PNNL

Key Takeaways 

• Researchers captured how a molecule absorbs light and gains a proton while its watery environment reorganizes in response.
• The new multimodal X-ray approach opens new opportunities to study how molecular structure and solvent environments work together during chemical transformations important for biological and energy-conversion processes.

RICHLAND, Wash. — Some of nature’s most important chemical reactions rely on the coupled movement of negatively and positively charged particles. These processes play central roles in photosynthesis, catalysis and biological energy conversion yet remain difficult to observe. 

Now, a research team led by the Department of Energy’s Pacific Northwest National Laboratory, in collaboration with colleagues at SLAC National Accelerator Laboratory and several academic labs, has captured snapshots of these events that are triggered when light strikes a molecule. 

The findings, published in Nature Communications, could help researchers better understand and ultimately design better flow batteries, fuel cells and catalysts. 

The research team focused on the coupled movement of positively charged particles called protons with negatively charged electrons. This coordinated energy transfer is among the most efficient known to exist and in plants is used to capture the sun’s energy and convert it into stored energy, among other processes in nature. 

By moving electrons and protons in a coordinated fashion, molecules can bypass energetically costly intermediate steps. This makes reactions faster and dramatically more energy efficient. In this case, the research team focused on how changes in a molecule’s electronic structure, the addition of a proton and the surrounding water environment are linked during the reaction. 

A first look 

Despite studying this interplay for decades, no one had previously captured it in a single study, with local and structural sensitivity. Advanced X-ray methods available at the Linac Coherent Light Source at SLAC, combined with state-of-the-art quantum chemistry calculations and molecular dynamics simulations, gave unprecedented insight into this crucial process. 

PNNL experimental chemical physicist Elisa Biasin, former PNNL scientist Abdullah Kahraman and PNNL theorists Niranjan (Niri) Govind and Amity Andersen, together with their collaborators, used a combination of ultrafast X-ray spectroscopy, scattering and advanced simulations to capture key steps in a light-driven proton-coupled electron transfer reaction, or PCET. This combined approach reveals for the first time with structural sensitivity how gaining a proton reshapes a molecule’s electronic structure at specific sites and reorganizes the surrounding water environment. 

“We have captured for the first time how electronic changes associated with proton transfer are coupled to reorganization of the surrounding solvent,” said Biasin. “This gives us a new way to understand how molecules and their environments evolve together during fundamental chemical transformations.” 

Why this reaction matters 

PCET is a workhorse in nature, allowing plants to harvest light for photosynthesis and animals to efficiently metabolize food for energy, among other essential energy-conversion processes. In the experimental system the team focused on here, the basic mechanism is well understood. 

However, in some PCET reactions, there continues to be debate about the order of movement among protons and electrons. 

“Are they happening together or not? At which molecular site? And how is the water network facilitating the proton hop?” Biasin asked. “These are some of the possible open questions. To answer them, you need ultra-fast time resolution, chemical and structural sensitivity, and alignment with theory. We have made a step forward to shed light on these questions." 

This new approach helps answer these questions. The study reveals how local changes in electronic structure are coupled with reorganization of the surrounding water network as the molecule gains a proton. By enabling researchers to probe these coupled molecular changes, the approach could help guide the design of more efficient catalysts, fuel cells, flow batteries and other energy-conversion technologies. 

Multiple techniques, one story 

Electrons move on timescales that make them difficult to track, and protons move almost as quickly. The water molecules bathing the reacting molecules reorganize themselves in ways that are notoriously difficult to observe directly. Until now, experiments could provide pieces of the picture but not a combined view of molecular electronic changes and reorganization. 

To design the experiment, Biasin and her collaborators started with a well-studied ruthenium-based molecule that absorbs light and, in acidic conditions, captures a proton from the surroundings. 

“We identified the metal complex used in this study because it does not undergo additional electronic and structural rearrangements that complicate interpretation of X-ray signals, allowing us to isolate signals associated with the electron, proton and solvent motion,” said Christopher Larsen, a co-investigator and senior lecturer at the University of Aukland, New Zealand. 

The research team then used time-resolved characterization techniques available at the University of Geneva to determine the optimal conditions and timescales for the X-ray experiments. 

To watch it in action, the team paired element-specific X-ray absorption spectroscopy from the chemRIXS instrument, which reveals how electrons move between molecular sites, with time-resolved X-ray scattering from the X-ray Correlation Spectroscopy (XCS) instrument, which tracks the rearrangement of atoms, including the motions of solvent molecules. 

The project then drew on the complementary theoretical expertise of Govind and Andersen. They performed time-dependent density functional theory and molecular dynamics simulations, respectively, that were essential for interpreting the complex signals produced by the X-ray measurements and revealing the underlying proton-electron dynamics. 

First author Abdullah Kahraman said the combination of techniques was crucial to the findings.

"Understanding the photochemistry of this complex required us to push the limits of our data analysis. By combining X-ray absorption spectroscopy with precise theoretical modeling, we gained an unprecedented look into the real-time electronic changes driving these reactions,” said Kahraman, who worked on the project at SLAC while he was a PNNL postdoctoral associate.

Govind highlighted the theoretical aspect of the research.

“While this was an experiment-driven discovery, our theoretical work provided the molecular-level interpretation needed to translate the X-ray measurements into a detailed picture of the underlying coordination between proton, electron and solvent motion.” 

Biasin notes that the study is limited in that the team could not directly observe the proton. 

“X-ray scattering mostly sees atoms that are rich with electrons, and so the proton is not seen directly," she said. “But we observe the local reorganization of the electronic structure, together with the global reorganization of the water networks, and we can draw conclusions based on the agreement between data and calculations." 

Nonetheless, the multimodal X-ray technique lays out a framework that other researchers can now use to study PCET reactions in more complex chemical systems. 

“Many of the most important chemical reactions involve electrons, protons, and their surrounding environment moving together on ultrafast timescales,” said Roberto Alonso Mori, senior scientist at SLAC and a coauthor on the study. “By combining complementary X-ray techniques at LCLS, this work provides a uniquely complete view of these coupled processes, opening new opportunities to understand and ultimately control the chemistry that underpins energy conversion and catalysis.” 

Coauthor and SLAC staff scientist David Hoffman added, “This is an important first step in combining X-ray scattering and spectroscopy to study these complicated processes in a model system. With the better signal-to-noise offered by the LCLS-II upgrade, we can use these methods to solve real problems in catalysis and energy harvesting.” 

A full list of authors and institutions is available in the published manuscript.  

This research was supported by the DOE Office of Science, Basic Energy Sciences, Chemical Sciences, Geosciences, and Biosciences Division, through the Condensed Phase and Interfacial Molecular Science (CPIMS) program and the Atomic, Molecular, and Optical Sciences (AMOS) program at PNNL. Use of the Linac Coherent Light Source at SLAC National Accelerator Laboratory is supported by the DOE Office of Science. A portion of the research was conducted at the Environmental Molecular Sciences Laboratory, a DOE Office of Science user facility located at PNNL.