Research Article: Primitive Photosynthetic Architectures Based on Self‐Organization and Chemical Evolution of Amino Acids and Metal Ions

Date Published: March 09, 2018

Publisher: John Wiley and Sons Inc.

Author(s): Kai Liu, Xiaokang Ren, Jianxuan Sun, Qianli Zou, Xuehai Yan.


The emergence of light‐energy‐utilizing metabolism is likely to be a critical milestone in prebiotic chemistry and the origin of life. However, how the primitive pigment is spontaneously generated still remains unknown. Herein, a primitive pigment model based on adaptive self‐organization of amino acids (Cystine, Cys) and metal ions (zinc ion, Zn2+) followed by chemical evolution under hydrothermal conditions is developed. The resulting hybrid microspheres are composed of radially aligned cystine/zinc (Cys/Zn) assembly decorated with carbonate‐doped zinc sulfide (C‐ZnS) nanocrystals. The part of C‐ZnS can work as a light‐harvesting antenna to capture ultraviolet and visible light, and use it in various photochemical reactions, including hydrogen (H2) evolution, carbon dioxide (CO2) photoreduction, and reduction of nicotinamide adenine dinucleotide (NAD+) to nicotinamide adenine dinucleotide hydride (NADH). Additionally, guest molecules (e.g., glutamate dehydrogenase, GDH) can be encapsulated within the hierarchical Cys/Zn framework, which facilitates sustainable photoenzymatic synthesis of glutamate. This study helps deepen insight into the emergent functionality (conversion of light energy) and complexity (hierarchical architecture) from interaction and reaction of prebiotic molecules. The primitive pigment model is also promising to work as an artificial photosynthetic microreactor.

Partial Text

Sunlight is the most ubiquitous and reliable energy source on earth, which fuels the origin and evolution of life.1 Photochemical reactions may have played an important role in abiotically generating high‐energy chemical bonds to enhance molecular complexity.2 Contemporary phototrophic organisms have developed pigment (e.g., chlorophyll (Chl))–protein complexes to capture light and generate reducing energy for carbon dioxide fixation.3 Utilization of light energy inevitably requires a pigment system to convert light into chemical energy rather than dissipating into heat. A fundamental but fascinating question is how the “first” pigment appears during the history of evolution.4, 5 Porphyrins are on the biosynthetic pathway to Chl,6 which is viewed to be closely related to the evolution of photosynthesis.7 In a pioneer work, uroporphyrinogen, the first macrocycle intermediate for Chl, was investigated as photocatalysts for H2 evolution under ultraviolet flux, suggesting a possible mechanism for proto‐photosynthesis on the primordial earth.7 Porphyrin molecules can also work as essential building blocks to form high‐level photosynthetic architectures, for example, light‐harvesting antenna8, 9, 10, 11 and photoactive lipid membrane.12, 13 The tetrapyrrole macrocycles have been detected by non‐enzymatical reaction of aminoketone and diketone or ketoester based on pyrroles formation and oligomerizations.14, 15, 16, 17 However, prebiotic synthesis of porphyrin is open to question at least in the context of robust reaction of prebiotic sources in aqueous solution to give a moderate synthesis efficiency.14, 18 Actually porphyrins have been even regarded as an ideal biomarker to search for extraterrestrial life.19 Therefore, experimental construction of a plausible scenario for abiogenesis of primitive photosynthetic architecture coincident with prebiotic conditions still remains a big challenge.

