Evolution of the Fenna-Matthews-Olson Complex and Its Quantum Coherence Features. Which Led the Way?

Few scientific questions are as intriguing and at the same time as relevant as those about the origin of life on Earth. Even fewer present-day phenomena are as related to its answer as that of photosynthesis and its origin. Even though photosynthesis is more commonly perceived as pertaining to the realm of biology, actually quantum molecular physics is the discipline most suitable to explore the transformation of electromagnetic energy into stored chemical energy and how living organisms evolved in order to take advantage of this energy transformation mechanism. The research article by Valleau and Aspuru-Guzik[1] reported in ACS Central Science is a testimony to the far-reaching lengths that both seemingly opposite scientific disciplines can go when working closely together to elucidate the influence that quantum phenomena exert over the evolution of an autotrophic organism—specifically, the evolution of the Fenna–Matthews–Olson (FMO) complex, a trimeric pigment–protein complex which lies between the antennae complexes and the reaction center of the photosystem II of sulfur green bacteria, and whose primary function is to serve as a molecular wire transporting the excitons generated during light harvesting by the pigments toward the reaction center where the cascade of redox chemical reactions take place. The excitation energy transfer dynamics are required to be fast or otherwise it is lost; it is now known that this transport occurs with quantum coherence;[2,3] that is, very little energy is dissipated as heat or radiation, making it an almost 100% efficient process. But how exactly did the FMO complex evolve to exhibit this remarkable feature of quantum coherence? Or even more puzzling, how did quantum coherence lead the evolution of FMO?

Learning about the evolution of the FMO complex of bacteria can further our understanding of photosynthesis more generally. Image credit: © Can Stock Photo Inc., Ruslan117.

Previous investigations about the evolution of the FMO complex through the study of their quantum photochemical properties have stemmed from the idea that the quantum coherence displayed by it is already at a maximum, and in fact it has been reported that the quantum entanglement is indeed maximum in two pathways along the seven bacteriochlorophyll-a molecules in a single monomer.[4] But even if the structure of the current FMO is optimal for the quantum coherent transport of excitons, the question of how it got to be so remains unanswered. Since finding fossil records of a unicellular organism containing an early FMO structure is next to impossible, earlier versions or ancestors, had to be constructed backward by performing a series of mutations on the reported structure of FMO found in P. aestuari and Chlorobium tepidium, a remarkable feat on its own right. Through this careful examination of FMO’s amino acid sequence, the authors were not only able to generate a phylogenetic tree for the complex, but also they were able to evaluate the structural robustness of the ancestors built by calculating changes in folding free energy of the enveloping protein. The quantum properties related to the quantum coherence present in the excitonic transport mechanism were later calculated and compared to those observed in present-day FMO-containing organisms; if the phylogenetic tree is truthful then at some point the resemblance in the spectra would be lost and the pathway up the tree would be discarded. From the absorption spectra simulations, it seems that the ancestors under study are more closely related to C. tepidium than to P. aestuari; however, it remains to be seen if the phylogenetic tree is fully covered or if all possibilities for its branching have been fully accounted; most likely, a higher climb up the tree is still needed.

Much work lies ahead in the research of the evolution of this fascinating complex and its quantum properties of excitonic transport, but also about the role of the enveloping protein in the photoprotection of the pigments and the evolution of their specific arrangement as well as its influence on relative orientation of the seven pigments, and even answering why seven and not six pigment molecules are needed. Computational chemistry offers an advantageous standpoint to assess the earlier forms of the FMO complex and the more sophisticated algorithms currently available—such as neural networks and machine learning techniques—will prove useful in generating a more plausible line of ascent for this organ and others involved in photosynthesis and any other biochemically relevant process; however these studies can only be fruitful with an interdisciplinary approach such as the one performed in this paper.

The study of photosynthesis continues to be a broad topic of research for various disciplines; it is not only the study of the origin of life but also of its evolution, from bacteria to plants and the animals who are nourished from them. Let us remember that cyanobacteria changed the chemical composition of Earth’s atmosphere and its climate through oxygenic photosynthesis during the Cambrian period roughly two and a half billion years ago in what is known as the oxygen catastrophe, a not-so-catastrophic event that cannot happen again soon enough.