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Abbreviation (ISO4): Prog Chem      Editor in chief: Jincai ZHAO

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Progress in Chemistry >

2025 , Vol. 37 >Issue 2: 157 - 172

DOI: https://doi.org/10.7536/PC240501

Review

Photo-Driven Whole-Cell Biohybrids Based on Semiconductors and Microorganisms

  • Kaichong Wang 1 ,
  • Han Wang 1 ,
  • Yayi Wang , 1, 2, *
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  • 1 School of Environmental Science and Engineering, Tongji University, Shanghai 200092, China
  • 2 State Key Laboratory of Pollution Control and Resource Reuse, Tongji University, Shanghai 200092, China
* e-mail:

Received date: 2024-05-07

  Online published: 2025-03-28

Supported by

National Natural Science Fund for Distinguished Young Scholars(52225001)

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Abstract

Solar energy is the energy source for all life on Earth, and its efficient conversion is of great significance for solving the global energy crises and environmental issues. Inspired by natural photosynthesis, researchers have recently developed whole-cell biohybrids based on semiconductors and microorganisms by integrating the excellent light absorption ability of photosensitizer semiconductors and the efficient biocatalysis ability of whole-cell microbes. The development of whole-cell biohybrids aims to realize efficient solar-to-chemical production in a green and low-carbon pathway. This review clarifies the operation principle and advantages of whole-cell biohybrids, and the properties of photosensitizer semiconductors are summarized, including the band structure, excitation wavelength and quantum yield. Moreover, this work innovatively concludes the construction mechanisms of whole-cell biohybrids and the electron transfer mechanisms in the interface between semiconductor and microbe. Moreover, the advanced progress of whole-cell biohybrids are reviewed, such as the high-value conversion of carbon dioxide, artificial nitrogen fixation, hydrogen production as well as pollutant removal and recovery. Finally, the environmental impacts and challenges of whole-cell biohybrids are discussed and the perspectives for the development of whole-cell biohybrids are proposed. This article is expected to provide fundamental insights for the further development and actual application of whole-cell biohybrids.

Contents

1 Introduction

2 Principles and advantages of whole-cell biohybrids

3 Types of photosensitizers in whole-cell biohybrids

3.1 Inorganic semiconductors

3.2 Organic semiconductors

4 Construction mechanisms of whole-cell biohybrids

5 Advanced application progresses of whole-cell biohybrids

5.1 High-value conversion of CO2

5.2 Artificial nitrogen fixation

5.3 Hydrogen production

5.4 Pollutants removal and resource recovery

6 The environmental impacts and challenges in whole-cell biohybrids

7 Conclusion and outlook

Key words： solar energy; semiconductor; microorganism; whole-cell biohybrid; electron transport

Cite this article

Kaichong Wang , Han Wang , Yayi Wang . Photo-Driven Whole-Cell Biohybrids Based on Semiconductors and Microorganisms[J]. Progress in Chemistry, 2025 , 37(2) : 157 -172 . DOI: 10.7536/PC240501

1 Introduction

Currently, the increasingly severe energy and environmental crises are major challenges faced by all humanity, seriously restricting the sustainable development of human society[1]. According to the "World Energy Statistics Yearbook", the global energy consumption and carbon dioxide (CO2) emissions in 2022 have reached 604.04 exajoules and 39.315 billion tons, respectively, with fossil energy accounting for up to 82% and 87%. To reduce dependence on fossil fuels, researchers are accelerating the promotion of the utilization of renewable energy sources such as solar, wind, and hydrogen energy[2-3]. Among them, the maximum flux density of sunlight reaching the Earth is 0.2~1 kW/m2, and the energy transmitted per hour can meet the Earth's annual demand, showing great application potential[4⇓⇓-7]. At the same time, solar energy can also be converted into other types of energy such as electricity, fuel, and thermal energy to meet global energy demands. Therefore, achieving efficient conversion of solar energy has become a research hotspot in the current energy and environmental fields.
Solar energy is the source of all life activities on Earth, and all life on Earth directly or indirectly relies on solar energy for survival[4,8 -9]. In nature, photoautotrophic organisms such as plants, algae, and photosynthetic bacteria store solar energy in chemical energy through photosynthesis, achieving the activation of various natural small molecules like water (H2O), CO2, and nitrogen (N2) as well as green and efficient energy conversion, providing a classical paradigm for the efficient utilization of solar energy[4,10]. Photosynthesis converts solar energy into chemical energy, driving a series of biochemical reactions in photoautotrophic organisms, such as converting CO2 and H2O into organic energy carriers and oxygen, which constitutes the core mechanism of energy and carbon cycling in carbon-based life forms[11-12]. However, the conversion efficiency of solar energy to chemical energy in photosynthesis is relatively low; although the theoretical maximum can reach 12%, in practice it is generally less than 1%, greatly limiting the application of photosynthesis[13-14].
Inspired by photosynthesis, researchers have achieved the directional conversion of solar energy into chemical energy in recent years by constructing semiconductor-enzyme and semiconductor-microbe hybrids[15-16]. These hybrids integrate the excellent light absorption properties of semiconductors (solar energy conversion efficiency >20%) with the efficient biocatalytic capabilities of enzymes/microorganisms. Through electronic interactions at the semiconductor-microbe interface, they show great potential in achieving light-driven CO2 conversion, clean energy production, and other fields[17⇓-19]. Compared with semiconductor-enzyme hybrids, the whole-cell hybrids of semiconductor-microbes have attracted much attention due to their high stability, functional diversity, and self-replication capability[20⇓-22]. This paper focuses on the research progress of whole-cell hybrids in recent years, starting from the working principles and advantages, summarizing and comparing the types and performance of photosensitizers, mainly elucidating the different construction mechanisms of whole-cell hybrids and the electronic interaction mechanism at the semiconductor-microbe interface, and reviewing the research status of whole-cell hybrids in high-value CO2 conversion, artificial nitrogen fixation, hydrogen production, pollutant removal, and resource utilization. In addition, the environmental impacts and challenges of whole-cell hybrids are discussed, and future research directions are proposed for reference.

