Electron ‘track switch’ sheds light on photosynthesis

Researchers have reversed electrons’ course in the reaction center of photosynthetic bacteria—advancing understanding of the earliest light-driven events of photosynthesis.

Photosynthetic organisms have a switch point that’s similar to a split in train tracks where a train always goes right. After sunlight is absorbed, energy transfers rapidly to a protein called the reaction center. From this point, the electrons could move either to an A-branch (or “right-track”) set of molecules, or to a B-branch (“left-track”) set of identical molecules.

“In the bacterial reaction center, an electron goes to the A-branch of molecules 100% of the time. We have made it go to the B-branch molecules 90% of the time,” says Christine Kirmaier, research professor of chemistry at Washington University in St. Louis.

“After all, if you think you understand how the train and the tracks work, why shouldn’t you be able to make the train go to the left rather than the right? That’s essentially what we’ve done,” Kirmaier says.

“Why two tracks have evolved is still an open question, but the ability to control which track is utilized is exciting,” says lead author Philip D. Laible, a biophysicist in the biosciences division at Argonne National Laboratory.

“We would like to make the switching between them a more well understood phenomenon so that we could readily conduct electrons (pardon the pun) to any destination in a biological process,” he says. “Right now, we are controlling features that allows for electrons to transverse a biological membrane—the first step in making energy from sunlight in this organism.”

A side vs. B side

Plants, algae, and photosynthetic bacteria convert the energy of sunlight into charge-separated units that they use to power life processes on Earth. And they do it in a very specific way: The reaction centers in these organisms feature two mirror image-like arrangements of protein and pigment cofactors, the A and B sides. Only one of these chains is active—the A side—while the B side is silent.

Kirmaier, with collaborator Dewey Holten, a professor of chemistry, and the team at Argonne National Laboratory have designed many iterations of photosynthetic mutants with the goal of achieving charge separation using the B branch instead. The new research re-engineers a pathway in a purple photosynthetic bacteria, one of nature’s solar cells.

“Using molecular biology, we’ve been changing the amino acids around the pigments to try and find the magic combination to make the B branch work,” she says.

The game was to make structural changes that detune, or make less optimal, electron transfers along the A side or normal path—and then, at the same time, speed up the reactions along the B side.

The researchers were able to step up this trial-and-error process by testing all possible amino acids at a specific target site on the A or B side, finding one or more that improve the B-side yield. They then carried that “hit” forward in the mutant background to probe the next target site, and so on.

“It was unexpected,” Kirmaier says. “We picked a site, and in one of our best mutant backgrounds, placed all 20 amino acids there—and one of them gave us a 90% yield.”

“This is a breakthrough achievement and something that [everyone in] the field has been actively trying to figure out for decades—ever since we first set eyes on the two tracks in a high-profile structural study in Nature nearly 35 years ago,” says co-lead author Deborah K. Hanson of the biosciences division at Argonne National Laboratory.

Rethinking photosynthesis

The new work illuminates basic structure-function principles that govern efficient, light-induced electron transfer.

This knowledge can aid design of biohybrid and bioinspired systems for energy conversion and storage, the researchers say. The findings also will provoke additional experiments and analysis.

“The results raise lots of questions about what is required to get unidirectional charge separation,” Holten says.

In nature, purple bacteria do initial charge separation with a two-step process that takes place in several trillionths of a second. But the team’s new B-branch solution gets almost the same yield, even though it uses a tandem one-step process that takes 5-10 times longer.

“In the original history of photosynthesis, maybe such a combination of a fast two-step and slower one-step processes gave a 80 or 90% yield—and then, over time, it optimized,” Holten says.

The findings appear in the Proceedings of the National Academy of Sciences. Funding for the research came from the US Department of Energy.

Source: Washington University in St. Louis

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