Photosynthesis, the basis of life on Earth, is based on the capacity a living organism has of capturing solar energy and transform it into chemical energy through the synthesis of macromolecules like carbohydrates. Despite the fact that most of the molecular processes present in most photosynthetic organisms (plants, algae and even some bacteria) are well described, the mechanism of energy transference from the light harvesting molecules to the reaction centers are not entirely known. Therefore, in our lab we have set ourselves to study the possibility of some excitonic transference mechanisms between pigments (chlorophyll and its corresponding derivatives). It is widely known that the photophysical properties of chlorophylls and their derivatives stem from the electronic structure of the porphyrin and it is modulated by the presence of Mg but its not this ion the one that undergoes the main electronic transitions; also, we know that Mg almost never lies in the same plane as the porphyrin macrocycle because it bears a fifth coordination whether to another pigment or to a protein that keeps it in place (Figure 1).
During our calculations of the electronic structure of the pigments (Bacteriochlorophyll-a, BChl-a) present in the Fenna-Matthews-Olson complex of sulfur dependent bacteria we found that the Mg²⁺ ion at the center of one of these pigments could in fact create an intermolecular interaction with the C=C double bond in the phytol fragment which lied beneath the porphyrin ring.
This would be the first time that a dihapto coordination is suggested to occur in any chlorophyll and that on itself is interesting enough but we took it further and calculated the photophysical implications of having this fifth intramolecular dihapto coordination as opposed to a protein or none for that matter. Figure 3 shows that the calculated UV-Vis spectra (calculated with Time Dependent DFT at the CAM-B3LYP functional and the cc-pVDZ, 6-31G(d,p) and 6-31+G(d,p) basis sets). A red shift is observed for the planar configuration, respect to the five coordinated species (regardless of whether it is to histidine or to the C=C double bond in the phytyl moiety).
Before calculating the UV-Vis spectra, we had to unambiguously define the presence of this observed interaction. To that end we calculated to a first approximation the C-Mg Wiberg bond indexes at the CAM-B3LYP/cc-pVDZ level of theory. Both values were C(1)-Mg 0.022 and C(2)-Mg 0.032, which are indicative of weak interactions; but to take it even further we performed a non-covalent interactions analysis (NCI) under the Atoms in Molecules formalism, calculated at the M062X density which yielded the presence of the expected critical points for the η²Mg-(C=C) interaction. As a control calculation we performed the same calculation for Magnoscene just to unambiguously assign these kind of interactions (Fig 4, bottom).
This research is now available at the International Journal of Quantum Chemistry. A big shoutout and kudos to Gustavo “Gus” Mondragón for his work in this project during his masters; many more things come to him and our group in this and other research ventures.
Recently, the journal ACS Central Science asked me to write a viewpoint for their First Reactions section about a research article by Prof. Alán Aspuru-Guzik from Harvard University on the evolution of the Fenna-Matthews-Olson (FMO) complex. It was a very rewarding experience to write this piece since we are very close to having our own work on FMO published as well (stay tuned!). The FMO complex remains a great research opportunity for understanding photosynthesis and thus the origin of life itself.
In said article, Aspuru-Guzik’s team climbed their way up a computationally generated phylogenetic tree for the FMO from different green sulfur bacteria by creating small successive mutations on the protein at a time while also calculating their photochemical properties. The idea is pretty simple and brilliant: perform a series of “educated guesses” on the structure of FMO’s ancestors (there are no fossil records of FMO so this ‘educated guesses’ are the next best thing) and find at what point the photochemistry goes awry. In the end the question is which led the way? did the photochemistry led the way of the evolution of FMO or did the evolution of FMO led to improved photochemistry?
Since both the article and viewpoint are both published as open access by the ACS, I wont take too much space here re-writing the whole thing and will instead exhort you to read them both.
Thanks for doing so!
If you work in the field of photovoltaics or polyacene photochemistry, then you are probably aware of the Singlet Fission (SF) phenomenon. SF can be broadly described as the process where an excited singlet state decays to a couple of degenerate coupled triplet states (via a multiexcitonic state) with roughly half the energy of the original singlet state, which in principle could be centered in two neighboring molecules; this generates two holes with a single photon, i.e. twice the current albeit at half the voltage (Fig 1).
It could also be viewed as the inverse process to triplet-triplet annihilation. An important requirement for SF is that the two triplets to which the singlet decays must be coupled in a 1(TT) state, otherwise the process is spin-forbidden. Unfortunately (from a computational perspective) this also means that the 3(TT) and 5(TT) states are present and should be taken into account, and when it comes to chlorophyll derivatives the task quickly scales.
SF has been observed in polyacenes but so far the only photosynthetic pigments that have proven to exhibit SF are some carotene derivatives; so what about chlorophyll derivatives? For a -very- long time now, we have explored the possibility of finding a naturally-occurring, chlorophyll-based, photosynthetic system in which SF could be possible.