2 Principles and Advantages of Whole-cell Hybrids

The whole-cell hybrid mainly consists of four elements, namely photosensitizer, electron donor, electron carrier, and biocatalyst (Fig. 1). The basic principle of the whole-cell hybrid is as follows: under certain wavelength conditions, when the energy of photons absorbed by the photosensitizer is greater than or equal to the bandgap width, the ground-state electrons (e-) on the valence band (VB) are excited to transition to the conduction band (CB), thereby generating higher-energy photogenerated electrons; subsequently, the photogenerated electrons can be transferred to the active sites of the biocatalyst through direct transfer, electron carriers, and other pathways, driving a series of subsequent metabolic activities[10]. In the whole-cell hybrid, the photosensitizer is composed of structurally controllable and biocompatible photosensitive semiconductors[23]. The electron donor, also known as the sacrificial agent, mainly serves to quench the photogenerated holes (h+) of the photosensitive semiconductor, preventing the recombination of holes and electrons. Water, as an electron donor, has the advantages of stable chemical properties, easy availability, and no harmful by-products[24], making it the most ideal electron donor in the whole-cell hybrid. However, due to the kinetic limitations of slow four-electron migration during water oxidation and constraints from the inherent defects of the photosensitive semiconductor itself (such as self-oxidation corrosion caused by rapid recombination of photogenerated carriers), water is difficult to use as an electron donor in the whole-cell hybrid[25]. Therefore, at this stage, substances that are easily oxidized are usually used instead of water as electron donors, such as cysteine, lactate, sulfite, etc.[15,26].
图1 基于半导体和微生物的全细胞杂合体工作原理示意图

Fig. 1 The schematic diagram of the principle of whole-cell biohybrids based on semiconductors and microorganisms

The electron carrier is crucial for transferring photogenerated electrons to the biocatalyst. In whole-cell hybrids, soluble redox substances (methyl viologen, flavins, etc.) or redox-active proteins (microbial cytochromes, nanowires, etc.) are typically used as electron carriers to transfer photogenerated electrons to the biocatalyst[20,27]. Additionally, hydrogen-mediated electron transfer processes also play a significant role in the transfer of photogenerated electrons[15,28]. In whole-cell hybrids, the biocatalysts are mainly undertaken by electroactive microorganisms, such as Shewanella oneidensis MR-1 (S. oneidensis MR-1), Methanosarcina barkeri (M. barkeri), etc.[29,30]. Furthermore, based on the different functions of microorganisms, multifunctional designs of whole-cell hybrids can be implemented to achieve full utilization and conversion of solar energy[31].
Compared with semiconductor-enzyme hybrids, whole-cell hybrids have the following advantages. First, microorganisms possess higher stability and self-repair capability. During long-term continuous operation, microorganisms can maintain their activity and undergo self-repair through growth and reproduction, avoiding enzyme inactivation[32]. Second, microorganisms have an efficient multi-enzyme cascade catalytic mechanism, enabling complex metabolic processes through various enzymes rather than being limited to single-enzyme catalysis[33]. Finally, compared with highly purified enzymes, microorganisms are generally easier to cultivate and obtain on a large scale, and at a lower cost, reducing the operational cost and difficulty of the system[10].

3 Types of Photosensitizers in Whole-Cell Hybrids

In full-cell hybrids, the electron donors, electron carriers, and microbial species are relatively fixed, while the types and properties of photosensitizers have the greatest impact on the system. Stable full-cell hybrids impose comprehensive requirements on the band structure, light absorption range, and biocompatibility of the photosensitizer. Typically, to achieve the transfer of photogenerated electrons, the band structure of the photosensitizer in full-cell hybrids should satisfy: (1) The reduction potential of photogenerated electrons is more negative than the reduction potentials of electron carriers and biocatalysts; (2) The oxidation potential of photogenerated holes is more positive than the oxidation potential of electron donors. Meanwhile, compared with the ultraviolet range, efficient absorption of visible light by photosensitizers is more conducive to stable microbial metabolic activities[34]. Additionally, the compatibility between the photosensitizer and microorganisms determines the electron transfer efficiency in full-cell hybrids, and quantum efficiency (QY) can serve as an important evaluation index for the matching degree between photogenerated electrons and microbial utilization. Therefore, the photosensitizer is the core of full-cell hybrids, and its band structure, excitation wavelength, and biocompatibility are the main selection criteria in full-cell hybrids. At present, photosensitizers in full-cell hybrids can mainly be divided into inorganic semiconductors and organic semiconductors.

3.1 Inorganic Semiconductors

Semiconductors are materials with conductivity between conductors and insulators, with resistivity in the range of 10-9~10-2 Ω·cm[35]. Among inorganic semiconductors, cadmium sulfide (CdS) is widely used in whole-cell hybrids due to its wide range of light absorption wavelengths (can absorb visible and ultraviolet light with wavelengths shorter than 516 nm), good carrier transport rate, excellent biocompatibility, and ease of preparation. In addition, researchers have employed various inorganic semiconductors for constructing whole-cell hybrids, such as indium phosphide (InP), cuprous oxide (Cu2O), and cadmium selenide quantum dots (CdSe QDs), etc. Specific material information is shown in Table 1.
表1 全细胞杂合体中无机半导体的种类、能带结构、激发波长及量子效率

Table 1 The types, band structures, excitation wavelength and quantum yield of inorganic semiconductors in whole-cell biohybrids

Type VB (V vs SHE) CB (V vs SHE) Bandgap (eV) Excitation wavelength (nm) QY (%) ref
CdS -0.68 1.62 2.30 395~ 460 0.06 ~ 23.4 20,39⇓⇓ -42
NiCu@CdS -1.00 1.68 2.68 395 12.41 43
CdS@Fe3O4 - - - 420 11.5 44
BiVO4:Mo -0.3 2.1 2.40 > 200 0.70 45
SrTiO3:La,Rh -0.9 2.3 3.20 > 200 0.70 45
InP 0.9 -0.44 1.34 Cold white 0.70 46
CdSexS1-x -0.63 1.83 2.46 420 27.56 47
Cd0.8Zn0.2S -0.58 1.75 2.62 450 16.82 37
Cu2O 1.89 -0.51 2.40 > 420 - 48
InP QDs - - 1.35 - 6~8 49
CdSe QDs -1.4 1.0 2.40 530 0.17 29
CdTe QDs - - 2.19 505~657 7.1~ 47.2 13
InP/ZnSe QDs - - 2.64~3.1 400 - 50
CuInS2/ZnS QDs -0.6 1.5 2.1 420~780 15.02 51
TiO2 -0.29 2.91 3.2 300~350 31.2 27
Al2O3 - - 3.20 410 - 52
Ag3PO4 - - 1.55 400~780 - 34
Au NCs - - - Simulated solar light 2.86 53
Au nanoparticles - - - 400~800 19.31 54
To address the issues of rapid recombination of photogenerated electron-hole pairs and high energy barriers at surface sites in inorganic semiconductor materials, researchers have employed strategies such as constructing homojunctions and heterojunctions to modulate their structural properties, thereby enhancing the performance of hybrids[36]. Zhang et al.[37] synthesized Cd0.8Zn0.2S nanoparticles with a homojunction and combined them with Sporomusa ovata (S. ovata) to construct a whole-cell hybrid for the reduction of CO2 to acetate. Under the same operating conditions, the whole-cell hybrid based on Cd0.8Zn0.2S achieved the highest acetate production (35.20 ± 3.28 mmol·L-1), significantly outperforming whole-cell hybrids using either pure CdS or ZnS (26.20 ± 1.33 mmol·L-1 and 18.69 ± 3.28 mmol·L-1, respectively). However, most inorganic semiconductor materials contain heavy metals, whose toxic effects on microorganisms and the release of heavy metal ions after photocorrosion constrain the construction and application of whole-cell hybrids[38].

