MIT chemists have uncovered a potential reason behind the high efficiency of energy transfer in photosynthetic cells, focusing on purple bacteria as a model. Their study, utilizing ultrafast spectroscopy and cryo-electron microscopy, reveals that the disordered arrangement of light-harvesting proteins enhances energy transduction efficiency. This discovery challenges the notion that biological disorder is a drawback, suggesting instead that it may be an evolutionary advantage for optimal energy transfer. By measuring energy movement between proteins within synthetic nanodiscs, the team found that closer, randomly organized proteins transfer energy faster and more efficiently than those in a structured lattice, shedding light on the mechanisms of near-unity quantum efficiency in photosynthesis.
Gabriela Schlau-Cohen, an associate professor of chemistry at MIT and the senior author of the new study, set aside time to discuss her research with SCINQ.
Could you provide some background on what prompted your participation in this study and where the study originated?
Yes, absolutely. One of the remarkable aspects of photosynthesis, particularly in purple bacteria, is their high quantum efficiency. This efficiency means that almost every photon is converted into an electron. For instance, the quantum efficiency in purple bacteria is around 5%. This is notable when compared to solar cells, which have what is known as the Shockley-Queisser limit of 33% absorption for a single junction.
The reason for this difference lies in the unique design of photosynthetic organisms. They absorb light in one part of their protein architecture and then transport it over distances of 20 to 200 nanometers to the site where electricity is generated. The key to this efficiency is the long-distance energy transduction.
Our interest in this process is twofold. Firstly, we want to understand this efficiency in detail. Secondly, we are considering the implications of how energy can be moved over such long distances in complex biological systems. Understanding this could open up a range of applications, not just in solar energy, but also in the broader field of electronic energy transduction.
Can you explain the significance of near unity quantum efficiency?
Essentially, this refers to the ratio of photons to electrons. Thus, a higher quantum efficiency translates to a greater yield of electrons. In the context of solar energy, or specifically this aspect of photosynthesis, the process involves converting photons into electrons.
Later in the photosynthetic process, these electrons, along with the corresponding ‘holes’ or deficits of electrons, are utilized to drive biochemical reactions. However, in the case of a solar cell, the primary function is the conversion of photons directly into electrons.
How does that influence energy transfer in photosynthesis?
In photosynthesis, achieving high quantum efficiency requires efficient energy transfer. Essentially, the process encompasses absorption, long-distance energy transfer, and charge separation. The characteristics of absorption and the kinetics of charge separation are relatively well understood. However, the aspect of long-distance energy transfer had been a significant gap in the field. Our study focused on investigating this particular element.
What inspired the team to use purple bacteria, specifically? What was the allure?
Purple bacteria, first and foremost, exhibit a particularly high quantum efficiency in photosynthesis, higher than what we see in oxygenic photosynthesis in plants. In plants, the quantum efficiency is somewhat lower, around 85%, compared to about 95% in purple bacteria. Therefore, if our goal is to explore a paradigm of high quantum efficiency, purple bacteria represent an ideal choice. Additionally, purple bacteria have been a model system for studying photosynthesis for decades. This historical context makes them an excellent starting point when we aim to extend our understanding to new aspects of the problem.
Are there any other organisms that are equally efficient?
Green sulfur bacteria also exhibit a high quantum efficiency, and they possess a unique architecture. Some of these bacteria are believed to live at the bottom of the ocean, surviving on photons from geothermal events. They often thrive in extreme environments, classifying them as extremophiles. Our objective was to understand this behavior in such robust environments, which are somewhat analogous to those that humans may encounter or create.
Can you explain how the light harvesting proteins LH2 and LH3 differ? Why were they chosen for the study?
Yes, indeed. To delve a bit deeper into the specific aspect of long-distance energy transduction that we examined, let’s consider how energy transfer occurs over distances. This process involves energy transfer within a protein and then between proteins. The transfer within a protein has been extensively studied, with hundreds of papers written over decades. However, our focus was on the energy transfer between proteins, which we believe is crucial. To achieve extensive distance coverage, the energy cannot be confined to just one protein.
