Tracking energy transfer between light harvesting complex 2 and 1 in photosynthetic membranes grown under high and low illumination

Abstract

Energy transfer (ET) between B850 and B875 molecules in light harvesting complexes LH2 and LH1/RC (reaction center) complexes has been investigated in membranes of Rhodopseudomonas palustris grown under high-and low-light conditions. In these bacteria, illumination intensity during growth strongly affects the type of LH2 complexes synthesized, their optical spectra, and their amount of energetic disorder. We used a specially built femtosecond spectrometer, combining tunable narrowband pump with broadband white-light probe pulses, together with an analytical method based on derivative spectroscopy for disentangling the congested transient absorption spectra of LH1 and LH2 complexes. This procedure allows real-time tracking of the forward (LH2 → LH1) and backward (LH2 ← LH1) ET processes and unambiguous determination of the corresponding rate constants. In low-light grown samples, we measured lower ET rates in both directions with respect to high-light ones, which is explained by reduced spectral overlap between B850 and B875 due to partial redistribution of oscillator strength into a higher energetic exciton transition. We find that the low-light adaptation in R. palustris leads to a reduced elementary backward ET rate, in accordance with the low probability of two simultaneous excitations reaching the same LH1/RC complex under weak illumination. Our study suggests that backward ET is not just an inevitable consequence of vectorial ET with small energetic offsets, but is in fact actively managed by photosynthetic bacteria.bacteriochlorophylls | ultrafast spectroscopy

Tracing of backward energy transfer from LH1 to LH2 in photosynthetic membranes grown under high and low irradiation.

“…The availability of both equilibration dynamics and the population ratio in equilibrium allows us to unambiguously determine both forward and backward ET rate constants. We find that in LL membranes backward ET is strongly reduced with respect to HL samples [4]. In the biological context, this finding is corroborated by the fact that LH1 → LH2 backward ET allows an exciton to reach various LH1 complexes during its lifetime.…”

Adaptation of Rhodopseudomonas acidophila strain 7050 to growth at different light intensities: what are the benefits to changing the type of LH2?

“…This type of approach has already been used. 35 However, what is really needed is an experimental protocol that is to be able to image the organisation of the LH complexes in individual membrane patches and which is then able to measure the energy transfer just from those small imaged regions. This approach would be able to avoid averaging over different arrangements of the LH complexes and thus would remove a lot of the current ambiguity.…”

Emergent Properties in Locally Ordered Molecular Materials

“…These rings serve the dual purpose of creating an energy gradient-increased coupling and number of chromophores in the larger rings redshift the excitonic spectra-and forming a structure that can robustly couple with neighboring antennae structures independent of their relative orientation. [108,121,124] The situation is even more remarkable for green bacteria, which possess dedicated organelles called chlorosomes that house 10 3 -10 5 self-assembling bacteriochlorophyll molecules. [110,123] Operating at heroically low photon fluxes (some of these bacteria survive by utilizing the black body radiation of thermal vents [125] ), large rod assemblies of bacteriochlorophylls funnel excitons over lengths of 10-100 nm using energy gradients of about 0.1-0.2 eV.…”

“…Because photoexcitations follow energy gradients from high to low energy, this excess energy is currency for unidirectional energy transfer toward the reaction center. [104] Depending on the bacterial species and growth conditions, [121] there are anywhere from hundreds [108] to hun- Figure 5. Schematic depiction of typical antenna complexes in purple bacteria.…”

“…In the context of photosynthesis, excitons are used as an intermediary to shuttle distant photoexcitations toward the photosynthetic machinery. [104,121] The pathways followed by the exciton are provided by chromophores and protein composites called "antennae complexes". In well-studied antennae complexes, such as those found in purple [108,122] and green bacteria, [110,123] light is absorbed at a higher energy than the actual redox potential required for catalysis ( Figure 5).…”