3.2 Organic Semiconductors

Organic semiconductor materials typically possess π-electron systems, which can directly adjust the properties of the materials themselves through chemical modification, enabling them to have absorption or fluorescence emission in the ultraviolet, visible, or near-infrared wavelength range, demonstrating structural richness and functional diversity[55-56]. In addition, compared with inorganic semiconductor materials, organic semiconductor materials have advantages such as efficient electron transfer and low biotoxicity, gradually becoming important photosensitizers in whole-cell hybrids[57]. In whole-cell hybrids, organic semiconductors mainly consist of conjugated polymer nanoparticles[58], organic conjugated semiconductors[59], carbon nitride (C3N4)[60], etc. The organic semiconductor materials reported so far are shown in Table 2. Moreover, strategies such as nanostructure optimization and heterojunction design of organic semiconductor materials can also be used for constructing whole-cell hybrids. For example, Gai et al.[38] utilized a heterojunction of perylene diimide derivative (PDI) and p-type polyfluorene derivative (PFP) with Moorella thermoacetica (M. thermoacetica) to construct a whole-cell hybrid, successfully achieving non-photosynthetic microorganism-mediated photodriven CO2 reduction.
表2 全细胞杂合体中有机半导体的种类、能带结构、激发波长及量子效率

Table 2 The types, band structures, excitation wavelength and quantum yield of of organic semiconductors in whole-cell biohybrids

Type LUMO (eV) HOMO (eV) Bandgap (eV) Excitation wavelength (nm) QY (%) ref
Oligofluorene (OF) -1.66 -5.01 3.35 Visible light - 67
Polythiophene (PTP) -2.40 -5.42 3.02 Visible light - 67
Poly(fluorene-alt-thienopyrazine) (PFTP) -3.51 -5.40 1.89 > 420 1.25 58
MEH-PPV -3.79 -6.03 2.24 > 420 1.25 58
Poly(fluorene-alt-phenylene) (PFP) -2.81 -5.73 2.92 350~800 0.83 68
PDI -3.89 -6.02 2.13 > 420 1.6 38
PFP -2.60 -5.54 2.94 White light 1.43~1.6 31,38
COE-IC -0.85 (VB) +0.90 (CB) 1.75 400~700 - 59
CDPCN -0.49 2.30 2.68 395 - 69
NCNCNx -0.86 1.90 2.76 395 50.3 61
PFODTBT -0.90（VB） +1.06（CB） 2.96 Simulated solar light 2.27 70
C3N4 QDs - - - Simulated solar light - 60
I-HTCC -0.53 0.66 1.19 470~700 9.11 71
Compared to inorganic semiconductors, the quantum efficiency of reported organic semiconductor systems is relatively low (Table 1 and Table 2), which may be due to the mismatch between the photogenerated electron yield of organic semiconductors and the microbial electron utilization rate[61]. Meanwhile, the stability of organic semiconductors is susceptible to factors such as light exposure and oxidation during prolonged use, leading to loss of photochemical activity[62-63], thereby causing a decline in the efficiency of whole-cell hybrid systems. For instance, the conjugated polymer MDMO-PPV can degrade under light exposure and undergo photo-induced crosslinking to form higher molecular weight polymers, completely losing photochemical activity within 25 hours of illumination[64]. Additionally, water and trace oxygen (~1015 cm-3) can also reduce the charge migration efficiency of organic semiconductors and decrease their stability[65-66]. Hu et al.[61] modified polymeric carbon nitride with cyano groups (NCNCNx) to impart capacitive properties; in the M. barkeri-NCNCNx hybrid, NCNCNx facilitates the storage and distribution of photogenerated electrons at the microbe-photosensitizer interface, enabling the hybrid to sustain methanogenic activity for over 180 minutes with just 10 minutes of illumination, achieving a quantum efficiency of up to 50.3%. In the future, further development of more high-performance photosensitizer materials will still be needed to achieve efficient light energy capture and stable microbial photoelectron utilization.

4 Mechanism of Whole-Cell Hybrid Construction

In whole-cell hybrids, the interface construction method is a key factor affecting the efficiency of the whole-cell hybrid, which not only influences the closeness between the semiconductor and the microorganism but also restricts the intensity of electron interaction between the semiconductor and microbial proteins and enzymes. Currently, the interface construction methods between semiconductors and microorganisms mainly include outer membrane binding and intracellular binding (Figure 2 and Figure 3).
图2 基于外膜结合的全细胞杂合体：（A）Saccharomyces cerevisiae-InP杂合体结构示意[46]；（B）M. thermoacetica -CdS杂合体（左）与M. thermoacetica（右）的对比[41]；（C）扫描电子显微镜下的M. barkeri -NiCu@CdS杂合体[43]；（D）扫描透射电子显微镜（STEM）下M. thermoacetica-CdS杂合体的高角环形暗场成像（HAADF）[15]；激光共聚焦显微镜（CLSM）下的M. barkeri -NCNCNx（E）和Azotobacter Chroococcum-PFP杂合体（F）[61,68]

Fig. 2 Whole-cell biohybrids based on outer membrane binding. (A) Structure of Saccharomyces cerevisiae-InP biohybrid[46]; (B) Comparison of M.thermoacetica-CdS biohybrid (left) with M.thermoacetica (right)[41]; (C) M.barkeri-NiCu @CdS biohybrid under scanning electron microscope[43]; (D) High-angle annular dark field imaging (HAADF) of M.thermoacetica-CdS biohybrid under scanning transmission electron microscopy (STEM)[15]; M.barkeri-NCNCNx (E) and Azotobacter Chroococcum-PFP biohybrids (F) under confocal laser scanning microscopy (CLSM)[61,68]

图3 基于胞内结合的全细胞杂合体：（A）STEM下的E. coli -CdS杂合体[75]；（B）Azotobacter vinelandii（A. vinelandii）- InP/ZnSe QDs杂合体的HAADF-STEM成像[50]；（C）E. coli -C3N4 QDs杂合体的CLSM成像组合图[60]；（D）M. thermoacetica-Au NCs杂合体的结构光照明显微成像（SIM）[53]；（E）基于同步辐射的三维X射线荧光层析成像实验方法及全细胞杂合体的三维X射线荧光断层扫描重构[75]

Fig. 3 Whole-cell biohybrids based on intracellular binding. (A) E.coli-CdS biohybrid under STEM[75]; (B) HAADF-STEM imaging of Azotobacter vinelandii (A.vinelandii)-InP/ZnSe QDs biohybrid[50]; (C) CLSM imaging of E.coli-C3N4 QDs biohybrids[60]; (D) The structure illumination microscopy (SIM) of M.thermoacetica-Au nanoclusters biohybrid [53]; (E) Synchrotron radiation-based three-dimensional X-ray fluorescence tomography experimental method and three-dimensional X-ray fluorescence tomography reconstruction of whole-cell biohybrid[75]

