Decades-old photosynthesis mystery finally solved

Their research reveals why the first movements of electrons, which are crucial for transferring energy, occur through only one side of a key protein-pigment structure. The findings were published in the Proceedings of the National Academy of Sciences.

Photosynthesis is a sequence of reactions in which electrons pass between multiple pigment molecules. Although it has been examined for decades, the process remains difficult to fully explain because it involves numerous intricate components, operates at extremely fast timescales, and varies slightly across different species. Gaining a deeper understanding of these steps could help scientists develop efficient artificial systems, such as synthetic leaves and solar-based fuel technologies, that replicate nature's design.

In most life forms that use photosynthesis, the process begins with a protein-pigment complex known as Photosystem II (PSII). This complex captures sunlight and splits water molecules, releasing oxygen and sending electrons onward to other molecules in the chain of energy transfer.

PSII contains two nearly identical branches, known as D1 and D2, surrounded by four chlorophyll molecules and two related pigments called pheophytins. These are symmetrically arranged and connected to electron carriers known as plastoquinones. In theory, electrons should move from chlorophyll to pheophytin and then to plastoquinone along both branches.

However, experiments have consistently shown that electrons move only through the D1 branch -- a finding that has baffled scientists for years. "Despite the structural symmetry between the D1 and D2 protein branches in PSII, only the D1 branch is functionally active," explains Aditya Kumar Mandal, the study's first author and a PhD student in the Department of Physics at IISc.

To investigate this imbalance, the team combined molecular dynamics simulations, quantum mechanical analyses, and Marcus theory (a Nobel Prize-winning model that describes how electrons are transferred) to chart the energy patterns in both pathways. "We assessed the electron transfer efficiency step-by-step through both D1 and D2 branches," says Shubham Basera, PhD student in the Department of Physics and one of the authors.

The team found that the D2 branch has a much higher energy barrier, which makes electron transport energetically unfavourable. Specifically, the transfer of electrons from pheophytin to plastoquinone in D2 requires twice as much activation energy as D1 -- a barrier that electrons seem unable to overcome, preventing energy from flowing forward.

The researchers also simulated the current-voltage characteristics of both branches and found that the resistance against electron movement in D2 was two orders of magnitude higher than that in D1.

The asymmetry in electron flow may also be influenced by subtle differences in the protein environment around the PSII and how the pigments are embedded in it, the researchers suggest. For example, the chlorophyll pigment in D1 has an excitation state at a lower energy than its D2 counterpart, suggesting that the D1 pigment has a better chance of attracting and transferring electrons.

The researchers also suggest that tweaking some of these components can boost or rewire electron flow across PSII. For example, swapping chlorophyll and pheophytin in D2 could overcome the electron block, because chlorophyll needs lower activation energy than pheophytin.

"Our research presents a significant step forward in understanding natural photosynthesis," says Prabal K Maiti, Professor at the Department of Physics and one of the corresponding authors of the study. "These findings may help design efficient artificial photosynthetic systems capable of converting solar energy into chemical fuels, contributing to innovative and sustainable renewable energy solutions."

This is a beautiful combination of theory at various levels to address a long-standing problem culminating in a new level of understanding, but still leaving mysteries to be challenged, says Bill Goddard, Professor at Caltech and one of the corresponding authors.