,79][80][81][82]. In addition, in order to overcome the instability of the system caused by the toxicity of metal ions to microorganisms, some researchers have introduced biocompatible gold nanoclusters (AuNCs) into microbial cells, which not only have efficient light harvesting ability, but also can be used as ROS inhibitors to effectively maintain the stability of the system[31].

4 Typical BMSAPS

Improving the solar energy conversion efficiency of photosynthetic systems is one of the key objectives for building efficient BMSAPSs. Therefore, the transmission and transformation of photogenerated electrons at the inorganic-biological micro-interface is a key scientific issue to improve the efficiency of solar energy conversion. At present, typical BMSAPS mainly include photoelectrode-organism, semiconductor-organism and plasmon-organism hybrid systems. Therefore, it is particularly important to study the photoelectron transport mechanism of these three BMSAPS.

4.1 Photoelectrode-biological hybrid system

In Photoelectrochemical systems, semiconductors are usually used as photoanodes or photocathodes (such as TiO2, NiO, BiFeO3, etc.) To construct photoelectrode-biological hybrid systems by combining with organisms (macromolecular enzymes, microorganisms)[83⇓~85]. The basic principle of this system is that the electrode is excited by sunlight to produce photogenerated electrons, which are then transferred to the organism attached to the electrode to drive the organism to carry out functional metabolism and material synthesis. Compared with the traditional photovoltaic cells, the system can simultaneously carry out operations such as electrode modification, organism gene regulation, enzyme expression regulation and the like, so that the system is more selective and controllable. The system can be divided into photoelectrode-enzyme and photoelectrode-microbe hybrid systems.
The photoelectrode-enzyme hybrid system uses a photoelectrode as an electron donor to drive a biological enzyme to carry out energy metabolism reaction. Among them, biological enzymes usually have electron transfer groups, such as heme, quinone and [Fe-S] clusters, which can be used to transfer electrons between reactive sites and redox mediators to achieve Photoelectrochemical conversion and generate target products[69]. At present, researchers have done a lot of work on how to rapidly improve the electron transfer rate between the enzyme catalytic reaction center and the electrode surface. Among them, Bachmeier combined CODH with a dye-sensitized p-type semiconductor NiO (p-NiO) photoelectrode to drive CO2 reduction[83]. Under visible light, the electrons generated by the p-NiO photoelectrode of this system are transferred to the [Ni4Fe-4S] active site on CODH, and then the CO2 is selectively reduced to CO through the proton-coupled two-electron reaction (Figure 5A). In addition, Sokol et al. Integrated dye-sensitized TiO2 with photosystem II (PSII) as a photoanode to achieve full-spectrum solar absorption, which was used to drive cathodic hydrogenase to reduce protons[84]. The redox polymer (diketopyrrole) was used in the reaction system to effectively overcome the limitation of low interfacial electron transfer efficiency and promote the effective electron transfer between PS II and diketopyrrole. In order to further enhance the catalytic efficiency of the photoelectrode and the biological enzyme system and realize the selective generation of the target product, Park et al. Designed an integrated three-stage enzyme-linked (TPIEC) system in series with a Photoelectrochemical cell[85]. Under visible light irradiation, the electrons excited by the photoanode (Co-Pi/α-Fe2O3) are transferred to the photocathode (BiFeO3), and then through the rhodium-based medium NAD+, the NAD+ to NADH cycle regeneration is realized, and finally NADH transfers the electrons to the tertiary enzyme union (formate dehydrogenase-formaldehyde dehydrogenase-alcohol dehydrogenase), which efficiently drives the bioselective synthesis of methanol at a rate up to 1280μmol·g-1·h-1 (Figure 5 B). To sum up, the hybrid system based on photoelectrode-enzyme can realize the conversion of light energy to chemical energy, and the efficiency of electron transfer can be improved by enzyme modification, addition of electron transfer medium and series connection, so as to enhance the efficiency of photocatalytic conversion. However, in vitro, enzymes have stringent environmental requirements (such as appropriate pH, temperature and oxygen partial pressure) and can not replicate themselves, which limits the large-scale application of photoelectrode-enzyme hybrid systems.
In order to overcome the limitations of electrode-enzyme hybrid system, electrode and microbial hybrid system came into being. The basic principle of the electrode-microorganism hybrid system is as follows: photoexcitation drives the electrode to generate photogenerated electrons, and microorganisms capture the photogenerated electrons and use them in their own redox metabolic reactions to achieve selective product generation. For example, Lu Anhuai et al. constructed an electrode-microorganism hybrid system with A. ferrooxdans, ZnS, and FeOOH as anodes and Acidithiobacillus ferrooxidans (A. ferrooxdans) as cathodes[44]. The results showed that the photogenerated electrons generated by the photoanode under light excitation could be transferred to the cathode through the external circuit, which was used to reduce A. ferrooxdans to Fe2+ for the growth and metabolism of A. ferrooxdans. Since then, Yang Peidong and others have developed light-harvesting nanowire arrays with good biocompatibility (TiO2 nanoarrays as photoanodes and silicon nanoarrays as photocathodes)[86]. Upon light excitation, the reducing force generated by the S. ovata nanoarray photoanode can be directly used to drive the selective reduction of CO2 to acetic acid by S. ovata supported in a silicon nanoarray photocathode (Faradaic efficiency up to 90%). However, the lower pH value of the system in the reaction process will lead to a decrease in the number of microorganisms and catalytic efficiency. Therefore, by adjusting the pH value of the electrolyte and increasing the buffer capacity of the reaction system, the research group optimized the interface between silicon nanowires and S. ovata, so that more microorganisms were loaded on the nanowires to form a tightly packed nanowire-bacteria cathode, which improved the efficiency of direct transfer of photogenerated electrons between the electrode and microorganisms. Under the excitation of light, in addition to the electrons generated by the photoanode, the electrons generated by the silicon nanowires can also be transferred from the cathode of the Si nanowires to S. ovata through direct electron transfer or S. ovata mediation, generating reducing power in cells, and further converting acetyl-Coa into acetate and biomass through the Wood-Ljungdahl pathway (fig. 5C). In addition, the nanowire-bacteria hybrid system combined with photovoltaic devices was shown to be 3.6% efficient in immobilizing CO2 using solar energy within 7 days[87]. Although the electrode-microbial hybrid system has largely solved the problem that biological enzymes can not replicate themselves and the harsh environmental requirements, it needs further optimization in terms of organism stability, reaction continuity and reactor complexity.