Outer membrane binding is the most commonly used method for constructing whole-cell hybrids, and both inorganic and organic semiconductors can achieve binding with the microbial outer membrane (Figure 2). Inorganic semiconductors can bind to the microbial outer membrane through external addition deposition and induced precipitation methods (Figures 2A to E)[15,30]. For example, CdS can be externally prepared and then added and deposited on the microbial surface[26], or Cd2+ can be introduced into the culture medium and CdS nanoparticles can be formed on the microbial surface using S2- produced by microbial metabolism[40]. Organic photoelectric semiconductors mainly achieve binding with the microbial outer membrane through electrostatic interactions, hydrophobic interactions, and in-situ catalytic synthesis methods (Figure 2F)[38,72]. For instance, PDI and PFP, as cationic polymers of organic semiconductors, can bind to the negatively charged microbial outer membrane through electrostatic interactions, and the cationic side chains can embed into the cell membrane via hydrophobic effects, achieving efficient transfer of photogenerated electrons to the microorganisms[38]. The in-situ induction synthesis of organic photoelectric semiconductors on the microbial outer membrane surface is mainly achieved through a bio-palladium catalytic polymerization strategy. Qi et al.[72] utilized bio-palladium catalysis to perform the Sonogashira polymerization reaction for the first time, synthesizing the organic semiconductor poly(phenylene ethynylene) (PPE) in situ on the microbial outer membrane, providing new ideas for the construction methods of whole-cell hybrids.
In whole-cell hybrids based on outer membrane binding, microbial outer membrane proteins capture photogenerated electrons from semiconductors and drive the generation of reducing equivalents (NADH and NADPH), which can further enhance the transfer of photogenerated electrons in the electron transport chain, thereby driving microbial metabolic reactions[53,68]. Since most enzymatic reactions in microorganisms occur intracellularly, it is difficult for photogenerated electrons from extracellular semiconductors to directly interact with intracellular functional enzymes[73]. Meanwhile, the transmembrane transport of electron carriers consumes a large amount of energy, and the rate and efficiency of transmembrane diffusion are easily limited by the properties of the cell membrane and the selectivity of channels, thereby reducing the conversion efficiency of solar energy[53]. Therefore, if photogenerated electrons and reducing equivalents can be produced intracellularly and the distance for photogenerated electrons to reach functional enzymes is shortened, it will hopefully improve the energy transfer efficiency of semiconductors.
In whole-cell hybrids, intracellular binding is mainly achieved through microbial internalization and intracellular synthesis of semiconductors (Fig. 3). Semiconductor quantum dots (< 10 nm) and semiconductor nanoclusters (< 100 nm) have the advantages of small size, strong tunability, and high biocompatibility[29,74]. Microorganisms can construct whole-cell hybrids by internalizing semiconductor quantum dots and semiconductor nanoclusters (Fig. 3B and 3C). M. thermoacetica can internalize gold nanoclusters (Au NCs) with glutathione surface ligands via passive targeting to achieve the construction of whole-cell hybrids in the cytoplasm (Fig. 3D)[53]. Compared with outer membrane-bound CdS, internalizing Au NCs can increase the photoconversion efficiency of M. thermoacetica hybrids from 2.14% ± 0.16% to 2.86% ± 0.38% (Fig. 4A)[53]. However, microorganisms exhibit high selectivity for the internalization of semiconductor quantum dots and semiconductor nanoclusters, and excessive semiconductor internalization can also lead to microbial cell membrane rupture, which limits the construction of whole-cell hybrids through microbial internalization[13,29,50]. To date, the semiconductor materials successfully internalized by microorganisms in whole-cell hybrids mainly include carbon quantum dots[73], gold nanoclusters[53], InP/ZnSe quantum dots[50], and CuInS2/ZnS quantum dots[51].
图4 利用全细胞杂合体实现CO2向乙酸（A）[53]、甲烷（B）[43]和PHB（C）[70]高值转化的原理示意图

Fig. 4 The principle of high-value conversion of CO2 to acetic acid (A)[53], methane (B)[43] and PHB (C)[70] using whole-cell biohybrids

The intracellular synthesis of semiconductors is mainly achieved through the biomineralization of microorganisms (Fig. 3A and 3E)[47,75]. Biomolecules (proteins, peptides, etc.) in the microbial cells serve as nucleation sites for semiconductors, which can induce the self-assembly of semiconductors within the cells and generate ordered structures[76]. The periplasm is a unique structure of Gram-negative bacteria, located between the inner and outer membranes of the bacteria. The periplasmic space contains a large number of enzymes and peptidoglycans and is close to the electron transport chain attached to the inner membrane[40,51,75]. Lin et al.[75] utilized peptidoglycan as a nucleation site for biomineralization and generated defect-rich CdS nanoclusters in the periplasm through Escherichia coli (E. coli) biomineralization, which increased the ATP level of E. coli by 8.1 times under light. Meanwhile, dissimilatory metal-reducing bacteria (such as S. oneidensis MR-1, E. coli, Pseudomonas aeruginosa (P. aeruginosa), etc.) can rely on their extracellular electron transfer capabilities to synthesize semiconductor quantum dots from metal ions intracellularly[77]. These biologically synthesized quantum dots have better biocompatibility compared to chemically synthesized quantum dots[78]. Cui et al.[79] used the denitrifying bacterium P. aeruginosa to synthesize CdSexS1-x quantum dots in the periplasm and cytoplasm. The synthesized quantum dots enhanced the NADH content and the expression of various denitrification enzymes in P. aeruginosa under visible light.

5 Advances in the Application of Whole-Cell Hybrids

5.1 CO2High-Value Transformation

As the global energy crisis and climate issues become increasingly severe, the high-value conversion of CO2 has great potential in reducing greenhouse gas emissions and achieving sustainable development, and has received widespread attention worldwide[80]. Compared with CO2 conversion technologies such as chemical, photochemical, electrochemical, and thermochemical catalysis, the biocatalytic conversion of CO2 has the advantages of being environmentally friendly, having mild reaction conditions (room temperature and pressure), and high product selectivity[38,81]. However, inefficient electron transfer processes greatly limit the efficiency of microbial CO2 conversion[80]. In whole-cell hybrids, the photogenerated electrons from semiconductors can promote electron transfer in microorganisms, which is expected to improve the efficiency of microbial CO2 conversion[37].
In 2016, Sakimoto et al[15] achieved the construction of M. thermoacetica-CdS full-cell hybrids by inducing CdS nanoparticle deposition on the surface of M. thermoacetica, and for the first time utilized full-cell hybrids to achieve high-value conversion of CO2. The outer membrane proteins of M. thermoacetica capture photogenerated electrons from CdS and generate reducing equivalents NADH, thereby driving the Wood-Ljungdahl pathway for the conversion of CO2 to acetic acid (CH3COOH), with a maximum yield of 0.7 mM/d and a quantum efficiency of up to 2.44% ± 0.62%. Subsequently, researchers have continuously optimized the microbial species, semiconductor types, and full-cell construction mechanisms of the full-cell hybrids to achieve efficient conversion of CO2 to CH3COOH (Table 3). To date, the S.ovata-InP QDs hybrid based on intracellular and extracellular coupling exhibits the most excellent CO2 conversion performance, with a CH3COOH production rate reaching 0.9 mmol·L-1[49]. Additionally, the S.ovata-InP QDs hybrid can achieve continuous acetic acid production for 7 days, demonstrating good operational stability.
表3 全细胞杂合体在CO2高值转化中的应用进展及性能对比

