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.

Studying bacteria-nanostructure interactions is crucial to gaining controllable interfacing of biotic and abiotic components in advanced biotechnologies. For bioelectrochemical systems, tunable cell-electrode architectures offer a path toward improving performance and discovering emergent properties. As such, Sporomusa ovata cells cultured on vertical silicon nanowire arrays formed filamentous cells and aligned parallel to the nanowires when grown in increasing ionic concentrations. Here, we propose a model describing the kinetic and the thermodynamic driving forces of bacteria-nanowire interactions.

The apparent incongruity between the increasing consumption of fuels and chemicals and the finite amount of resources has led us to seek means to maintain the sustainability of our society. Artificial photosynthesis, which utilizes sunlight to create high-value chemicals from abundant resources, is considered as the most promising and viable method. This Minireview describes the progress and challenges in the field of artificial photosynthesis in terms of its key components: developments in photoelectrochemical water splitting and recent progress in electrochemical CO2 reduction. Advances in catalysis, concerning the use of renewable hydrogen as a feedstock for major chemical production, are outlined to shed light on the ultimate role of artificial photosynthesis in achieving sustainable chemistry.

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.

Improving natural photosynthesis can enable the sustainable production of chemicals. However, neither purely artificial nor purely biological approaches seem poised to realize the potential of solar-to-chemical synthesis. We developed a hybrid approach, whereby we combined the highly efficient light harvesting of inorganic semiconductors with the high specificity, low cost, and self-replication and -repair of biocatalysts. We induced the self-photosensitization of a nonphotosynthetic bacterium, Moorella thermoacetica, with cadmium sulfide nanoparticles, enabling the photosynthesis of acetic acid from carbon dioxide. Biologically precipitated cadmium sulfide nanoparticles served as the light harvester to sustain cellular metabolism. This self-augmented biological system selectively produced acetic acid continuously over several days of light-dark cycles at relatively high quantum yields, demonstrating a self-replicating route toward solar-to-chemical carbon dioxide reduction.

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.

Semi-artificial photosynthetic systems aim to overcome the limitations of natural and artificial photosynthesis while providing an opportunity to investigate their respective functionality. The progress and studies of these hybrid systems is the focus of this forward-looking perspective. In this Review, we discuss how enzymes have been interfaced with synthetic materials and employed for semi-artificial fuel production. In parallel, we examine how more complex living cellular systems can be recruited for in vivo fuel and chemical production in an approach where inorganic nanostructures are hybridized with photosynthetic and non-photosynthetic microorganisms. Side-by-side comparisons reveal strengths and limitations of enzyme- and microorganism-based hybrid systems, and how lessons extracted from studying enzyme hybrids can be applied to investigations of microorganism-hybrid devices. We conclude by putting semi-artificial photosynthesis in the context of its own ambitions and discuss how it can help address the grand challenges facing artificial systems for the efficient generation of solar fuels and chemicals.

The rise of inorganic-biological hybrid organisms for solar-to-chemical production has spurred mechanistic investigations into the dynamics of the biotic-abiotic interface to drive the development of next-generation systems. The model system, Moorella thermoacetica-cadmium sulfide (CdS), combines an inorganic semiconductor nanoparticle light harvester with an acetogenic bacterium to drive the photosynthetic reduction of CO₂ to acetic acid with high efficiency. In this work, we report insights into this unique electrotrophic behavior and propose a charge-transfer mechanism from CdS to M. thermoacetica Transient absorption (TA) spectroscopy revealed that photoexcited electron transfer rates increase with increasing hydrogenase (H₂ase) enzyme activity. On the same time scale as the TA spectroscopy, time-resolved infrared (TRIR) spectroscopy showed spectral changes in the 1,700-1,900-cm^-1 spectral region. The quantum efficiency of this system for photosynthetic acetic acid generation also increased with increasing H₂ase activity and shorter carrier lifetimes when averaged over the first 24 h of photosynthesis. However, within the initial 3 h of photosynthesis, the rate followed an opposite trend: The bacteria with the lowest H₂ase activity photosynthesized acetic acid the fastest. These results suggest a two-pathway mechanism: a high quantum efficiency charge-transfer pathway to H₂ase generating H₂ as a molecular intermediate that dominates at long time scales (24 h), and a direct energy-transducing enzymatic pathway responsible for acetic acid production at short time scales (3 h). This work represents a promising platform to utilize conventional spectroscopic methodology to extract insights from more complex biotic-abiotic hybrid systems.

Direct solar-powered production of value-added chemicals from CO2 and H2O, a process that mimics natural photosynthesis, is of fundamental and practical interest. In natural photosynthesis, CO2 is first reduced to common biochemical building blocks using solar energy, which are subsequently used for the synthesis of the complex mixture of molecular products that form biomass. Here we report an artificial photosynthetic scheme that functions via a similar two-step process by developing a biocompatible light-capturing nanowire array that enables a direct interface with microbial systems. As a proof of principle, we demonstrate that a hybrid semiconductor nanowire-bacteria system can reduce CO2 at neutral pH to a wide array of chemical targets, such as fuels, polymers, and complex pharmaceutical precursors, using only solar energy input. The high-surface-area silicon nanowire array harvests light energy to provide reducing equivalents to the anaerobic bacterium, Sporomusa ovata, for the photoelectrochemical production of acetic acid under aerobic conditions (21% O2) with low overpotential (η < 200 mV), high Faradaic efficiency (up to 90%), and long-term stability (up to 200 h). The resulting acetate (∼6 g/L) can be activated to acetyl coenzyme A (acetyl-CoA) by genetically engineered Escherichia coli and used as a building block for a variety of value-added chemicals, such as n-butanol, polyhydroxybutyrate (PHB) polymer, and three different isoprenoid natural products. As such, interfacing biocompatible solid-state nanodevices with living systems provides a starting point for developing a programmable system of chemical synthesis entirely powered by sunlight.