Exploring Delocalised Energy Transport in Bacterial Reaction Centres

Photosynthetic organisms such as plants, algae and bacteria, harness the energy from sunlight to drive all downstream processes such as synthesis of carbohydrates, which are essential for cell growth, function, and repair. Reaction centres (RCs) play the pivotal role of accepting energy absorbed by 1000s of light absorbing carotenoid and (bacterio)chlorophyll molecules and use it to induce charge separation, generating electrons (and holes). Electrons are then used to form a vital concentration gradient of protons that drive adenosine triphosphate synthesis. The process of initial light capture in light harvesting antenna, rapid energy transfer between (bacterio)chlorophyll molecules and charge separation in RCs is, remarkably, 100% efficient under low light intensities. Despite many prior studies of RCs, several important factors underling the high yield of chemical charge separation have yet to be directly experimentally determined.

RCs of Rhodobacter sphaeroides contain seven tightly packed light absorbing molecules: four bacteriochlorophylls-a, two bacteriopheophytins-a (both bacteriochlorin pigments) and a 15,15'-cis-spheroidene carotenoid moiety. Energy transfer between adjacent RC pigments takes place on ~100 fs timescales (1 fs = one millionth billionth of a second).

The rate of energy transfer, which underpins the yield of eventual charge-separation, is dictated by the electronic structure of RCs, and the extent to which photoexcited molecules share electrons (delocalisation). In the regime of spatially separated molecules, the interaction between chormophores is minimal and electrons remain localised on their respective molecules. However, in RCs the distances between pigments ranges between 5 and 10 Angstroms and through inter-molecular interactions electrons can become delocalised over multiple pigments. To date, no experiment has been able to directly measure the delocalisation of RC excited states.

Ultrafast laser spectroscopies using pulses of light shorter than the dynamical processes involved can be used to take snapshots of the system and infer the route(s) and associated timescales of energy flow through the system. One such emerging technique, two-dimensional electronic-vibrational spectroscopy will be used to investigate the spatial location of excited states in RCs as a function of time, and transform our knowledge of the inter-molecular interactions and of the RC electronic structure.

Carotenoid pigments play a dual role in photosynthesis, acting as both accessory light harvesting pigments and regulatory elements that can protect plants from damage caused by excessive sunlight. In their light harvesting capacity, they can absorb parts of the solar spectrum where (bacterio)chlorophyll absorption is weak. Carotenoids increase the total coverage of the solar spectrum by transferring energy to (bacterio)chlorophyll molecules. The carotenoid to bacteriochlorin energy transfer mechanisms for RCs have not been fully characterised and may involve pathways that have hitherto been ignored. Two-dimensional electronic spectroscopy will be used to follow the energy transfer between carotenoid and different bacteriochlorin pigments, revealing the energy transfer pathways and associated timescales that enhance the light harvesting capability of RCs.

The proposed experiments seek to transform our current description of the electronic structure of Rhodobacter sphaeroides RCs and how energy is transferred between constituent light absorbing molecules, preparing the system for one of nature's most efficient charge-carrier generation events. The study will provide key design principles of inter-molecular couplings in RCs, and unravel the blueprint for the efficient energy transduction. These design principles will be key for engineering bio-inspired molecular solar cell technology or water splitting catalysts.

The immediate beneficiaries from this grant will primarily be academic research groups exploring the molecular mechanisms of efficient natural light harvesting and those trying to synthesise molecular artificial reaction centres. Quantitative information about several key parameters is required to understand natural reaction centres or synthesise bio-inspired counterparts: these parameters include the precise inter-nuclear distances between chromophores, isolated constituent pigment excitation energies and the inter-pigment electronic coupling constants. The latter factors are difficult to determine independently, and values have only been estimated by a combination of semi-empirical theory and experiments. This coupling dictates the energy transfer between moieties and the degree of delocalisation of excitons over multiple pigments. This study aims to unravel these details with cutting-edge ultrafast laser spectroscopies, which will provide one of the missing design principles required to build a reaction centre from the ground up.

The proposed research will also introduce expertise in advanced ultrafast spectroscopies to the UK and disseminate it through training of highly skilled personnel and collaborative research. The postdoctoral research associate (PDRA) employed by this grant will be trained and will gain expertise in cutting edge spectroscopies at the frontier of biophysics. The PDRA will directly collaborate with a group who grow bacterial reaction centres (Dr Mike Jones in the School of Biochemistry at Bristol). The PDRA will benefit from being part of the Bristol Laser Chemistry, Spectroscopy and Dynamics Group who have a broad range of scientific interests. She/he will also have many opportunities for interactions with researchers in the fields of computational and theoretical chemistry. The collegiate scientific atmosphere in the School of Chemistry will facilitate broad training for a PDRA that will equip her/him with the necessary skills to face the next stages of her/his career.

The longer-term impact of the proposed research will be to use the design principles of nature's reaction centre to engineer efficient and robust molecular based solar cell technologies, where a high yield of charge-separation is key. The findings may also influence solar driven water-splitting catalysts that require a reliable source of electrons to drive water oxidation. The proposed research will contribute to impacts envisaged for the EPSRC research themes in Energy, Physical Sciences and Manufacturing the Future and is aligned with EPSRC Grand Challenge: Understanding the Physics of Life.