Table 3 The application progress and performance comparison of whole-cell hybrids in the high-value conversion of CO2

Semiconductors Microbes Products Product yields QY (%) Operation time ref
CdS M. thermoacetica CH3COOH 0.7 mM/d 2.44 ± 0.62 4 d 15
Au NCs M. thermoacetica CH3COOH 6.0 mmol/gdcw 2.86 ± 0.38 7 d 32
PFP/PDI M. thermoacetica CH3COOH 0.21 mM/d 1.6 3 d 38
InP QDs S.ovata CH3COOH 0.9 mM/h 6~8 7 d 49
CdS S.ovata CH3COOH 0.17 mM/h 16.8 ± 9 5 d 82
SrTiO3:La,Rh and BiVO4:Mo S.ovata CH3COOH 0.6 mM/h 0.7 15 h 45
Cd0.8Zn0.2S S. ovata CH3COOH 8.2 ± 0.6 mM/d 16.82 ± 1.21 7 d 37
Zn-metal organic framework functionalized with TiO2 Mixed culture composed of Clostridium ljungdahlii, Acetobacterium woodii, and P. aeruginosa CH3COOH
CH3CH2OH		 0.32 g/(L·d)
1.06 g/(L·d)		 - 70 h 83
CdS-mineralized biofilms E. Coli HCOOH 0.11 mM/h 0.13 15 h 20
Co porphyrin Paenibacillus azotofixans HCOOH 1.4 × 10−14 mol/(h·cell) 2.25 48 h 84
CdS M. barkeri CH4 0.19 μmol/h 0.34 5 d 85
NiCu@CdS M. barkeri CH4 9.5 mmol/gcat 12.41 ± 0.16 5 d 43
NCNCNx M. barkeri CH4 341.8 ± 15.7 μmol/gcat 50.3 20 d 61
PFODTBT RH16 PHB 21.3 ± 3.8 mg/(L·d) 2.27 2 d 70
CdTe QDs X. autotrophicus Biomass 60.5 mgCO2/(L·d) 47.2 ± 7.3 4 d 13

*dcw represents cell dry weight, cat indicates catalyst

The methanogen M. barkeri can utilize CO2 and H2 for CH4 synthesis, but its energy conversion efficiency is relatively low and the synthesis rate of CH4 is slow[61,86]. Ye et al.[85] constructed an M. barkeri-CdS hybrid by precipitating CdS on the surface of M. barkeri, which was the first to achieve light-driven conversion of CO2 to CH4 using a whole-cell hybrid. However, the hydrogen production rate of the semiconductor far exceeded the metabolic rate of M. barkeri, leading to significant accumulation of H2 and reducing the CH4 yield and quantum efficiency (only 0.19 μmol/h and 0.34%). Subsequently, Ye et al.[43] further loaded NiCu alloy and CdS nanoparticles sequentially on the surface of M. barkeri (Fig. 4B), suppressing hydrogen production at the bio-inorganic interface through the dual active sites of NiCu, and enhancing CH4 production and the quantum efficiency of the semiconductor (9.5 mmol/gcat and 12.41% ± 0.16%) via extracellular and intracellular hydrogen cycling in M. barkeri.
Moreover, whole-cell hybrids can also achieve the transformation of CO2 into high-value chemicals such as formic acid (HCOOH) and poly-β-hydroxybutyrate (PHB)[87], further expanding the future application prospects of whole-cell hybrids. Yu et al.[70] used organic semiconductor polymer dots (PFODTBT) as photosensitizers to construct a hybrid with Ralstonia eutropha H16 (RH16) and the electron shuttle neutral red (Figure 4C). The photogenerated electrons produced by PFODTBT after excitation increased the proportion of NADPH in RH16 through neutral red, driving the Calvin cycle for PHB synthesis. The PHB yield of this hybrid was 21.3 ± 3.78 mg/L, which is nearly three times higher than that of RH16 alone.

5.2 Artificial Nitrogen Fixation

At present, artificial nitrogen fixation mainly adopts the Haber-Bosch process, that is, N2 and hydrogen (H2) react on an iron catalyst to produce ammonia at high temperature and high pressure[88,89]. The Haber-Bosch process has strongly promoted the development of artificial nitrogen fixation over the past century, but it also consumes 1%~2% of the total global energy production, accounts for 3%~5% of the world's natural gas production, and generates 1%~3% of CO2 emissions[90⇓-92]. Therefore, it is urgent to develop a greener nitrogen fixation technology. Biological nitrogen fixation can achieve ammonia synthesis under mild conditions and is one of the promising green nitrogen fixation technologies. However, the rate of Pi release from ATP hydrolysis by microorganisms themselves is relatively slow (25~27 s-1), which cannot meet the energy demand of the biological nitrogen fixation process[50].
Studies have shown that semiconductors can replace Fe protein to transfer electrons to MoFe protein, and the photogenerated electrons produced by semiconductors can directly induce MoFe protein for nitrogen fixation (Figure 5A)[93]. However, since nitrogenase, Fe protein, and MoFe protein will quickly become inactive under aerobic conditions[50], the direct semiconductor-enzyme approach will reduce the stability of artificial nitrogen fixation. By precipitating CdS nanoparticles on the surface of Rhodopseudomonas palustris (R. palustris), Wang et al.[39] achieved for the first time a whole-cell hybrid-mediated photo-driven artificial nitrogen fixation and improved nitrogenase activity through the photogenerated electrons of CdS. The photogenerated electrons of CdS under visible light irradiation can combine with the photosynthetic electron transport chain of R. palustris, transferring via ferredoxin and NADP+ oxidoreductase to nitrogenase and NADP+, ultimately generating more reducing power within the cell. Compared to R. palustris, the R. palustris-CdS hybrid can increase biomass production by 153%, with a quantum efficiency of 6.73%. Koh et al.[50] further constructed a whole-cell hybrid by internalizing InP/ZnSe quantum dots in the nitrogen-fixing bacterium A. vinelandii. Compared to A. vinelandii, the ammonia (NH3) production inside the cells of this hybrid can be increased more than fivefold under light (400 nm, 18 W). Theoretical predictions based on the electron transfer cycle of nitrogenase and experimental results also indicate that photogenerated electrons can directly transfer from intracellular InP/ZnSe quantum dots to MoFe protein, reducing MoFe protein while promoting the electron transfer cycle between Fe protein and MoFe protein[50]. Additionally, conjugated oligoelectrolytes (COE-IC)[59], PFP[68], and other semiconductors can also form hybrids with nitrogen-fixing bacteria, thereby enhancing microbial nitrogen fixation ability (Figure 5B) (Table 4).
图5 全细胞杂合体固氮机理及示意图：（A）半导体光生电子向MoFe蛋白转移示意图[50]；（B）A. vinelandii-COE-IC杂合体[59]；（C）单一全细胞杂合体和（D）多个全细胞杂合体联用同步CO2和N2固定示意图[13,31]