The mixture of Cys and Zn2+ leads to form Cys/Zn microspheres via coordination‐driven self‐organization (Figure S1, Supporting Information), including hydrogen bond‐mediated stacking of coordinated molecular chains into nanorod crystals followed by their hierarchical splitting growth.44 The obtained Cys/Zn microspheres were placed into autoclave to simulate volcanic hydrothermal environment. After hydrothermal treatment of Cys/Zn microspheres below 160 °C (hereafter, 120 °C is taken as an example), scanning electron microscopy (SEM) images show monodispersed microspheres that are composed of nanorods (Figure1a and Figure S2, Supporting Information), suggesting that the hierarchical structure in the Cys/Zn microspheres is preserved. The nanorods are aligned to form an inherent porosity (Figure 1b–d), which may create many nanochannels for chemical entities traveling into the microspheres. High‐resolution transmission electron microscopy (HRTEM) image exhibits a lattice spacing of 0.31 nm on the surface of the nanorods (Figure 1e), which is ascribed to an interplanar distance of the (002) plane of wurtzite ZnS.45 The in situ formed ZnS nanocrystals have sizes within 5 nm (Figure 1e), which may facilitate photocatalytic reactions due to quantum confinement effects.45 The lattice fringes of Cys/Zn microspheres can be observed to be adjacent to that of ZnS (Figure 1e), indicating that the ZnS nanocrystals are deposited on the template of Cys/Zn microspheres. The high angle annular dark‐field scanning TEM (HAADF‐STEM) image and elemental mapping images suggest that the elements of Zn, S, C, and N are uniformly distributed throughout the microspheres (Figure 1f), further proving that the resulting microspheres are derived from the Cys/Zn matrices. The Cys/Zn microspheres retain structure integrity in high temperature (at least 140 °C) and only parts of Cys in the surface are decomposed to mineralize ZnS nanocrystals. This robustness in assembled structure is presumably resulted from multiple synergies of intermolecular coordination and hydrogen bonds.46

In summary, a primitive photosynthetic architecture has been developed based on chemical evolution of Cys and Zn2+ in a volcanic hydrothermal “prebiotic soup.” The assembled Cys/Zn microspheres provide templates and precursors for heat‐driven in situ nucleation of ZnS, resulting in the decoration of ZnS nanocrystals on the nanorods from the hierarchical Cys/Zn framework. CO32− derived from the thermal decomposition of Cys is doped on the surface of ZnS nanocrystals, which makes it responsive to visible light. The ZnS nanocrystals on the Cys‐Zn framework have an architectural principle similar to biological light‐harvesting complex, where proteins work as a template to tune the organization of pigments. The ZnS‐Cys/Zn microspheres can further trigger various photochemical reactions, including H2 evolution, CO2 photoreduction, and NADH regeneration, reminiscent of phototrophic life. Although the prebiotic relevance of some of the molecules used in above reactions (e.g., TEOA, MV2+, K2PtCl4, and NAD+) is questionable, it is confirmed that the ZnS‐Cys/Zn microspheres can indeed induce photochemical process, including light harvesting and charge separation. We note that anaerobic H2 evolution has been considered as a model of proto‐photosynthesis,7, 55 and nonbiological photochemical reduction of NAD+ to NADH may provide an evolutionary link to biochemical reactions.62 Therefore, the ZnS‐Cys/Zn microspheres can be deemed as a primitive pigment model, taken together with their plausible abiogenesis. Besides CO2 photoreduction, ZnS‐Cys/Zn microspheres can potentially drive more strict prebiotic photochemical synthesis due to the strong reduction potential of ZnS, as shown in previous studies.58, 60 This study provides a new perspective of origin of pigment through molecular self‐organization in prebiotic conditions, which help deepen insight into the potential role of adaptive self‐organization during chemical evolution. From the view of applications, the hierarchical ZnS‐Cys/Zn microspheres are capable of guest encapsulation, which may facilitate molecular concentration and multicomponent functional coupling in confined space, for example, photoenzymatic reaction for solar energy conversation. Self‐organization and chemical evolution can not only help understand historical trajectory for origin of life but also may provide a simple but robust strategy to fabricate functional materials with emergent properties in the assistance of “natural creative force.”

Preparation of Cys/Zn Microspheres: Cys was dissolved in ultrapure water by adjusting the pH to ≈12.0 using 1 m NaOH. Zinc chloride (ZnCl2) solution was obtained by dissolving ZnCl2 in ultrapure water. Cys/Zn microspheres were prepared by a direct mixture of Cys solution and ZnCl2 solution. In a typical process, 40 µL of 50 × 10−3m Cys solution was added to 940 µL of ultrapure water, followed by addition of 20 µL of 100 × 10−3m ZnCl2 aqueous solution, and the finial pH was around 8.0. After mixing, the solution became turbid immediately. White precipitates were obtained by centrifugation of the turbid solution at 8000 rpm for 10 min. The precipitates attributed to Cys/Zn microspheres were then washed by ultrapure water to remove free cystine and ZnCl2.

The authors declare no conflict of interest.




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