Ultrafast X-Ray Study Reveals How Protons, Electrons, and Water Move Together

Some of nature’s most important chemical reactions depend on positively charged protons and negatively charged electrons moving together. These reactions power photosynthesis, catalysis, and biological energy conversion, but they happen so quickly that they are extremely difficult to observe.

A research team led by the U.S. Department of Energy’s Pacific Northwest National Laboratory (PNNL), in collaboration with scientists at SLAC National Accelerator Laboratory and several universities, has captured snapshots of these light-driven molecular events.

The findings, published in Nature Communications, could help scientists better understand proton-coupled electron transfer reactions and, ultimately, improve catalysts, fuel cells, flow batteries, and other energy technologies.

How protons and electrons drive energy conversion

The research focuses on the coordinated movement of protons and electrons, a process known as proton-coupled electron transfer, or PCET. This form of energy transfer is among the most efficient mechanisms found in nature. Plants use related processes to capture sunlight and convert it into stored chemical energy during photosynthesis.

When protons and electrons move in concert, molecules can avoid intermediate steps that require additional energy. The result can be a faster and more efficient chemical reaction.

The researchers investigated how changes in a molecule’s electronic structure, the arrival of protons, and rearrangements in the surrounding water environment are connected during PCET reactions.

Capturing a chemical reaction at the molecular level

Scientists have studied proton-coupled electron transfer for decades. However, no previous experiment had captured the process in a single study with both local electronic sensitivity and structural sensitivity.

The team combined advanced X-ray technology at SLAC’s Linac Coherent Light Source (LCLS) with quantum chemical calculations and molecular dynamics simulations. Together, these tools provided a detailed view of how the reaction unfolds.

PNNL experimental chemical physicist Elisa Biasin, former PNNL scientist Abdullah Kahraman, and PNNL theoreticians Niranjan “Nili” Govind and Amity Andersen worked with collaborators to study light-driven PCET reactions.

Using ultrafast X-ray spectroscopy, time-resolved X-ray scattering, and advanced simulations, the researchers captured key steps in the reaction. The structural measurements showed how a molecule’s electronic structure changes at specific locations as it gains protons, while the surrounding water environment reorganizes at the same time.

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

Why proton-coupled electron transfer matters

PCET plays an important role throughout nature. Plants use related processes to absorb and convert light during photosynthesis, while animals rely on similar mechanisms to efficiently convert food into energy. PCET is also involved in many other biological and chemical energy-conversion reactions.

For the experimental system studied here, researchers already understood the basic reaction mechanism. However, important questions remain about other PCET reactions, including the precise timing and sequence of proton and electron transfer.

“Are they happening together or not? At what molecular sites? And how does the water network facilitate proton hops?” Biasin asked. “These are some of the possible open questions. Answering them requires ultrafast temporal resolution, chemical and structural sensitivity, and consistency with theory. We have taken a step forward in answering these questions.”

The new approach allows researchers to investigate these questions more directly. The results show that when molecules acquire protons, local changes in electronic structure occur alongside larger-scale rearrangements in the surrounding water network.

Understanding these linked changes could eventually help scientists design more efficient catalysts, fuel cells, flow batteries, and other energy-storage and energy-conversion technologies.

Tracking electrons, protons, and water

One of the greatest challenges in studying PCET is the speed of the process. Electrons move on extremely short time scales, and protons move at roughly the same speed. Meanwhile, the water molecules surrounding the reacting molecules are constantly moving and rearranging, making them notoriously difficult to observe directly.

Previous experiments had captured individual parts of the process, but they had not provided a complete picture combining electronic changes within a molecule with the reorganization of the surrounding solvent.

To create a system that was easier to interpret, Biasin and her colleagues selected a well-studied ruthenium-based molecule. The molecule absorbs light and, under acidic conditions, captures protons from its surroundings.

“We identified the metal complexes used in this study because they do not undergo additional electronic and structural rearrangements that complicate interpretation of the X-ray signals,” said co-investigator Christopher Larsen, a senior lecturer at the University of Auckland in New Zealand. “This allowed us to separate signals related to electron, proton, and solvent motion.”

The researchers also used time-resolved characterization methods at the University of Geneva to identify the optimal experimental conditions and time scales for the X-ray measurements.

Combining X-ray spectroscopy, scattering, and simulations

To follow the reaction, the team combined two complementary X-ray methods.

Element-specific X-ray absorption spectroscopy, performed with a chemRIXS instrument, revealed how electrons moved between different sites in the molecule. At the same time, time-resolved X-ray scattering using an X-ray Correlation Spectroscopy (XCS) instrument tracked atomic rearrangements, including the movement of solvent molecules around the reaction.

The team also relied on theoretical modeling. Govind contributed time-dependent density functional theory, while Andersen contributed molecular dynamics simulations. These calculations were essential for interpreting the complex X-ray signals and revealing the underlying behavior of electrons and protons.

“To understand the photochemistry of this complex, we needed to push the boundaries of data analysis,” said lead author Abdullah Kahraman, who worked on the project at SLAC while serving as a PNNL postdoctoral fellow. “By combining X-ray absorption spectroscopy with accurate theoretical modeling, we were able to obtain unprecedented observations of the real-time electronic changes that drive these reactions.”

Govind emphasized the importance of the theoretical analysis.

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

What the experiment could not directly observe

Biasin noted that the experiment could not directly detect the protons themselves.

“X-ray scattering primarily looks at electron-rich atoms, so protons are not directly observed,” she said. “However, we are observing local reconfigurations of the electronic structure along with global reconfigurations of the surrounding water network, and we can draw conclusions based on the agreement between our data and calculations.”

Despite this limitation, the combined X-ray approach provides a framework that researchers can apply to 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 time scales,” said Roberto Alonso Mori, a senior scientist at SLAC and co-author of the study. “By combining complementary X-ray techniques at LCLS, this study provides a unique and complete view of these bonding processes, opening new opportunities to understand and ultimately control the chemistry underlying energy conversion and catalysis.”

SLAC staff scientist and co-author David Hoffman said the study is an important first step toward combining X-ray scattering and spectroscopy to investigate complex chemical processes in model systems.

“The increased signal-to-noise ratio provided by the LCLS-II upgrade will allow these techniques to be used to solve real-world problems in catalysis and energy harvesting,” Hoffman said.

Support for the research

This research was supported by the DOE Office of Science, Basic Energy Sciences, Chemical Sciences, Earth Sciences, and Biological Sciences Division through PNNL’s Condensed Phase and Interfacial Molecular Science (CPIMS) Program and Atomic, Molecular, and Optical Sciences (AMOS) Program.

Use of the Linac Coherent Light Source at SLAC National Accelerator Laboratory is supported by the DOE Office of Science. Some of the research was also conducted at the Environmental Molecular Sciences Laboratory, a DOE Office of Science user facility located at PNNL.