Fig. 5 Nitrogen fixation mechanism and diagram of whole-cell biohybrids. (A) The illustration of the transfer of photogenerated electrons from semiconductor to MoFe protein[50]; (B) schematic diagram of A.vinelandii-COE-IC biohybrid[59]; schematics of single whole-cell biohybrids (C)and multiple whole-cell biohybrids (D) for synchronized CO2 and N2 fixation[13,31]

表4 全细胞杂合体在人工固氮中的应用进展及性能对比

Table 4 The application progress and performance comparison of whole-cell hybrids in artificial nitrogen fixation

Semiconductors Microbes Products Product yields QY (%) Operation time ref
CdS R. palustris Biomass 0.25 × 109 cell/(mL·d) 6.73 120 h 39
CdTe QDs X. autotrophicus Biomass 3.85 mgN/(L·d) 7.1 ± 1.1 4 d 13
InP/ZnSe QDs A. vinelandii NH3 4.6 × 107 mol NH4+/mol CFUinitial - 8 h 50
COE-IC A. vinelandii NH3 1.47 nmol/(mL·h) - 24 h 59
Poly(fluorene-alt-phenylene) A. Chroococcum NH3
L-amino acids		 0.215 μg/(109 cell·d)
0.725 nmol/(109·cell d)		 0.83 48 h 68
PFP Synechocystis sp.-PFP
R. palustris		 γ-PGA 14.42mg/(L·d) 1.43 10 d 31
In recent years, the synergistic fixation of CO2 and N2 through the combined use of single or multiple whole-cell hybrids has gradually gained attention[13,31]. Guan et al.[13] constructed a hybrid of Xanthobacter autotrophicus (X. autotrophicus)-CdTe QDs (Fig. 5C), achieving the synergistic fixation of CO2 and N2. The quantum efficiencies of light-driven CO2 and N2 fixation reached 47.2 % ± 7.3 % and 7.1 % ± 1.1 %, respectively, surpassing the theoretical limits of biochemical pathways (46.1 % and 6.9 %). Yu et al.[31] constructed an artificial symbiosis system integrating CO2 conversion, nitrogen fixation, and biopolymer synthesis by combining two whole-cell hybrids: Synechocystis sp.-PFP and R. palustris-PFP. This system achieved light-driven synthesis of γ-polyglutamic acid (γ-PGA) from CO2 and N2, increasing its yield by 104 % and significantly enhancing the selectivity (from 36 % to 64 %) and productivity (quantum efficiency from 0.71 % to 1.43 %) in natural peptide synthesis (Fig. 5D).

5.3 Hydrogen Production

Hydrogen energy possesses the advantages of zero carbon emissions, high conversion efficiency, and high energy density; thus, H2 is considered an ideal energy carrier[94]. Current hydrogen production technologies still mainly rely on fossil fuels, while efficient hydrogen production utilizing solar energy can provide a sustainable solution for global carbon neutrality[95,96]. Hydrogenases within microbial cells act as catalysts that can highly specifically catalyze the transfer of electrons and protons to generate H2[29]. Under ambient temperature and normal pressure, microorganisms can produce hydrogen by merely utilizing organic substances (e.g., glucose, starch, glycerol) or through photosynthesis[60]. However, the efficiency of microbial hydrogen production remains relatively low, primarily limited by the low substrate conversion rate of microorganisms and unstable environmental factors (e.g., heavy metal ions, sulfates)[97]. Currently, light-driven bio-hydrogen production based on fully hybrid systems has become one of the most promising strategies for efficient hydrogen production[60,98] (Table 5).
表5 全细胞杂合体在制氢中的应用进展及性能对比

Table 5 The application progress and performance comparison of whole-cell hybrids in hydrogen production

Semiconductors Microbes H2 yields QY (%) Operation time ref
TiO2 E. coli - 31.2 > 400 min 27
CdS E. coli - 0.1 6 h 99
I-HTCC E. coli ~0.7 mmol/h 9.11 9 h 71
CdSxSe1-x E. coli 70.2 μmol/108 cells 27.56 48 h 47
C3N4 QDs E. coli 7800 ± 12 μmol/(gdcw·h) - 50 h 60
TiO2−x E. coli 0.42 mmol/h - 3 h 100
CdS E. coli BL21 0.52 ± 0.01 mmol/(108 cells·d) - 96 h 101
Cu2O/reduced graphene oxide S. oneidensis MR-1 80.5 μmol/(gCu2O·h) - 4 h 48
CuInS2/ZnS QDs S. oneidensis MR-1 56.64μmol/h 15.02 45 h 51
CdS S. oneidensis MR-1 5.03 μmol/mg - 72 h 40
CdSe QDs S. oneidensis MR-1 75.65 μmol/h 0.17 ± 0.05 350 h 29
CdS S. oneidensis 6.71 μmol/(gdcw·h) 6.2 70 h 44
CdS@Fe3O4 S. oneidensis 17.45 μmol/(gdcw·h) 11.5 70 h 44
CdS Desulfo vibrio desulfuricans 418 μmol/(gdcw·h) 23 100 h 98
CdS Desulfo vibrio desulfuricans 36 μmol/(gdcw·h) 4 10 d 98
OF/PTP R. palustris 1.25 μmol/h - 2 h 67
Au nanoparticles C. butyricum 5.67 mL/(L·h) 19.31 168 h 54
CdS Rhodospirillum rubrum 240 μmol/(OD600·d) 0.17 5 d 102
As early as 1987, Krasnovsky and Nikandrov[103] first demonstrated that the photogenerated electrons of TiO2 could be transferred via methyl viologen to Clostridium butyricum (C. butyricum) for hydrogen production. Honda et al.[27] constructed a recombinant strain of E. coli expressing [FeFe] hydrogenase from C. butyricum, which produced hydrogen by transferring photogenerated electrons of TiO2 through methyl viologen, achieving a quantum efficiency of 31.2% under irradiation at a wavelength of 350 nm. Wei et al.[101] constructed a whole-cell hybrid for hydrogen production by in-situ depositing CdS nanoparticles on the outer membrane of engineered E. coli BL21, achieving a hydrogen production of 81.80 ± 7.39 μmol in 24 hours. Considering the potential cytotoxicity and photocorrosion of inorganic semiconductors, it is necessary to explore safer and more efficient photosensitive semiconductors to improve the efficiency and stability of whole-cell hybrids. Xiao et al.[71] combined iodine-doped hydrothermal carbonized nitrogen (I-HTCC) with E. coli. Under visible light irradiation at 700 nm, the hydrogen production rate of this hybrid approached 0.7 mmol/h, with a quantum efficiency of 9.11%. To enhance the interaction between photogenerated electrons and hydrogenase, Wu et al.[60] utilized E. coli to internalize C3N4 QDs, forming a C3N4 QDs/NAD+ junction within E. coli through π-π electron conjugation, which promoted the separation of photogenerated electrons. The hydrogen production rate of this hybrid reached up to 7800 ± 12 μmol/(gdcw·h), the highest reported hydrogen production rate for whole-cell hybrids, and no decline in hydrogen production activity was observed over 50 hours of light/dark cycling.
表6 全细胞杂合体在污染物去除及资源化中的应用进展及性能对比

