Solar-driven carbon dioxide fixation using photosynthetic semiconductor bio-hybrids.

Solar-driven conversion of carbon dioxide to value-added carbon products is an ambitious objective of ongoing research efforts. However, high overpotential, low selectivity and poor CO2 mass transfer plague purely inorganic electrocatalysts. In this instance, we can consider a class of biological organisms that have evolved to achieve CO2 fixation. We can harness and combine the streamlined CO2 fixation pathways of these whole organisms with the exceptional ability of semiconducting nanomaterials to harvest solar energy. A novel nanomaterial-biological interface has been pioneered in which light-capturing cadmium sulfide nanoparticles reside within individual organisms essentially powering biological CO2 fixation by solar energy. In order to further develop the photosensitized organism platform, more biocompatible photosensitizers and cytoprotective strategies are required as well as elucidation of charge transfer mechanisms. Here, we discuss the ability of gold nanoclusters to photosensitize a model acetogen effectively and biocompatibly. Additionally, we present innovative materials including two-dimensional metal organic framework sheets and alginate hydrogels to shield photosensitized cells. Finally, we delve into original work using transient absorption spectroscopy to inform on charge transfer mechanisms

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

Roadmap on semiconductor-cell biointerfaces.

This roadmap outlines the role semiconductor-based materials play in understanding the complex biophysical dynamics at multiple length scales, as well as the design and implementation of next-generation electronic, optoelectronic, and mechanical devices for biointerfaces. The roadmap emphasizes the advantages of semiconductor building blocks in interfacing, monitoring, and manipulating the activity of biological components, and discusses the possibility of using active semiconductor-cell interfaces for discovering new signaling processes in the biological world