4.2 Inorganic semiconductor-biological hybrid system

Inorganic semiconductor-organism hybrid system is a semi-artificial photosynthetic system which combines inorganic semiconductor with organism. The system uses sunlight to excite a semiconductor to generate photogenerated electrons, and the photogenerated electrons are transferred to an organism through different electron transfer paths to drive the physiological metabolism and product synthesis of the organism. In the process of electron transfer, the rapid recombination of electrons and holes will affect the transfer and utilization efficiency of photogenerated electrons. Therefore, it is of great significance to explore the electron transfer mechanism of inorganic semiconductor-biological hybrid system for maximizing the use of photogenerated electrons and improving the solar energy conversion efficiency.
In 2016, Kornienko et al. Used CdS semiconductor nanoparticles as photosensitizers to achieve efficient reduction of M. thermoacetica to acetic acid by combining with acetogenic bacteria (M. thermoacetica)[88]. Upon photoexcitation, CdS oxidizes cysteine (Cys) to cystine (CySS) to fill the valence band hole, while the photogenerated electrons from the conduction band can be transferred to membrane-bound proteins or soluble electron acceptors (Figure 6a). In addition, they further clarified the charge transfer and energy transfer mechanism of M. thermoacetica-CdS interface by transient absorption and time-resolved infrared spectroscopy. The results show that the photogenerated electrons can not only directly enter the Wood-Ljungdahl cycle through the H2 produced by the membrane-bound NiFe hydrogenase, but also be transferred to the corresponding enzymes for metabolic reactions through the membrane-bound cytochrome, ferredoxin (Fd), flavoprotein (Fp) and menaquinone (MK) pathways[88]. On this basis, Zhang et al. studied the charge transfer in the biohybrid system of M. thermoacetica-CdS and the proteome and metabolome of M. thermoacetica immobilization related pathways (Fig. 6B)[89]. It was found that the expression of electron carriers (membrane-bound proteins, Fd, Fp and NADH dehydrogenase) was significantly up-regulated during the transfer of photogenerated electrons to the cytoplasm and the immobilization of CO2. Electrons are transported along the cell membrane through the carrier, and then shuttled into the cell through menaquinones to produce acetyl-Coa with CO dehydrogenase and acetyl-Coa synthetase, and further participate in cell metabolism to produce acetic acid. In addition, the results of targeted metabolome and proteome data analysis show that glycolysis and tricarboxylic acid (TCA) cycle in biohybrid systems can participate in ATP production to form reducing equivalents, thus promoting cell functional metabolism[89].