Table 6 The application progress and performance comparison of whole-cell hybrids in pollutants removal and recovery

Semiconductors Microbes Pollutants Removal efficiencies Operation time ref
Bi12O17Cl2 coated carrier Sludge cultured by oxytetracycline-containing wastewater Oxytetracycline, 10 mg/L 94% 400 h 105
BiVO4/FeOOH Sludge cultured by pyridine-containing wastewater Pyridine, 150 mg/L 100% 48 h 118
Ag3PO4 S. oneidensis MR-1 Rhodamine B, 15 mg/L 100% 7 d 34
CdS S. oneidensis MR-1 Direct blue 71, 100 mg/L 100% 5 h 119
CdS/g-C3N4 S. oneidensis MR-1 Acid orange7, 15 mg/L 100% 120 min 36
Ag2S QDs E. coli Methylene blue, 20 mg/L 70.8% 100 min 120
CdS Clostridium thermocellum Methyl violet, 100 mg/L 100% 30 min 121
CdS Clostridium thermocellum Crystal violet, 100 mg/L 99.6% 30 min 121
CdS Clostridium thermocellum Malachite green, 100 mg/L 100% 20 min 121
CDPCN M. barkeri Poly(lactic acid), 50 mg/mL CH4 yield of 9.39 mmol/gcat and CH4 selectivity of 99.1% 120 d 69
CdS T. denitrificans Nitrate, 14 mgN/L 72.1% ± 1.1% 68 h 111
CdS@Mn3O4 T. denitrificans Nitrate, 8 mgN/L 100% 18 h 109
Anthraquinone-2-Sulfonate T. denitrificans Nitrate, 7 mgN/L 100% 10 h 122
Suwannee River natural organic matter (2R101N) T. denitrificans Nitrate, 2~40 mgN/L 4.7 ± 0.9 μg/(L·h·109 cell) 12 h 113
CdSexS1-x QDs P. aeruginosa Nitrate, 1 mM 97.1% 5 d 79
CdS Anammox bacteria Nitrate, 10 mgN/L 88% 12 h 26
g-C3N4 Anammox bacteria Ammonia and total nitrogen 100 % and 94.25 % 100 d 123
CdS S. oneidensis Cr(VI), 25 mg/L 100% 450 min 107
NH2-doped carbon dots S. oneidensis MR-1 Cr(VI), 50 mg/L 100% 72 h 124
Moreover, in different whole-cell hybrids, the photogenerated electrons used for hydrogen production also exhibit two distinct transfer pathways (Fig. 6). In the S. oneidensis MR-1-CdS hybrid, the photogenerated electrons from CdS can reverse the extracellular electron transfer chain of S. oneidensis MR-1, achieving photoactivation of hydrogenase and thereby enhancing hydrogen production capability (Fig. 6A)[40]. In contrast, in the S. oneidensis MR-1-CdSe hybrid, researchers utilized the extracellular electron transfer of S. oneidensis MR-1 to fill the photogenerated holes in CdSe, effectively preventing hole-electron recombination while using the photogenerated electrons from CdSe to complete the hydrogen evolution reaction, achieving visible-light-driven sustainable hydrogen production (Fig. 6B)[29]. To further enhance the hydrogen production efficiency of whole-cell hybrids, electron carriers (such as methyl viologen, reduced graphene oxide, etc.) can be introduced at the semiconductor-microbe interface or semiconductors can be incorporated intracellularly to shorten the transfer distance of photogenerated electrons to hydrogenase[47-48,60].
图6 不同光生电子转移途径下的全细胞杂合体制氢机理示意图[29,40]

Fig. 6 The mechanism of hydrogen production by whole-cell biohybrids under different photogenerated electron transfer pathways[29,40]

Currently, the hydrogen production efficiency of existing whole-cell hybrids is still relatively low. In the future, the metabolic pathways for microbial hydrogen production should be further optimized to enhance the efficiency and yield of H2 generation while reducing by-product formation and improving system stability and controllability. For practical applications, whole-cell hybrids capable of working efficiently in complex substrate mixtures should be developed. Additionally, exploring a wider variety of substrates (such as waste materials, biomass, etc.) as electron donors for whole-cell hybrids can improve resource utilization efficiency and sustainability.

5.4 Pollutant Removal and Resource Recovery

The use of microorganisms for pollutant removal and resource recovery has the advantages of low cost and environmental friendliness, but the large number of electron donors required by microorganisms also increases operating costs and the risk of secondary pollution[104]. The concept of coupling photocatalysis with microorganisms for efficient pollutant degradation was first proposed by Ding et al.[105]. By preparing carrier fillers loaded with Bi12O17Cl2, their team achieved stable electron transfer between the photogenerated electrons in Bi12O17Cl2 and microorganisms under visible light irradiation. Over 400 hours of operation, the degradation rate of oxytetracycline (OTC) remained above 94%, and both pollutant removal efficiency and operational stability outperformed single photocatalysis or biodegradation alone. In recent years, with the continuous development of whole-cell hybrids, an increasing number of such hybrids have been applied to the removal and resource recovery of pollutants (e.g., dyes, nitrates, heavy metals, microplastics, etc.) (Figure 7), with the aim of achieving highly efficient and low-carbon removal and resource recovery of pollutants[26,69,79,106⇓-108].
图7 全细胞杂合体在污染物去除及资源化中的应用及机理示意图。（A）利用V. natriegens -CdS杂合体实现有机污染物资源化[110]；（B）T. denitrificans-CdS杂合体去除硝酸盐并生成氧化亚氮[116]；（C）M. barkeri-CDPCN杂合体将微塑料转化为CH4甲烷[69]；（D）S. oneidensis-CdS杂合体还原Cr(VI)[107]

Fig. 7 The application and mechanism of whole-cell biohybrids in pollutants removal and resource recovery. (A) Utilization of V. natriegens-CdS biohybrid for the resource recovery of organic pollutants[110]; (B) nitrate removal and nitrous oxide production by T. denitrificans -CdS biohybrid[116]; (C) the conversion of microplastics into methane via M. barkeri-CDPCN biohybrids[69]; (D) Reduction of Cr(VI) by S.oneidensis-CdS biohybrids[107]