Sustainable CO2 valorization by coupling electro- and biocatalysis

The core of the research presented in this dissertation consists of using solar energy to renewably drive the conversion of CO2 and N2 to value-added chemicals, materials, feedstocks, and fuels. Nature has provided a blueprint for capturing and storing solar energy in chemical bonds through photosynthesis. However, our energy demands realistically outmatch the short-term capability of this natural process. Meanwhile, the solar capture ability of semiconductor materials outpaces that of biological organisms. Through my work I have developed photosynthetic biohybrid systems combining the solar capture of semiconductor nanomaterials and the selectivity and low substrate activation of whole cell “living” biocatalysts. Chapter 1 lays out the current state of the field and how it has evolved from the first demonstrations combining semiconductor materials with whole-cell biocatalysts for CO2 fixation. In Chapter 2 I describe an approach to improve the interface between light-active silicon nanowires and Sporomusa ovata (S. ovata), an electrophilic bacterium that converts CO2 into multi-carbon acetate. The silicon nanowires function as a cathode within an electrochemical cell allowing for a superior interface with the bacterial biocatalysts. S. ovata take up electrons at the cathode interface to jumpstart their native CO2 fixing metabolism. Although considerable efforts have been invested to optimize microorganism species and electrode materials separately, the microorganism-cathode interface has not been systematically studied as a function of operational parameters including applied electrochemical potential, electrolyte composition and biocatalyst loading. We found that as a more negative electrochemical potential was applied to an unoptimized system, the CO2-reducing current plateaued resulting from a fragmented bioinorganic interface as the bacteria broke away due to increasing local pH. By mitigating the pH change at the cathode-bacteria interface, we achieved a direct CO2 bioelectrosynthesis current density of 0.65 mA cm-2 with an ~80% faradaic efficiency. Furthermore, when powered with solar light, our platform attained a 3.6% solar-to-chemical efficiency. Acetate represents a valuable multi-carbon product because it can be readily used as a feedstock for a secondary bacterium. By carefully selecting a downstream microorganism, we achieved a broader biomanufacturing platform where acetate serves as a universally upgradeable cornerstone. In Chapter 3, I demonstrate that acetate, the primary product of the nanowire-bacteria biohybrid system, can be used as a feedstock for a secondary bacterial biocatalyst that upgrades the acetate to a biopolyester. This proof-of-concept consists of fueling the generation of biopolymer polyhydroxybutyrate (PHB) by Cupriavidus basilensis with CO2-derived acetate Our bioprocess enables the complete conversion of CO2 to PHB which is to be spun into 3D printing filament material. Although this demonstration contextualizes the ability to upgrade acetate to a material for additive manufacturing, the production rate is too low for successful industrial scaling. Through modeling of the bioprocess, we uncovered the reaction bottleneck to the be the H2 mass transfer from the gas phase to the liquid phase during autotrophic cultivation of S. ovata with CO2 and H2, as reducing substrate. By increasing the H2 mass transfer modestly, the time required to produce the equivalent mass of acetate would decrease by 75%. Furthermore, adapting the design to a flow cell platform would increase productivity two-fold and limit pH imbalances caused by acetate acidification. The sequential biocatalysis approach enables the straightforward downstream conversion of the initial CO2 product acetate to a higher value chemical, fuel, or material by a secondary bacterium. In Chapter 4, I report an advance on this concept by expanding the bioelectrosynthesis beyond CO2 reduction to include N2 reduction. We directly co-culture primary CO2-fixing S. ovata producing acetate with a secondary N2-fixing bacteria in Rhodopseudomonas palustris (R. palustris) that uses the acetate to both fuel N2 fixation and for the generation of a biopolyester. We demonstrate that the co-culture platform provides a robust ecosystem for continuous CO2 and N2 fixation where its outputs are directed by substrate gas composition. Moreover, we show the ability to support the co-culture on a high surface-area silicon nanowire cathodic platform. The biohybrid co-culture achieved peak faradaic efficiencies of at least 100, 19.1, and 6.3% for acetate, nitrogen in biomass and ammonia respectively while maintaining product tunability. Ultimately, this work demonstrates the ability to employ and electrochemically manipulate bacterial communities on demand to expand the suite of CO2 and N2 bioelectrosynthesis products. There are several advantages of bioelectrochemical CO2 fixation over the purely inorganic approach. Bioelectrochemical CO2 fixation offers products that are inaccessible to inorganic electrocatalysis, lower substrate activation energy translating to small overpotentials and the catalysts are self-regenerating and self-repairing. However, inorganic electrocatalysis reduces CO2 at rates that are orders of magnitudes higher. In Chapter 5 I lay out a roadmap to further combine the best attributes of electrocatalysis and the biologically mediated approach. CO2 was electrochemically converted to glycolaldehyde using a copper nanoparticle decorated cathode. Glycolaldehyde served as the key autocatalyst for the formose reaction, where it was combined with formaldehyde in the presence of an alkaline earth metal catalyst to form a variety of C4 - C8 sugars, including glucose. In turn, these sugars were used as a feedstock for fast-growing and genetically modifiable Escherichia coli. By electrocatalytically generating sugars, a high-energy bacterial feedstock, from CO2 we open the door to biomanufacturing with metabolically rapid and flexible microorganism. There are several obstacles to overcome but we introduce a roadmap to push the boundaries of product complexity achievable from CO2 conversion while demonstrating CO2 integration into life-sustaining sugars

Abiotic sugar synthesis from CO2 electrolysis

CO2 valorization is aimed at converting waste CO2 to value-added products. While steady progress has been achieved through diverse catalytic strategies, including CO2 electrosynthesis, CO2 thermocatalysis, and biological CO2 fixation, each of these approaches have distinct limitations. Inorganic catalysts only enable synthesis beyond C2 and C3 products with poor selectivity and with a high energy requirement. Meanwhile, although biological organisms can selectively produce complex products from CO2, their slow autotrophic metabolism limits their industrial feasibility. Here, we present an abiotic approach leveraging electrochemical and thermochemical catalysis to complete the conversion of CO2 to life-sustaining carbohydrate sugars akin to photosynthesis. CO2 was electrochemically converted to glycolaldehyde and formaldehyde using copper nanoparticles and boron-doped diamond cathodes, respectively. CO2-derived glycolaldehyde then served as the key autocatalyst for the formose reaction, where glycolaldehyde and formaldehyde combined in the presence of an alkaline earth metal catalyst to form a variety of C4 - C8 sugars, including glucose. In turn, these sugars were used as a feedstock for fast-growing and genetically modifiable Escherichia coli. Altogether, we have assembled a platform that pushes the boundaries of product complexity achievable from CO2 conversion while demonstrating CO2 integration into life-sustaining sugars