In our study of energy transfer between proteins, we utilized LH2 and LH3. These proteins are from the same organism, with LH3 being a low-light variant of LH2. Under low-light conditions, LH3 is expressed, differing from LH2 by just a few amino acids.
Does everything occur at the nanoscale?
Yes, that’s completely correct. Everything we’re discussing occurs on the nanoscale, specifically at the protein level. This is a stark contrast to cell-based or organism-based experiments. It necessitates a significant shift in our thinking, both in terms of length and time scales, as we are dealing with dimensions and processes that are orders of magnitude smaller and more intricate.
As you may know, factors like weather, clouds, and shadows can impact light availability. In response to low light conditions, purple bacteria undergo a shift from expressing LH2 to expressing LH3. While LH3 is a similar protein to LH2, it differs slightly in its amino acid composition. This difference alters the wavelength of light they absorb, enabling them to more effectively utilize the available light.
The reason we chose these two proteins for our study is due to their similar structural properties and how they interact with energy. However, their ability to absorb different wavelengths of light is crucial. This variance in energy absorption allowed us to use laser-based spectroscopy for our measurements. With this technique, we could observe energy transfer from one protein to the other, as they operate at slightly different energy levels.
Can you explain the significance of you embedding those proteins?
Absolutely. As you’ve likely noticed, this study is highly interdisciplinary. Our primary technique was ultrafast spectroscopy, which involves pulses a millionth of a billionth of a second long, enabling high-resolution laser spectroscopy. We also utilized cryo-electron microscopy (cryo-EM) for structural determination. Crucially, what made all this possible was a biotechnological tool called a nanodisc.
The reason why previous studies couldn’t access this key step of energy moving from one protein to another was due to a focus on two different extremes. On one hand, studies looked at a single protein in detergent, a soap-like substance used to purify individual proteins. This approach inherently doesn’t allow observation of energy moving from one protein to another. On the other hand, studies examined the intact membrane, where you have many proteins of unknown identity, making it unclear how far apart they are or where the energy is going.
What we achieved was the reconstitution of a reduced system, a ground-up construction with only these two proteins within a near-native membrane. This nanodisc technology, developed 10-20 years ago and finding increasingly broad applications, involves a discoidal lipid bilayer that mimics native membranes. Within this, we can embed proteins and control the number of proteins embedded, as we build it from the ground up. This entire structure is stabilized by a belt that naturally interacts with lipids on one side, allowing integration into the experimental setup on the other side.
How closely do they compare to the real thing?
That’s an excellent question. In many ways, we don’t fully understand what the actual biological system looks like. This situation provides an opportunity for both a top-down approach to figure out what’s present and a bottom-up approach for assembly. The real biological system is a native lipid bilayer, and in our study, we use native lipids, altering the lipid composition to mimic the natural environment as closely as possible.
However, the complexity of the actual system is significant. For example, lipid compositions can vary under different growth conditions or between species. In our model, we’ve managed to retain the key features relevant to our study while also having the flexibility to introduce different molecular factors.
It’s important to note that in the real biological setting, there are other proteins we aren’t examining here, both within the membrane and soluble within the cell, which interact in various ways. Many aspects of the natural environment aren’t incorporated into our model. Nevertheless, we view our approach as a way to work with a reduced system that maintains the essential elements of our investigation. From here, we can gradually introduce more complexity and examine additional interactions and aspects in future studies.
What did the results indicate regarding energy transfer this distance?
We were successful in determining the energy transfer timescales for two different distances. These experimental benchmarks enabled us to construct a theoretical description of energy transfer for these proteins as a function of distance. We observed a good agreement between our experimental values and the theoretical description. This achievement was made possible with the collaboration of another professor at MIT and a professor at the University of Nevada, Las Vegas.
Our approach allowed us to develop a detailed understanding of energy transfer between proteins relative to their distance. We found the most accurate representation using a model that combines both near-field and far-field effects. This is because the interactions between proteins vary significantly depending on their proximity. When proteins are very close, the interactions differ from when they are farther apart. By integrating these two models, we achieved good agreement with our experimental data, providing a comprehensive view of how energy transfer scales with distance.