The removal of contaminants by whole-cell hybrids can be divided into two modes. First, microorganisms utilize photogenerated electrons to drive contaminant removal, while the photogenerated holes are filled by external electron donors[79,109]. For instance, by introducing an aerobic sulfate reduction pathway (Fig. 7A) into Vibrio natriegens (V. natriegens), it enables the utilization of Cd2+ and SO42- in wastewater (glycerol wastewater, electroplating wastewater, starch wastewater, etc.) to synthesize CdS nanoparticles. Further exposure to light allows V. natriegens to use photogenerated electrons to convert organic pollutants in the wastewater into 2,3-butanediol[110]. Additionally, Thiobacillus denitrificans (T. denitrificans) can use the photogenerated electrons from CdS to reduce nitrate to nitrous oxide, which is an emerging energy substance whose efficient conversion and recovery are of great significance (Fig. 7B)[111]. Sacrificial agents are indispensable electron donors for maintaining the stable operation of reactions in whole-cell hybrids; thus, finding inexpensive and readily available sacrificial agents as alternatives to expensive chemical sacrificial agents is of great importance. Ye et al.[69] constructed a whole-cell hybrid for photoelectrochemical methane production using the model methanogenic strain M. barkeri and CDPCN, demonstrating that microplastics can serve as sacrificial agents to achieve highly efficient methane resource recovery from microplastics, with a methane yield of 9.39 mmol/gcat and a methane selectivity greater than 99% (Fig. 7C).
Secondly, microorganisms can also fill the photogenerated holes of semiconductors through extracellular electron transfer, thereby driving the photogenerated electrons to complete the removal of pollutants[112]. Xiao et al.[34] established a hybrid composed of electroactive bacteria S. oneidensis MR-1 and Ag3PO4 under anaerobic conditions, where S. oneidensis MR-1 can fill the photogenerated holes of Ag3PO4 through extracellular electron transfer, thus driving the separation of photogenerated electrons to achieve the degradation of rhodamine B. In the Cr(Ⅵ) removal by the S.oneidensis-CdS hybrid, the CdS on the surface of S.oneidensis can directly or indirectly transfer the photogenerated electrons to Cr(Ⅵ) for removal via microbial extracellular polymeric substances, meanwhile, the photogenerated electrons produced by CdS inside S.oneidensis can also promote the reduction of Cr(Ⅵ) through microbial extracellular electron transfer pathways (Fig. 7D)[107]. In nature, researchers have also found that natural photosensitive semiconductors (such as humic acid and chlorophyll, etc.) can transfer electrons to microorganisms (such as T. denitrificans and Raphidocelis subcapitata, etc.) under light to promote the migration and transformation of pollutants (such as nitrate, etc.)[113⇓-115], which also provides new insights into understanding the geochemical cycle of pollutants.
However, most current research on the removal of contaminants using whole-cell hybrids focuses on single pollutants and remains at the laboratory scale. It is worth paying attention to how to use various metal ions in actual wastewater for in-situ synthesis of semiconductors both inside and outside microbial cells while avoiding heavy metal toxicity inhibition on microorganisms. Meanwhile, in complex environments with multiple coexisting pollutants, the contaminant removal efficiency of whole-cell hybrids and the potential photochemical transformation of pollutants (such as the photolysis of nitrate to produce NO·, HO· and other radicals) still need further exploration[117].

6 Environmental Impact and Challenges of Whole-Cell Hybrids

Although the research history of whole-cell hybrids is relatively short, as an emerging research direction, it has shown broad application prospects in the high-value transformation of CO2, artificial nitrogen fixation, clean energy production, pollutant removal and resource utilization, providing new concepts and methods for global mitigation of the energy crisis and CO2 emission reduction[18]. However, there are still many potential environmental impacts and challenges for whole-cell hybrids in practical applications.
Firstly, the construction of whole-cell hybrids is greatly limited by application scenarios and costs. Only a few microorganisms have been reported to achieve in-situ semiconductor self-synthesis (such as CdS, CdSe, etc.)[15,79], but the types and ratios of matrix ions required for this process may not be available in the actual environment, which might affect the types and performance of the synthesized semiconductors. In the laboratory research phase, although the method of constructing whole-cell hybrids with externally added semiconductors and sacrificial agents has achieved good results, the high cost and stringent material preparation process also limit further promotion and application[18].
Secondly, the management and recycling of semiconductor materials increase the application difficulty of whole-cell hybrids. During operation, the detachment of inorganic semiconductors from the microbial surface and the photocorrosion of inorganic semiconductors may lead to the residue of heavy metal ions in downstream products, which increases the ecological risk of whole-cell hybrid applications[32,75]. Although it has been reported that photosensitizers can achieve close binding with the microbial surface through surface functionalization by making them positively charged and enhancing hydrophobicity[38,100], whether the photosensitizers can be reused and recycled after the decline of microorganisms is also a challenge for the future.
Finally, the complex operating conditions in real environments will reduce the performance of whole-cell hybrids. Compared with simulated wastewater (99.8%), the nitrate removal rates of P. aeruginosa-CdSexS1-x QDs hybrids when treating actual municipal sewage, aquaculture wastewater, and electroplating wastewater dropped to 73.5%, 82.8%, and 62.6%, respectively, which may be related to insufficient organics or high salinity inhibiting microbial activity in real wastewater[79]. Therefore, subsequent research should focus on addressing potential problems existing in real environments (such as load shocks, light intensity fluctuations, temperature changes, etc.) to achieve the industrial application of whole-cell hybrids as soon as possible.

7 Conclusion and Prospect

The efficient utilization of solar energy is a sustainable path to address global energy and environmental crises and achieve the sustainable development of human society. The proposal and development of whole-cell hybrids are of great significance for realizing the high-value transformation of CO2, clean energy production, and green and efficient treatment of pollutants. This article reviews the research progress of whole-cell hybrids, covering their working principles and advantages, semiconductor materials, hybrid construction mechanisms, and current application research status. It also discusses the potential environmental impacts and challenges of whole-cell hybrids, aiming to provide references for subsequent research and applications. Currently, the study of whole-cell hybrids is still in its infancy, and several issues remain to be further addressed.
(1) Develop green and efficient, highly biocompatible, and high quantum efficiency inorganic and organic semiconductors. The bandgap range of semiconductors can be precisely designed and regulated through interface engineering strategies such as co-doping, defect engineering, sensitization, and constructing heterojunctions, broadening their absorption range in visible light and infrared light. At the same time, strengthen the design and development of semiconductors using water as an electron donor and develop inexpensive and readily available sacrificial agents to reduce the cost of adding exogenous electron donors.
(2) Functional modification of microorganisms using synthetic biology and genetic engineering techniques to enhance their photogenerated electron transfer capability, optimize their metabolic pathways, and expand their biocatalytic ability, with the aim of improving the solar energy conversion efficiency of whole-cell hybrids.
(3) Clarify the interfacial interaction between semiconductors and microorganisms, achieve precise control over the binding of semiconductors and microorganisms in designated areas, thereby enabling efficient transfer of photogenerated electrons. Strengthen the exploration of the mechanisms of generation, transfer, and conversion of photogenerated electrons in whole-cell hybrids, and develop technologies such as in-situ electrochemistry or in-situ spectroscopy to monitor enhanced interfacial electron transfer, providing theoretical support for the efficient operation of whole-cell hybrids.
(4) To carry out research on the combination of multiple whole-cell hybrids and the assembly of artificial communities, which can utilize the metabolic differences of different microorganisms for different substrates to maintain the stable operation of the system, and is expected to achieve light-driven synthesis of higher-value complex chemicals, contributing to the sustainable development of biomanufacturing.
(5) Promote the expanded research of whole-cell hybrids. Currently, the operational efficiency and reaction mechanisms of whole-cell hybrids mainly come from laboratory studies. In the future, corresponding research should be conducted to address potential problems in real environments, such as reactor design and exploring operational efficiency under complex conditions, in order to accelerate the industrial application process of whole-cell hybrids.

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