4.3 Plasmon-biological hybrid system

Plasmon refers to the interaction between free electrons and photons on the surface of metal materials to form resonance, thus exciting the generation of electrons, which has attracted much attention because it can effectively overcome the shortcomings of inorganic semiconductor photosensitizers (limited biocompatibility and photocorrosion)[90][91]. Plasmonic materials include gold nanoclusters, silver nanoparticles and graphene[92][93][94]. The basic principle of plasmon generating electrons is that when metal nanoparticles are excited by light, the internal electrons produce dipole vibration, which redistributes the charges on the surface of metal nanoparticles and generates local electromagnetic field. Electrons migrate in different directions with the help of electromagnetic field, which effectively prolongs the lifetime of electrons and holes and promotes multi-electron redox reactions (Fig. 7A)[92]. Plasmon-biological hybrid systems use plasmons as photosensitizers, which can effectively drive the energy metabolism and material synthesis of organisms by generating electrons when excited by light. It is reported that the combination of gold nanoplasmons and photosystem I (PSI) can significantly enhance the photocurrent of the system through the plasmon electronic coupling effect[95]. In addition, Zhang et al reported that gold nanoclusters with good biocompatibility were embedded into M. thermoacetica cells to overcome the problem of slow extracellular electron transfer in existing photosensitizer-organism hybrid systems[31]. Under visible light irradiation, intracellular gold nanoclusters are excited by light to generate electrons, and through a series of electron transfer processes, a higher yield of acetic acid accumulation is finally achieved through the Wood-Ljungdahl pathway. In addition, gold nanoclusters can be used as ROS inhibitors to maintain the activity of cells, so that non-photosynthetic bacteria can reduce CO2 to produce acetic acid more efficiently and persistently (Fig. 7 B). Therefore, plasmons have the dual advantages of high electron and hole separation efficiency and good biocompatibility. It should be pointed out that the plasmon-biological hybrid system as a new semi-artificial photosynthetic system is still in its infancy and needs further study.
To sum up, the current electron transfer modes of BMSAPS can be summarized into three ways: first, the photosensitizer is excited by light to generate electrons that are directly transferred to the biocatalyst; Second, the photogenerated electrons are mediated to the biocatalyst by the redox species; Third, photogenerated electrons are delivered to the biocatalyst mediated by hydrogen/formic acid. However, there is an energy loss in the transfer of photogenerated electrons to the biocatalyst via redox species and hydrogen/formic acid-mediated pathways, which may be one of the reasons for the slow kinetics of photogenerated electron transfer[96]. In addition, there are other competing electron acceptors (such as water molecules, nitrate ions and sulfate ions) in the photogenerated electron transfer process of BMSAPS.Moreover, free radicals such as active oxygen produced in the system also have strong electron competition ability, which inhibits the effective combination between electrons and biocatalysts, resulting in slow electron kinetic transfer process. Although some researchers have introduced biocompatible gold nanoclusters (AuNCs) into microbial cells to avoid the slow electron kinetic transfer caused by electron acceptor competition[31]. However, most of the studies on electron transfer kinetics have focused on BMSAPS, which is composed of sulfur-based semiconductors and microorganisms. There are few reports on the kinetic mechanism of electron transfer between different semiconductors and microorganisms and how to enhance the electron capture and utilization ability of microorganisms, so the further study of the related mechanism is still the focus of future research to improve the electron transfer efficiency of BMSAPS.

