Peter J. Dahl

Wet adhesives that perform under water have broad applications in industrial and biomedical settings. To date, molecular designs for underwater adhesives have largely been inspired by marine animals including mussels and barnacles. Here, we propose bacterial biofilms as an alternative source of inspiration for underwater adhesives. Specifically, we demonstrate the application potential of a peptide derived from biofilms formed by the notorious pathogen Vibrio cholerae . We characterize the ability of this biofilm-derived peptide to adsorb onto various surfaces and to glue wet surfaces by using a combination of confocal microscopy, molecular dynamics simulations, atomic force microscopy, lap shear tests, and spectroscopic tools. We further show that the peptide can coaggregate with microspheres acting as an effective flocculant. Our results open new design possibilities for underwater adhesives inspired by natural biofilms.

Clostridium pasteurianum [FeFe]-hydrogenase II (CpII) is distinguished by having a ~103-fold preference for catalyzing the H2 oxidation reaction over H2 production. Here we used electron paramagnetic resonance and infrared spectroscopy to identify catalytic intermediates and role of the accessory [4Fe-4S] clusters in electron transport. In the resting state, CpII consisted of an oxidized, Hox, H-cluster and diamagnetic accessory F-clusters. Under reduction with H2, CpII converted to a singly reduced H-cluster, or Hred, whereas chemical reduction led to a mixture of Hred and the two-electron, super-reduced, Hsred, state. Exchange of a conserved proton-transfer cysteine for serine led to increased levels of Hsred. Analysis of the magnetic properties of reduced CpII revealed extensive spin-coupling among the F-clusters, and between F-clusters and the Hsred H-cluster state. We propose that the H2 oxidation bias in CpII is a synergistic outcome of the H-cluster electronic structure and spin-coupling to favor H2 binding and oxidation.

Photochemical reduction reactions catalyzed by nanocrystals (NCs) and enzymes require both electron transfer (ET) and hole transfer (HT) reactions to occur in spatial and temporal proximity. As a result, the observed photochemical reaction rates are complex functions of many competing ET and HT reactions. To facilitate interpretation of complex photochemical datasets, we developed a model that simultaneously evaluates the rates of both the reduction and oxidation reactions. We applied this model to electron-intensive reduction of dinitrogen to ammonia by CdS NCs and nitrogenase MoFe protein. A fit of the model to the kinetics of product accumulation determined that during prolonged illuminations the efficiency of N2 reduction was limited by MoFe protein oxidation, facilitated by the accumulation of the products of the oxidation reaction. Modeling time-resolved populations of catalytic intermediates revealed variability in the rates of reduction, indicating that accumulation of hydrides and N2 activation influenced the rates of electron transfer.

Developing systems that can efficiently capture photon energy and convert this energy into fuels and chemicals requires understanding how to assemble molecular components with diverse functions into complete systems possessing selectivity and efficiency in directing charge carriers to catalytic reactions. There are many challenges to achieving this goal. One promising approach is the development of hybrid systems that combine semiconductor nanocrystals (NCs) for light capture and enzymes as efficient catalysts. Such biohybrid systems capitalize on the tunable electronic and optical properties of NCs while leveraging the unmatched specificity and efficiency of enzymes in catalyzing chemical reactions, thereby offering opportunities to surpass the limitations of each component alone. Here, we focus on recent progress in developing a biohybrid system that combines CdS NCs for photon capture with the enzyme nitrogenase to accomplish light-driven dinitrogen (N₂) reduction to ammonia (NH₃). Integrating light-harvesting materials with biological catalysts requires a deep understanding of NC properties, protein stability, and electron transfer (ET), making it an inherently multidisciplinary problem. The reduction of N₂ to NH₃ is a challenging reaction, with a high demand in both agriculture and industrial chemical production. This reaction is intrinsically energy intensive, due to the need to activate the N≡N triple bond. The current standard industrial approach to N₂ reduction, the Haber–Bosch reaction, obtains the necessary energy input from fossil fuels, whereas biological systems capable of N₂ reduction utilize the hydrolysis of ATP as their energy source. Replacing these costly, energy-intensive inputs with renewable light energy represents a critical step toward sustainable NH₃ production. Recent progress has demonstrated that semiconductor CdS NCs can be coupled to the catalytic component of nitrogenase, the MoFe protein, to form a biohybrid CdS NC:MoFe protein complex, enabling light-driven N₂ reduction rather than energy input from fossil fuels or ATP. This illustrates how inorganic NCs can functionally replace the natural Fe protein partner, yielding a biohybrid catalyst that enables controlled electron delivery and provides not only light-driven NH₃ production but also new approaches for probing enzyme catalytic function. The CdS NC:MoFe protein biohybrid system enables light-initiated electron delivery at ambient temperature, as well as temperatures below freezing, allowing for stabilization and spectroscopic characterization of key reaction intermediates. These findings highlight how photochemical biohybrids can serve as both functional catalysts and mechanistic probes. Beyond studies of the nitrogenase mechanism, studies of the CdS NC:MoFe system reveal how variables such as NC size, electrostatic binding interactions, and sacrificial electron donors (SEDs) govern complex stability, charge transfer efficiency, and catalytic performance. In addition, studies of nitrogenase and the high activation barrier for N₂ reduction are enabling investigations of new and interesting questions regarding the properties and limitations of NC biocatalysis. In this Account, we describe the key features of CdS NC:MoFe protein biohybrids and the parameters for optimal light-driven N₂ reduction, and how controlling ET with light illuminates the path to new insights into the nitrogenase mechanism.

Electron transfer in cytochrome OmcZ and OmcS "nanowires" is explored computationally by integrating the quantum-mechanical stochastic Liouville equation with fluctuating energies and interaction matrix elements obtained from molecular-dynamics simulations and including a detailed treatment of vibronic coupling. Electron density oscillates between adjacent hemes very rapidly relative to thermal equilibration. These oscillations last for about 1.5 ns, which is long enough for a coherent wave of electron density to travel ∼60 Å, more than the length of the proteins' subunits. The calculated rates of electron flow underestimate the measured rates but reproduce the finding that long-range diffusion of electrons is significantly faster in OmcZ than in OmcS.

Although proteins are considered as nonconductors that transfer electrons only up to 1 to 2 nanometers via tunneling,Geobacter sulfurreducenstransports respiratory electrons over micrometers, to insoluble acceptors or syntrophic partner cells, via nanowires composed of polymerized cytochrome OmcS. However, the mechanism enabling this long-range conduction is unclear. Here, we demonstrate that individual nanowires exhibit theoretically predicted hopping conductance, at rate (>10¹⁰s⁻¹) comparable to synthetic molecular wires, with negligible carrier loss over micrometers. Unexpectedly, nanowires show a 300-fold increase in their intrinsic conductance upon cooling, which vanishes upon deuteration. Computations show that cooling causes a massive rearrangement of hydrogen bonding networks in nanowires. Cooling makes hemes more planar, as revealed by Raman spectroscopy and simulations, and lowers their reduction potential. We find that the protein surrounding the hemes acts as a temperature-sensitive switch that controls charge transport by sensing environmental perturbations. Rational engineering of heme environments could enable systematic tuning of extracellular respiration.