Photosystem II-based biomimetic assembly for enhanced photosynthesis

Abstract

Photosystem II (PSII) is a fascinating photosynthesis-involved enzyme, participating in sunlight-harvest, water splitting, oxygen release, and proton/electron generation and transfer. Scientists have been inspired to couple PSII with synthetic hierarchical structures via biomimetic assembly, facilitating attainment of natural photosynthesis processes, such as photocatalytic water splitting, electron transfer and ATP synthesis, in vivo. In the past decade, there has been significant progress in PSII-based biomimetic systems, such as artificial chloroplasts and photoelectrochemical cells. The biomimetic assembly approach helps PSII gather functions and properties from synthetic materials, resulting in a complex with partly natural and partly synthetic components. PSII-based biomimetic assembly offers opportunities to forward semi-biohybrid research and synchronously inspire optimization of artificial light-harvest micro/nanodevices. This review summarizes recent studies on how PSII combines with artificial structures via molecular assembly and highlights PSII-based semi-natural biosystems which arise from synthetic parts and natural components. Moreover, we discuss the challenges and remaining problems for PSII-based systems and the outlook for their development and applications. We believe this topic provides inspiration for rational designs to develop biomimetic PSII-based semi-natural devices and further reveal the secrets of energy conversion within natural photosynthesis from the molecular level.

Keywords: artificial chloroplast; biomimetic assembly; photoelectrobiological chemistry; photosynthesis; photosystem II.

Figure 1.

Schematic structure and function of PSII. (a) Structure of PSII. (b) Chemical structure of oxygen-evolving complex (OEC). (c) The current model of ‘kok’ cycle. (d) The ‘self-repair circle’ of PSII. Reprinted with permission from Ref. [26], Copyright 2019, National Academy of Sciences.

Figure 2.

PSII-based biomimetic structures. (a) PSII couples with ATPase and proteorhodopsin (PR) into the membrane of a lipid vesicle. (b) PSII assembles in the polymeric multilayer films via a layer-by-layer assembly process. (c) The PSII-particle conjugates: PSII anchors on the surface of the particle. (d) The PSII-enriched particle with an ATPase-lipid coating.

Figure 3.

Electron transfer systems based on photosystem proteins range from PSI, PSII to PSI-PSII. (a) PSI-anchored Au or Pt nanoparticles for hydrogen production. (b) PSI-enriched multilayer films for photocurrent production. (c) PSII pairs with hydrogenase for photoelectrochemical water splitting. (d) PPyBQ nanowire-supported PSII-enriched membrane as a photoanode to generate photocurrent. (e) Full Z-scheme mimic strategy using PSI-based photocathode and a PSII-based photoanode to generate electrical energy. Reprinted with permission from Ref. [78], Copyright 2015, Wiley-VCH. (f) Bias-free water splitting system comprises multilayered PSII/PSI as PBV²⁺/PSI/PBQ/PSII. Reprinted with permission from Ref. [79], Copyright 2013, Wiley-VCH.

Figure 4.

Semi-artificial chloroplast systems with the combination of PSII and ATPase for in vitro ATP synthesis. (a) An artificial chloroplast microparticle based on coassembly of PSII and ATPase for light-activated ATP synthesis. Confocal laser scanning microscope image of PSII-microparticle with ATPase-liposome coating: (i) chlorophylls in PSII (green light); (ii) Texas red-labeled proteoliposomes (red light); (iii) overlay image. Reprinted with permission from Ref. [13], Copyright 2016, American Chemical Society. (b) The artificial protocellular system is made of a giant vesicle containing ATPase and two photoconverters (plant-derived PSII and bacteria-derived PR). Red light facilitates PSII to generate proton for driving ATP synthesis, while green light impedes ATP synthesis by PR-depleting protons. (c) 3D distribution of PSII and ATPase in an artificial honeycomb multilayer to imitate natural thylakoid structure for light-activated ATP synthesis. (d) A polymeric structure with hierarchical and compartmentalized features for enhanced ATP synthesis.

Figure 5.

Biointerfacing engineering for biomimicking-chloroplasts through QDs modification. (a) Two fluorescent polymeric nanoparticles, PFP-NPs and PFBT-NPs, are used to coat on the surface of natural chloroplast to accelerate electron transfer via additional light absorption supply from UV light. (b) A couple of QDs, CuInS₂/ZnS, is served as an optical converter that changes UV light to the 680 nm red light for optical absorption of PSII in chloroplast to enhance photophosphorylation. Reprinted with permission from Ref. [17], Copyright 2018, Wiley-VCH. (c) Long-lived photoacid molecule (merocyanine, MEH) into natural chloroplast for generating a stable supply of protons. The insets: (i) time-dependent pH of MEH; (ii) SP aqueous solution; (iii) ATP production. Reprinted with permission from Ref. [90], Copyright 2017, Wiley-VCH.