4.4 Typical BMSAPS research method

Exploring the mechanism of action of BMSAPS depends on the development of research techniques. Table 2 lists representative methods used to characterize BMSAPS studies in recent years. According to the photogenerated electron transfer process of BMSAPS, the research techniques are divided into three aspects: (1) photogenerated electron excitation-transition process, including time-resolved infrared spectroscopy and fluorescence spectroscopy[88][97]; (2) photogenerated electron transfer process, including transient absorption spectroscopy and scanning electrochemical microscopy imaging[88][47]; (3) Photoelectron utilization processes, including NADH/NAD ratio, proteome, and metabolome (fig. 8)[26][89]. Kornienko et al. First used transient absorption spectroscopy (TA) and time-resolved infrared spectroscopy (TRIR) to characterize the electron transfer and transient lifetime of BMSAPS, in order to explore the charge transfer and energy transfer mechanism of CdS-M. thermoacetica hybrid system[88]. Since then, Wang et al. characterized the change of intracellular redox potential of microorganisms in BMSAPS by measuring the ratio of NADH/NAD, and clarified the change of intracellular charge[26]. Zhang et al. characterized gold nanoclusters in vivo using a structured light illumination microscope to further analyze the important functions of photosensitizers in BMSAPS[31]. In 2019, Ye et al. Introduced a new electrochemical method to characterize the photocurrent changes during the light-dark cycle of BMSAPS by scanning electrochemical microscopy[47]. In 2020, Zhang et al. Used highly sensitive mass spectrometry to study the proteome and metabolome changes of BMSAPS, and clarified the electron transfer and related metabolic pathways of biological hybrid systems[89]. However, the current research techniques can not accurately observe the electron transport mechanism of BMSAPS multi-interface. In addition, more advanced research methods need to be developed for the systematic study of diverse organisms and complex metabolic pathways.

5 BMSAPS Application

Since the first successful construction of BMSAPS, there have been many reports on the application of BMSAPS in energy production and environmental remediation. At present, that application of the BMSAPS mainly comprise two categories: firstly, the oxidizability of the BMSAPS is utilize, and environmental remediation such as pollutant degradation, disinfection and sterilization and the like is utilized[101][102,103]; Second, use the reducibility of BMSAPS for energy production such as carbon fixation, nitrogen fixation and hydrogen production[31][104][58]. This chapter focuses on the application of BMSAPS to energy production.

5.1 Carbon fixation

Carbon fixation is mainly through the construction of BMSAPS to drive heterotrophic microorganisms (or macromolecular enzymes) to immobilize CO2. Yang Peidong's team first proposed to use M. thermoacetica to load CdS in situ to construct BMSAPS, which drives the reduction of M. thermoacetica to acetic acid under visible light, opening a new chapter in the application of BMSAPS carbon fixation[24]. In 2019, Ye et al. constructed a M. barkeri-CdS hybrid system to effectively drive the methanogenesis process of M. barkeri, and the methane yield was 0. 19 μmol/H under illumination (395 ± 5 nm)[47]. On this basis, in view of the shortcomings of CdS, such as easy recombination of electrons and holes under light excitation and low efficiency of electron transmission, the research group doped CdS with nickel (Ni) (Ni: CdS) and constructed a hybrid system of M. barkeri and Ni: CdS. The results show that the M. barkeri-Ni: CdS hybrid system has a strong photogenerated electron separation and transfer efficiency, and its methane production is 250% higher than that of the M. barkeri-CdS hybrid system[77]. Furthermore, in order to overcome the metal toxicity and photocorrosion of inorganic semiconductors, Gai et al. Used organic semiconductors as photosensitizers to form a p-n heterojunction (PFP/PDI) photosensitive layer by coating perylene diimide derivatives (PDI) and Polyfluorene phenylene (PFP) on the surface of bacteria, thus achieving a higher hole/photogenerated electron separation efficiency[53]. Under illumination, M. thermoacetica gains photogenerated electrons from the PFP/PDI heterojunction to drive the synthesis of acetic acid by reducing M. thermoacetica with a quantum efficiency of 1.6%. In addition, the low photoregeneration efficiency of redox-active cofactors is also an important bottleneck restricting the application of semi-artificial photosynthetic systems. It has been reported that BMSAPS is composed of thiophene-modified double-shell hollow g-C3N4 clusters (ATCN-DSCN) and formate dehydrogenase, which can efficiently photoregenerate NADH and realize the reduction of CO2 by formate dehydrogenase to formic acid, and the yield of formic acid is 290.0μmol·L-1 after 9 H of illumination[43].

