Physical Biology of the Materials-Microorganism Interface.

Future solar-to-chemical production will rely upon a deep understanding of the material-microorganism interface. Hybrid technologies, which combine inorganic semiconductor light harvesters with biological catalysis to transform light, air, and water into chemicals, already demonstrate a wide product scope and energy efficiencies surpassing that of natural photosynthesis. But optimization to economic competitiveness and fundamental curiosity beg for answers to two basic questions: (1) how do materials transfer energy and charge to microorganisms, and (2) how do we design for bio- and chemocompatibility between these seemingly unnatural partners? This Perspective highlights the state-of-the-art and outlines future research paths to inform the cadre of spectroscopists, electrochemists, bioinorganic chemists, material scientists, and biologists who will ultimately solve these mysteries

Bacteria photosensitized by intracellular gold nanoclusters for solar fuel production.

The demand for renewable and sustainable fuel has prompted the rapid development of advanced nanotechnologies to effectively harness solar power. The construction of photosynthetic biohybrid systems (PBSs) aims to link preassembled biosynthetic pathways with inorganic light absorbers. This strategy inherits both the high light-harvesting efficiency of solid-state semiconductors and the superior catalytic performance of whole-cell microorganisms. Here, we introduce an intracellular, biocompatible light absorber, in the form of gold nanoclusters (AuNCs), to circumvent the sluggish kinetics of electron transfer for existing PBSs. Translocation of these AuNCs into non-photosynthetic bacteria enables photosynthesis of acetic acid from CO2. The AuNCs also serve as inhibitors of reactive oxygen species (ROS) to maintain high bacterium viability. With the dual advantages of light absorption and biocompatibility, this new generation of PBS can efficiently harvest sunlight and transfer photogenerated electrons to cellular metabolism, realizing CO2 fixation continuously over several days

Cyborgian Material Design for Solar Fuel Production: The Emerging Photosynthetic Biohybrid Systems.

Photosynthetic biohybrid systems (PBSs) combine the strengths of inorganic materials and biological catalysts by exploiting semiconductor broadband light absorption to capture solar energy and subsequently transform it into valuable CO2-derived chemicals by taking advantage of the metabolic pathways in living organisms. In this work, we first traverse through a brief history of recent PBSs, demonstrating the modularity and diversity of possible architectures to rival and, in many cases, surpass the performance of chemistry or biology alone before envisioning the future of these hybrid systems, opportunities for improvement, and its role in sustainable living here on earth and beyond

Cysteine-Cystine Photoregeneration for Oxygenic Photosynthesis of Acetic Acid from CO2 by a Tandem Inorganic-Biological Hybrid System.

Tandem "Z-scheme" approaches to solar-to-chemical production afford the ability to independently develop and optimize reductive photocatalysts for CO2 reduction to multicarbon compounds and oxidative photocatalysts for O2 evolution. To connect the two redox processes, molecular redox shuttles, reminiscent of biological electron transfer, offer an additional level of facile chemical tunability that eliminates the need for solid-state semiconductor junction engineering. In this work, we report a tandem inorganic-biological hybrid system capable of oxygenic photosynthesis of acetic acid from CO2. The photoreductive catalyst consists of the bacterium Moorella thermoacetica self-photosensitized with CdS nanoparticles at the expense of the thiol amino acid cysteine (Cys) oxidation to the disulfide form cystine (CySS). To regenerate the CySS/Cys redox shuttle, the photooxidative catalyst, TiO2 loaded with cocatalyst Mn(II) phthalocyanine (MnPc), couples water oxidation to CySS reduction. The combined system M. thermoacetica-CdS + TiO2-MnPc demonstrates a potential biomimetic approach to complete oxygenic solar-to-chemical production