But first things first; The methodology: It was soon enough clear, from María Eugenia Sandoval’s MSc thesis, that TD-DFT wasn’t going to be enough to capture the whole description of the coupled states which give rise to SF. It was then that we started our collaboration with SF expert, Prof. David Casanova from the Basque Country University at Donostia, who suggested the use of Restricted Active Space – Spin Flip in order to account properly for the spin change during decay of the singlet excited state. A set of optimized bacteriochlorophyll-a molecules (BChl-a) were oriented ad-hoc so their Qy transition dipole moments were either parallel or perpendicular; the rate to which SF could be in principle present yielded that both molecules should be in a parallel Qy dipole moments configuration. When translated to a naturally-occurring system we sought in two systems: The Fenna-Matthews-Olson complex (FMO) containing 7 BChl-a molecules and a chlorosome from a mutant photosynthetic bacteria made up of 600 Bchl-d molecules (Fig 2). The FMO complex is a trimeric pigment-protein complex which lies between the antennae complex and the reaction center in green sulfur dependent photosynthetic bacteria such as P. aestuarii or C. tepidium, serving thus as a molecular wire in which is known that the excitonic transfer occurs with quantum coherence, i.e. virtually no energy loss which led us to believe SF could be an operating mechanism. So far it seems it is not present. However, for a crystallographic BChl-d dimer present in the chlorosome it could actually occur even when in competition with fluorescence.
I will keep on blogging more -numerical and computational- details about these results and hopefully about its publication but for now I will wrap this post by giving credit where credit is due: This whole project has been tackled by our former lab member María Eugenia “Maru” Sandoval and Gustavo Mondragón. Finally, after much struggle, we are presenting our results at WATOC 2017 next week on Monday 28th at poster session 01 (PO1-296), so please stop by to say hi and comment on our work so we can improve it and bring it home!
It is with great pride that I’d like to announce that for the first time we have a Masters Student graduated from this Comp.Chem. lab: María Eugenia “Maru” Sandoval-Salinas has finished her graduate studies and just last Friday defended her thesis admirably earning not only the degree of Masters of Science in Chemistry but doing so with the highest honors given by the National Autonomous University of Mexico.
Maru’s thesis is for many reasons a landmark in this lab not only because it is the first graduate thesis published from our lab but also the first document on our work about the study of Photosynthesis, a long sought after endeavor now closer to publication. It must also be said that Maru came to this lab when she was an undergraduate student five years ago when I just recently joined UNAM as a researcher fresh out of a postdoc stay. After getting her B.Sc. degree and publishing an article in JCTC (DOI: 10.1021/ct4004178) she now is about to publish more papers that I’m sure will be as highly ranked as the previous one. Thus, Maru was a pioneer in our lab giving it a vote of confidence when we had little to nothing to show for; thanks to her hard work and confidence, along with that of the students who have followed her, we managed to succeed as a consolidated research group in the field of computational chemistry.
More specifically, her thesis centered around finding a mechanism for the excitonic transference between pigments (bacteriochlorophyl-a, BChl-a) in the Fenna-Matthews-Olson (FMO) complex, a protein trimer with seven BChl-a molecules in each monomer, located between the antenna complex and the reaction center in green sulfur bacteria. Among the possible mechanisms explored were Förster’s theory, a modification to Marcus’ theory and finally we explored the possibility of Singlet Fission occurring between adjacent molecules with the help of Dr. David Casanova from the Basque Country University where Maru took a short research stay last autumn. Since nature doesn’t conform to any specific mechanism -specially in a complex arrangement such as the FMO- then it could be possible that a combination of the above might also occur but lets just wait for the papers to be published to discuss it. Calculations were performed through the TD-DFT and the C-DFT formalisms using G09 and Q-Chem; comparing experimental data in CH3OH (SMD implicit calculations with the SVWN5 functional) were undertaken previously for selection of the level of theory.
Now, after two original theses written and successfully defended, an article published in JCTC and more in process, at least five posters, a couple of oral presentations and countless hours at her desk, Maru will go pursuit a PhD abroad where I’m sure she will exceed anyone’s expectations with her work, drive, dedication and scientific curiosity. Thank you, Maru, for all your hard work and trust when this lab needed it the most, we wish you the best for you earn it. You will surely be missed.
Last week at the congress of the Mexican Society of Chemistry I presented some of our results in the study of photosynthesis. Below I embeded the talk. Unfortunately for the wider audience of this blog, the talk is in Spanish (if anyone out there is willing to make subtitles for it I’ll hire you on the spot!)
The slides are also in Spanish although they should be easier to follow for non-Spanish speakers and they are uploaded in SlideShare at this link.
A big thank you to Maria Eugenia “Maru” Sandoval for all the hard work and time invested in this project!
Thanks for clicking!