5.2 Nitrogen fixation

In 2016, Brown et al. First used CdS nanocrystals as photosensitizers to combine with molybdenum iron (MoFe) protein to construct BMSAPS[34]. This system can effectively drive MoFe protein to reduce N2 to NH3 with a turnover rate of 75 min-1. In addition, Wang et al. loaded CdS nanoparticles onto the surface of photoheterotrophic bacteria (R. palustris)[59]. The results showed that CdS photoexcited electron significantly improved the biological nitrogen fixation ability of R. palustris, the cumulative biomass increased by 153%, and the photosynthetic efficiency was 6. 73%. The hydrogen produced by Liu et al. Through photoelectrocatalytic water splitting was utilized by hydrogen-oxidizing bacteria (X. autotrophicus), which was able to reduce X. autotrophicus and CO2 to biomass with a turnover frequency of 1.9×104s-1·cell-1[104]. The system can be powered by renewable electricity to sustainably and selectively produce ammonia and biofertilizers. In 2020, Lu et al. Designed a photoelectrode-driven biohybrid system with nodule function[105]. The silicon-based microarray electrode is compatible with nitrogen-fixing symbionts (X. autotrophicus and B. japonicum) that harvest energy and reducing equivalents (X. autotrophicus) from the photoelectrode and fix B. japonicum as biomass and free ammonia. The reduction rate of N2 in this device is up to 6.5 mg N2g dry biomass-1·h-1, which is about two orders of magnitude higher than that under natural conditions.

5.3 Hydrogen production

As early as 2012, Brown et al. Constructed a hybrid system of [FeFe] -hydrogenase and CdS nanorods[23]. Hydrogen production from hydrogenase was achieved under the excitation of semiconductor light at 405 nm, and the photon conversion efficiency was 20%. However, the enzyme requires a harsh environment in an ex vivo environment to maintain activity. In order to overcome the influence of external environment on enzyme activity, Honda et al integrated the [FeFe] -hydrogenase gene of C. acetobutylicum into Escherichia coli, and used engineered Escherichia coli and C. acetobutylicum to form a biological hybrid system[35]. The system uses methyl viologen as an electron transfer medium to realize continuous hydrogen production under illumination. In addition, in order to solve the problem that the oxygen produced in the hydrogen production process of BMSAPS will lead to the reduction of microbial activity, Wei et al. Constructed a hybrid system using semiconductors and engineered Escherichia coli[58]. E. coli used in situ biosynthesis of CdS nanoparticles and biomimetic silica to encapsulate the hybrid system. The system can produce hydrogen continuously for 96 hours under aerobic conditions. However, the semiconductor CdS and TiO2 used in the above BMSAPS suffer from low efficiency of photoexcited electron-hole separation. Therefore, Jiang et al. enhanced the separation efficiency of photoexcited electrons and holes and improved the conversion efficiency of H2 by constructing a hybrid system of AglnS2/In2S3 heterojunction and Escherichia coli, with a quantum efficiency as high as 3.3%[52].

6 Prospect

The development and application of solar-driven BMSAPS are of great significance for carbon dioxide fixation, clean fuel production and alleviating global energy shortage and environmental problems. The key problem in the construction of BMSAPS is the interaction between photosensitizer and biocatalyst, and the core is the electron transfer and energy conversion pathway. However, the research on the electron and energy transfer of BMSAPS is not deep enough, and there is a lack of accurate characterization techniques and means, which can not provide theoretical support for the development of efficient BMSAPS. In addition, most of the currently constructed BMSAPS require exogenous sacrificial reagents to quench the photoexcited holes, and the commonly used photosensitizers are toxic to organisms due to the presence of metals, which restricts the industrial application of BMSAPS.
The fundamental solution to the above problems depends on the deepening of basic research. In order to promote the practical process of BMSAPS, it is necessary to systematically summarize the existing research results and refine the key points to solve the problems, so as to provide guidance for the development of high-performance BMSAPS. Based on the photocatalytic principle of photosensitizers, new theories can be introduced and advanced experimental techniques can be used to develop photocatalytic materials with high quantum efficiency, expand the range of light absorption and enhance the performance of light harvesting. From the perspective of biocatalysts, microorganisms can be functionalized by means of synthetic biology to enhance their specific binding and selective photocatalytic properties. In addition, it is necessary to deepen the understanding of the electron transport mechanism of BMSAPS, and to conduct a comprehensive in-situ study of the generation, transport and transformation of photogenerated electrons and the interfacial dynamics process from multi-interface, multi-element and multi-process.The electron transfer and energy conversion mechanism of BMSAPS was explored to enhance the electron-hole separation efficiency of photocatalytic materials and give full play to the electron capture and utilization efficiency of organisms. In addition, it is necessary to break through the existing theoretical framework and introduce other disciplines for interdisciplinary integration to provide technical support for the development of more efficient, greener and more economical BMSAPS.

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Funding

National Natural Science Foundation of China(41925028)

National Natural Science Foundation of China(41977281)

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