Scientists finally see how nature moves energy so efficiently

A team led by the Department of Energy's Pacific Northwest National Laboratory, working with researchers at SLAC National Accelerator Laboratory and several universities, has now captured snapshots of these events after they are triggered by light striking a molecule.

The findings, published in Nature Communications, could deepen scientists' understanding of these reactions and eventually contribute to improved flow batteries, fuel cells and catalysts.

At the center of the study is the coordinated motion of positively charged protons and negatively charged electrons. This type of energy transfer is among the most efficient known in nature. Plants use related processes to capture energy from sunlight and convert it into stored chemical energy.

When electrons and protons move in a coordinated way, molecules can avoid intermediate steps that would otherwise require more energy. That can make a reaction both faster and much more efficient. The researchers investigated how changes in a molecule's electronic structure, the arrival of a proton and shifts in the surrounding water environment are connected during this process.

Capturing a Reaction at the Molecular Level

Scientists have studied this interaction for decades, but no previous experiment had captured the process in a single study with both local and structural sensitivity. Advanced X-ray techniques at the Linac Coherent Light Source at SLAC, combined with state-of-the-art quantum chemistry calculations and molecular dynamics simulations, provided an unusually detailed view.

PNNL experimental chemical physicist Elisa Biasin, former PNNL scientist Abdullah Kahraman and PNNL theorists Niranjan (Niri) Govind and Amity Andersen worked with collaborators to study a light-driven proton-coupled electron transfer reaction, or PCET.

The team combined ultrafast X-ray spectroscopy, X-ray scattering and advanced simulations to capture important stages of the reaction. For the first time with structural sensitivity, the researchers were able to show how a molecule's electronic structure changes at specific locations as it gains a proton, while the surrounding water environment reorganizes at the same time.

"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 Proton-Coupled Electron Transfer Matters

PCET plays an important role throughout nature. Plants rely on it during photosynthesis to harvest light, while animals use related processes to efficiently convert food into energy. It is also involved in many other forms of biological and chemical energy conversion.

For the particular experimental system examined in this study, researchers already understand the basic mechanism. But many questions remain about other PCET reactions, especially the precise timing and order in which electrons and protons move.

"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."

The new method gives researchers a way to investigate those questions more directly. The results show that local changes in electronic structure occur alongside a broader rearrangement of the surrounding water network as the molecule gains a proton.

Being able to examine these connected changes could eventually help researchers design more efficient catalysts, fuel cells, flow batteries and other technologies for converting and storing energy.

Following Electrons, Protons and Water

One major challenge is speed. Electrons move on extremely short timescales, and protons move nearly as fast. At the same time, water molecules surrounding the reacting molecules constantly shift and reorganize in ways that are notoriously difficult to observe directly.

Previous experiments could capture individual parts of this process, but they could not provide a combined picture of both the electronic changes inside the molecule and the reorganization occurring around it.

To create a system that would be easier to interpret, Biasin and her colleagues selected a well-studied ruthenium-based molecule. The molecule absorbs light and, in acidic conditions, captures a proton from its 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 researchers next used time-resolved characterization methods at the University of Geneva to identify the best experimental conditions and timescales for the X-ray measurements.

Combining X-Ray Techniques With Simulations

To track what happened during the reaction, the team combined two complementary X-ray methods.

Element-specific X-ray absorption spectroscopy using the chemRIXS instrument showed how electrons moved between different molecular sites. Meanwhile, time-resolved X-ray scattering from the X-ray Correlation Spectroscopy (XCS) instrument tracked how atoms rearranged, including the motion of solvent molecules around the reaction.

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

First author Abdullah Kahraman said the combination of methods was essential.

"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."

One Important Limitation

Biasin noted that the experiment could not directly observe the proton itself.

"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."

Even with that limitation, the combined X-ray approach provides a framework that researchers can now apply to PCET reactions in more complicated 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."

Support for the Research

The 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. Part of the research was also conducted at the Environmental Molecular Sciences Laboratory, a DOE Office of Science user facility located at PNNL.