Supramolecular Assembly of Photosystem II and Adenosine Triphosphate Synthase in Artificially Designed Honeycomb Multilayers for Photophosphorylation.

Plant thylakoids have a typical stacking structure, which is the site of photosynthesis, including light-harvesting, water-splitting, and adenosine triphosphate (ATP) production. This stacking structure plays a key role in exchange of substances with extremely high efficiency and minimum energy consumption through photosynthesis. Herein we report an artificially designed honeycomb multilayer for photophosphorylation. To mimic the natural thylakoid stacking structure, the multilayered photosystem II (PSII)-ATP synthase-liposome system is fabricated via layer-by-layer (LbL) assembly, allowing the three-dimensional distributions of PSII and ATP synthase. Under light illumination, PSII splits water into protons and generates a proton gradient for ATP synthase to produce ATP. Moreover, it is found that the ATP production is extremely associated with the numbers of PSII layers. With such a multilayer structure assembled via LbL, one can better understand the mechanism of PSII and ATP synthase integrated in one system, mimicking the photosynthetic grana structure. On the other hand, such an assembled system can be considered to improve the photophosphorylation.

[1]  Paola Turina,et al.  H+/ATP ratio of proton transport‐coupled ATP synthesis and hydrolysis catalysed by CF0F1—liposomes , 2003, The EMBO journal.

[2]  A. Waas,et al.  Abiotic tooth enamel , 2017, Nature.

[3]  H. Möhwald,et al.  25th Anniversary Article: Dynamic Interfaces for Responsive Encapsulation Systems , 2013, Advanced materials.

[4]  Bao-Lian Su,et al.  Bio-inspired Murray materials for mass transfer and activity , 2017, Nature Communications.

[5]  D. Cosgrove.  Growth of the plant cell wall , 2005, Nature Reviews Molecular Cell Biology.

[6]  P. Leeuwen,et al.  Rapid and simple isolation of pure photosystem II core and reaction center particles from spinach , 1991, Photosynthesis Research.

[7]  Can Li,et al.  Water Oxidation Mechanism on Alkaline-Earth-Cation Containing Birnessite-Like Manganese Oxides , 2015 .

[8]  Jian-Ren Shen,et al.  Direct electron transfer from photosystem II to hematite in a hybrid photoelectrochemical cell. , 2015, Chemical communications.

[9]  Can Li,et al.  Biomimetic electron transport via multiredox shuttles from photosystem II to a photoelectrochemical cell for solar water splitting , 2017 .

[10]  Chun H. Wang,et al.  Micropatterning of Proteins on 3D Porous Polymer Film Fabricated by Using the Breath‐Figure Method , 2007 .

[11]  Can Li,et al.  Spatially Separated Photosystem II and a Silicon Photoelectrochemical Cell for Overall Water Splitting: A Natural-Artificial Photosynthetic Hybrid. , 2016, Angewandte Chemie.

[12]  G. Schoehn,et al.  Plastid thylakoid architecture optimizes photosynthesis in diatoms , 2017, Nature Communications.

[13]  Vincent Artero,et al.  Artificial Photosynthesis: From Molecular Catalysts for Light‐driven Water Splitting to Photoelectrochemical Cells , 2011, Photochemistry and photobiology.

[14]  H. Möhwald,et al.  Mimicking Primitive Photobacteria: Sustainable Hydrogen Evolution Based on Peptide-Porphyrin Co-Assemblies with a Self-Mineralized Reaction Center. , 2016, Angewandte Chemie.

[15]  Nathan Nelson,et al.  Structure and function of photosystems I and II. , 2006, Annual review of plant biology.

[16]  Qiang He,et al.  Adenosine triphosphate biosynthesis catalyzed by FoF1 ATP synthase assembled in polymer microcapsules. , 2007, Angewandte Chemie.

[17]  R. Yegani,et al.  Performance evaluation and antifouling analyses of cellulose acetate/nanodiamond nanocomposite membranes in water treatment , 2017 .

[18]  Z. Li,et al.  Crucial Roles of Electron-Proton Transport Relay in the Photosystem II-Photocatalytic Hybrid System for Overall Water Splitting , 2017 .

[19]  Helmuth Möhwald,et al.  Redox-controlled molecular permeability of composite-wall microcapsules , 2006, Nature materials.

[20]  D. P. O'Neal,et al.  Layer-by-Layer-Coated Gelatin Nanoparticles as a Vehicle for Delivery of Natural Polyphenols. , 2009, ACS nano.

[21]  Zhengu Chen,et al.  Highly active water oxidation on nanostructured biomimetic calcium manganese oxide catalysts , 2016 .

[22]  Christopher Hein,et al.  High-speed atomic force microscopy reveals rotary catalysis of rotor-less F 1 -ATPase , 2011 .

[23]  Kazuhiko Kinosita,et al.  Direct observation of the rotation of F1-ATPase , 1997, Nature.

[24]  J. Fei,et al.  Coassembly of Photosystem II and ATPase as Artificial Chloroplast for Light-Driven ATP Synthesis. , 2016, ACS nano.

[25]  Can Li,et al.  Achieving solar overall water splitting with hybrid photosystems of photosystem II and artificial photocatalysts , 2014, Nature Communications.

[26]  Xuehai Yan,et al.  Trace Solvent as a Predominant Factor To Tune Dipeptide Self-Assembly. , 2016, ACS nano.

[27]  Egbert J Boekema,et al.  Supramolecular organization of thylakoid membrane proteins in green plants. , 2005, Biochimica et biophysica acta.

[28]  F. Longobardi,et al.  Photosystem II based multilayers obtained by electrostatic layer-by-layer assembly on quartz substrates , 2014, Journal of Bioenergetics and Biomembranes.

[29]  A G Leslie,et al.  Molecular architecture of the rotary motor in ATP synthase. , 1999, Science.

[30]  Yue Cui,et al.  Motor Protein CF0F1 Reconstituted in Lipid‐Coated Hemoglobin Microcapsules for ATP Synthesis , 2008 .

[31]  U. Bunz,et al.  Breath Figures as a Dynamic Templating Method for Polymers and Nanomaterials , 2006 .

[32]  Shinichiro Nakamura,et al.  Theoretical study on the role of Ca(2+) at the S2 state in photosystem II. , 2014, The journal of physical chemistry. B.

[33]  Hongmin Ma,et al.  Ordered patterns and structures via interfacial self-assembly: superlattices, honeycomb structures and coffee rings. , 2011, Chemical Society reviews.

[34]  H. Möhwald,et al.  Application of Inhibitor‐Loaded Halloysite Nanotubes in Active Anti‐Corrosive Coatings , 2009 .

[35]  Katsuhiko Ariga,et al.  Enzyme nanoarchitectonics: organization and device application. , 2013, Chemical Society reviews.

[36]  Katsuhiko Ariga,et al.  Nanoarchitectonics for Dynamic Functional Materials from Atomic‐/Molecular‐Level Manipulation to Macroscopic Action , 2016, Advanced materials.