In previous studies, researchers had only made approximations in this regard. So, I’ll make sure this point is clear before discussing the broader implications for energy transfer across membranes.
Using the timescales we established, we were able to delve deeper into the concept of long-distance energy transduction. As I mentioned earlier, energy moves across distances ranging from 20 to 200 nanometers, often involving multiple energy transfer steps. Previous studies, focusing on intact systems, recovered a timescale at the much shorter end of our spectrum. This approach failed to accurately capture the long-distance energy transfer across the various distances present in a membrane.
We constructed a simulation using our timescales for long-distance energy transfer. Initially, we used a lattice model, where all proteins are equidistant, reflecting previous models and common design thinking in system organization. This model predicted a single timescale. However, when we introduced heterogeneity, incorporating the different timescales we measured, we discovered that this leads to enhanced energy transport efficiency.
Our findings suggest that a disordered organization, rather than a well-ordered one, results in more efficient energy transduction. This is particularly exciting because biological systems are inherently warm, wet, and noisy. In contrast, when designing material systems, there’s a tendency to aim for well-organized, perfectly ordered structures. Our results indicate that the disorder commonly seen in biological systems isn’t just an accidental feature, but rather an advantageous one for efficient energy transfer.
Indeed, there is an ‘ordering within the disorder.’ There’s a structural organization present even amidst what appears to be disorderly. What I’m referring to in terms of order is a kind of regularity in spacing, akin to a crystal structure. We found that as soon as you disrupt this regularity, you start to see benefits. The fundamental physics behind this phenomenon is that the time required for energy transfer scales nonlinearly with distance. So, when some protein pairs are placed in close proximity, the benefits are amplified significantly because the energy transfer process becomes much faster.
What did you find most surprising? What did you find most surprising about the energy transfer time?
What we found most surprising is that previous measurements in heterogeneous membranes had focused only on the closely spaced protein pairs. This indicates that there was a lack of understanding regarding the broader energy transfer through the entire protein network. Essentially, researchers had characterized only the fastest energy transfer step, neglecting the various other energy transfer steps that occur.
This realization motivated us to investigate long-distance energy transduction. Our goal was to understand the disproportionate role played by these closely spaced protein pairs in the overall energy transfer process.
How does energy transfer? How does that relate to the overall efficiency of the photosynthetic process?
That’s an excellent question. Essentially, the moment a photon is absorbed, a timer starts. You have about three nanoseconds before the light energy is lost due to radiative processes, such as fluorescence. This means that the light energy can only be retained for a few nanoseconds.
For instance, if you aim for a 90% quantum efficiency, the entire process must be completed within 100 picoseconds. This includes all the energy transfer steps and charge separation. So, it’s a ‘use it or lose it’ system, where the relationship between time and efficiency is crucial.
Can you sort of speculate on the implications of your findings on how we understand biological systems?
I believe what’s fundamentally exciting and broadly applicable about our findings is the new understanding of protein behavior within membranes. These proteins are constantly fluctuating and diffusing, always in motion. Our discovery that a disordered organization, which is inevitable due to thermal motion and diffusion, can actually be beneficial, is quite profound.
This insight suggests a general principle that might be relevant to other protein networks. Many proteins form organizations and networks, and the idea that their fluctuations and movements could be advantageous is potentially fundamental to basic biology.
What are the broader implications for this outside of biology? You mentioned solar cells and its energy transfer, etc.
I think when discussing alternative energy sources, it’s clear that solar cells are effective and worthy of investment, but we’ll also need additional solutions. For example, there’s talk of designing materials that can absorb light on a window and then transport that light through a photonic circuit to generate electricity. For such materials to be practical, they need to be easy to apply and synthesize on a macroscale. In this context, achieving a single crystal structure is not feasible.
Therefore, understanding how disorder can be beneficial for long-distance energy transfer could be invaluable for the design of these types of materials. This knowledge could lead to the development of more efficient and practical energy-harvesting systems.
IMAGE CREDIT: Gabriela S. Schlau-Cohen.
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