Evidence for high efficiency of photosynthesis

Dr. Neil Canter, Contributing Editor | TLT Tech Beat December 2017

Electron transfer moves in the forward direction only because it is discouraged from moving backward.

KEY CONCEPTS
• The reason that photosynthesis is very efficient is that the electrons generated rarely move backward.
• Using a combination of experiments and modeling, researchers determined that the backward process known as the recombination reaction takes place in the inverted region where it is inhibited during photosynthesis.
• The experimental data was obtained at low temperature where only the recombination reaction occurs. 

ATTEMPTS TO HARNESS SOLAR ENERGY are continuing, and the efficiency of man-made processes continues to improve. A recent TLT article discussed the development of a photoelectrochemical cell that achieved a quantum efficiency over 100% in the ultraviolet-visible light range (1). Researchers used a method known as multiple exciton generation that enables an electrode in the photoelectrochemical cell to extract additional energy that might otherwise be lost as heat. This enables one photon to generate multiple electrons instead of just one.

But the ultimate goal of solar cell research is to develop an approach that generates a comparable efficiency to photosynthesis. Gary Hastings, professor in the department of physics and astronomy at Georgia State University in Atlanta, Ga., says, “The quantum efficiency of photosynthesis as determined by the conversion seen in photosystem I is 98%.”

Photosystem I is a large pigment-protein complex that spans the thylakoid membrane in the chloroplast of a green plant where photosynthesis occurs. When photosystem I is exposed to light, electrons are generated. Hastings says, “Electrons hop from one pigment to another across the thylakoid membrane. The transferred electron is used to power carbon dioxide reduction and its eventual incorporation into glucose.”

Hastings adds, “Electron transfer leads to one side of the membrane being positive, the other negative, much like the terminals of a battery. The biomolecular light-induced battery in this case leads to fuel production rather than electricity.

He further says, “Once the electron starts on its forward trek across the thylakoid membrane, it will rarely move backward. In contrast, electrons produced in artificial solar devices often seem to move backward by participating in so-called recombination reactions, which results in a loss of the captured solar energy and decreased efficiency.” 

Hastings says, “The question therefore is: Why are natural systems that use photosynthesis so efficient? A potential answer is that the recombination reaction can occur in the so-called inverted region where it will be inhibited, allowing forward electron transfer to dominate.”

The status of an electron in the inverted region is shown in Figure 3. The electron is at a certain energy state and can either move downhill back to its original ground state, which is what occurs in the recombination reaction, or move uphill to continue on its forward pathway to reducing carbon dioxide.


Figure 3. In photosynthesis an electron in the inverted region does not choose the recombination reaction, which is downhill, but rather moves uphill to continue the process to reduce carbon dioxide. (Figure courtesy of Georgia State University.)

Hastings says, “The electron chooses not to go downhill, which may seem a bit counterintuitive as this would seem to be the less thermodynamically favored process. A theory predicting inverted region electron transfer was initially proposed by professor Rudolph Marcus in 1954 for which he received the Nobel Prize in chemistry in 1992.”

Inverted region electron transfer has been suggested to be important in leading to high efficiency in photosynthetic electron transfer, but experimental confirmation has not been reported until now. 

TIME-RESOLVED SPECTROSCOPY
Hastings and his colleagues used a combination of experimental data, kinetic modeling and electron transfer theory to demonstrate that the recombination reaction in photosystem I does take place in the inverted region. The researchers confirmed Marcus’ theory by using a photosystem I from the cyanbacterium Synechocystis sp. PCC 6803. Hastings says, “This organism carries out photosynthesis in the same manner as green plants. We used it in our study because this cyanobacterium is easier to modify and grow.”

As mentioned above, the electron hops via a series of pigments across the thylakoid membrane. One of these pigments is a quinone molecule. In Hastings’ experiments, modifications of the electron transfer chain were made by exchanging the native quinone for eight slightly different quinones. By using multiple quinones, the researchers can determine different driving forces and electron transfer rates enabling them to put together a Marcus curve, which shows the logarithm of the electron transfer rate versus the driving force. The data points for the recombination reaction were found to occur in the inverted region for all of the quinones evaluated, including the natural one. 

The experimental data was obtained using time-resolved visible and FTIR spectroscopy. Measurements were undertaken at room temperature (298 K) and at low temperature (77 K). Hastings says, “All of the electron transfer reactions are dependent not only on the structure of the quinones but also on temperature. At room temperature, measurements are difficult because there are many competing reactions occurring. At low temperature, however, forward electron transfer is inhibited and only the recombination reaction that is of interest occurs.”

Through computational modeling, the researchers determined that if the recombination reaction did not occur in the inverted region, then the quantum efficiency of photosynthesis would drop from above 98% to 72%. 

Future work for the researchers will involve evaluating the electron transfer properties of photosystem I with additional quinones incorporated. Hastings says, “So far we have primarily worked with napthoquinones because they are most easily incorporated into the photosystem I electron transfer chain. Other quinones such as benzoquinone and anthraquinone derivatives will be incorporated and studied.”

The researchers also intend to evaluate the electron transfer rate at all temperatures between 77 K and 298 K. 

Hastings believes that his research findings will be helpful to develop more efficient artificial solar cells capable of reducing a variety of molecular species that can be used to enable a multitude of chemical reactions, including, for example, carbon dioxide reduction or even hydrogen production. 

Additional information can be found in a recent article (2) or by contacting Hastings at ghastings@gsu.edu. 

REFERENCES
1. Canter, N. (2017), “Photoelectrochemical generation of hydrogen over 100% quantum efficiency,” TLT, 73 (8), pp. 12-13.
2. Makita, H. and Hastings, G. (2017), “Inverted-region electron transfer as a mechanism for enhancing photosynthetic solar energy conversion efficiency,” Proceedings of the National Academy of Sciences, 114 (35), pp. 9267-9272.


Neil Canter heads his own consulting company, Chemical Solutions, in Willow Grove, Pa. Ideas for Tech Beat can be submitted to him at neilcanter@comcast.net.